BGBiogeosciencesBGBiogeosciences1726-4189Copernicus PublicationsGöttingen, Germany10.5194/bg-13-3585-2016Water column biogeochemistry of oxygen minimum zones in the eastern tropical
North Atlantic and eastern tropical South Pacific oceansLöscherCarolin R.cloescher@geomar.dehttps://orcid.org/0000-0002-2044-6849BangeHermann W.https://orcid.org/0000-0003-4053-1394SchmitzRuth A.CallbeckCameron M.EngelAnjahttps://orcid.org/0000-0002-1042-1955HaussHelenaKanzowTorstenKikoRainerLavikGauteLoginovaAlexandraMelznerFrankMeyerJudithNeulingerSven C.PahlowMarkusRiebesellUlfhttps://orcid.org/0000-0002-9442-452XSchunckHaraldThomsenSörenhttps://orcid.org/0000-0002-0598-8340WagnerHannesGEOMAR Helmholtz Centre for Ocean Research Kiel,
Düsternbrooker Weg 20, 24105 Kiel, GermanyInstitute of General Microbiology,
Christian-Albrechts-Universität zu Kiel, Am Botanischen Garten 1–9, 24118 Kiel,
GermanyMax Planck Institute for Marine Microbiology,
Celsiusstraße 1, 28359 Bremen, Germanynow at: Nordic Center for Earth Evolution, Department of
Biology, University of Southern Denmark, Campusvej 55, 5230 Odense M,
Denmarknow at: AWI, Bremerhaven, Germanynow at: omics2view.consulting GbR, Kiel, GermanyCarolin R. Löscher (cloescher@geomar.de)20June201613123585360622January201517March20154May201624May2016This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/This article is available from https://bg.copernicus.org/articles/13/3585/2016/bg-13-3585-2016.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/13/3585/2016/bg-13-3585-2016.pdf
Recent modeling results suggest that oceanic oxygen levels will decrease
significantly over the next decades to centuries in response to climate
change and altered ocean circulation. Hence, the future ocean may experience
major shifts in nutrient cycling triggered by the expansion and
intensification of tropical oxygen minimum zones (OMZs), which are connected
to the most productive upwelling systems in the ocean. There are numerous
feedbacks among oxygen concentrations, nutrient cycling and biological
productivity; however, existing knowledge is insufficient to understand
physical, chemical and biological interactions in order to adequately assess
past and potential future changes.
In the following, we summarize one decade of research performed in the framework of the
Collaborative Research Center 754 (SFB754) focusing on climate–biogeochemistry
interactions in tropical OMZs. We investigated the influence of low environmental oxygen conditions on biogeochemical cycles, organic matter formation and remineralization, greenhouse gas production and the ecology in OMZ regions of the eastern tropical South Pacific compared to the weaker OMZ of the eastern
tropical North Atlantic. Based on our findings, a
coupling of primary production and organic matter export via the nitrogen
cycle is proposed, which may, however, be impacted by several additional
factors, e.g., micronutrients, particles acting as microniches, vertical and
horizontal transport of organic material and the role of zooplankton and
viruses therein.
Introduction
Eastern boundary upwelling systems are ocean areas where cold and
nutrient-rich waters are upwelled to the sea surface, where they fuel high
biomass production (Carr, 2002; Chavez and Messie, 2009). While covering
only 0.2 % of the ocean, those upwelling areas account for about 50–58 %
of global fish catch (Pauly and Christensen, 1995). Two eastern boundary
upwelling systems were subject to this study: the upwelling off Mauritania,
located in the eastern tropical North Atlantic (ETNA), and the upwelling
system off Peru, located in the eastern tropical South Pacific (ETSP). While
both systems are characterized by intense primary production, their
biogeochemical properties differ strongly (Karstensen et al., 2008), which
partially results from a combination of different water mass ages and
characteristics (Körtzinger et al., 2004), topography and atmospheric
impacts (e.g., Duce et al., 2008). A major difference between the ETNA and
the ETSP is the intensity of the oxygen minimum zone (OMZ) associated with
those upwelling regions (Capone and Hutchins, 2013): the ETNA OMZ has
O2 concentrations typically above 40 µmol kg-1, whereas the
large and persistent OMZ in the ETSP located off Peru and Chile has O2
concentrations below the detection limit based on conventional methods
(∼ 2 µmol kg-1, Fig. 1) with sometimes even
sulfidic conditions on the shallower shelf (Schunck et al., 2013).
Global distribution of O2 at σθ= 26.4 kg m-3
(∼ 400 m depth): the major regions of low oxygen in the world
ocean are all located in the tropical oceans, at shallow to intermediate
depths. The area off Peru represents one of the most pronounced OMZs. The
investigated areas in the eastern tropical South Pacific and the eastern
tropical North Atlantic oceans are marked with black boxes; examples of the
O2 distribution are given along two sections from the coast to the open
ocean at 10∘ S in the OMZ off Peru and at 18∘ N in the
eastern tropical North Atlantic; O2 concentrations are indicated by the
color code.
Besides the age of the water mass and other physical constraints, biological
remineralization and respiration processes consume O2 below the highly
productive surface waters and contribute to the development and maintenance
of OMZ waters (Walsh, 1981; Quiñones et al., 2010). The intensity of the OMZ
may be determined by a positive feedback, with increased primary production
leading to enhanced organic matter export back to underlying
O2-depleted waters (Dale et al., 2015). As a consequence of enhanced
organic matter export, respiration processes may increase. Anoxia, on the
other hand, would promote O2 sensitive N loss processes, creating a
nitrogen (N) deficit in upwelled waters. This would then stimulate N2
fixation at the sea surface and enhance again primary production. A critical issue to understand is to what
extent a feedback between primary production, organic matter remineralization and
the N cycle is a valid model in OMZ waters and what role sulfidic
conditions play therein.
Modeling results (Bopp et al., 2013; Cocco et al., 2013) predict that
O2 levels will decrease significantly over the next decades in response
to climate change and eutrophication. Hence, the future ocean may experience
major shifts in nutrient cycling triggered by the possible expansion and
intensification of tropical OMZs (Codispoti, 2010). Currently, the estimated
volume of OMZs with O2 concentrations < 20 µmol kg-1
is about 1 % of the global ocean volume (Lam and Kuypers, 2011).
Approximately 0.05 % of the global ocean volume has O2 levels below
5 µmol kg-1. The effects of O2-sensitive nutrient cycling
processes occurring in these relatively small regions (Codispoti, 2010) are
conveyed to the rest of the ocean (see, e.g., Deutsch et al., 2007). Hence,
comparatively “small” volumes of OMZs can significantly impact nutrient
budgets, biological productivity and the overall potential for CO2
fixation in the ocean. An important factor is further that deoxygenation of
OMZs has been proposed to increase the production of the greenhouse gas
nitrous oxide (N2O) (Codispoti, 2010). Therefore, understanding the
present biogeochemistry of those systems and exploring the potential to
respond to climate change is critical.
The following review of the major biogeochemical processes in OMZ waters is
based on studies of the SFB754,
“Climate-Biogeochemistry Interactions in the Tropical Ocean” (www.sfb754.de).
Comparisons between the ETNA and ETSP upwelling
systems, their OMZs, and differences in remineralization processes and
associated marine sources and sinks of important nutrient elements are
discussed in order to understand potential controls on the intensity of
those OMZs, as well as their future development.
Primary production in the ETSP and ETNA
In eastern boundary upwelling systems, phytoplankton blooms are stimulated
by nutrient supply from upwelled waters and provide the basis for vibrant
ecological systems. Both the ETNA and the ETSP are major sites of primary
production (Longhurst et al., 1995), with the ETNA exceeding primary production of
the ETSP by a factor of ∼ 2 depending on the applied method
(see Table 1 for an overview of major primary production-related
parameters). This difference may be explained, for example, by the stoichiometry of
the macronutrients N and phosphate (P), with the deficit of N based on a
Redfieldian equilibrium of N : P = 16 : 1 being significantly stronger in the
ETSP compared to the ETNA (Deutsch et al., 2007). This difference may be due
to intensified N loss mirrored by a strongly positive δ15N-nitrate
signal (Ryabenko et al., 2012) in the more O2-depleted water column and
sediments of the ETSP. On the other hand, enhanced P release from the
sediments at decreasing O2 (Ingall and Jahnke, 1994), or a difference
between N and P remineralization from organic material (Jilbert et al.,
2011), may impact decreased N : P ratios. A stronger N deficit in the water
column may influence primary production in different ways: it may
stimulate N2 fixation in order to replenish the N deficit, or it may stimulate non-Redfield primary production. A way to detangle these potential
responses is thus to understand the community composition.
A comparison of the O2 minimum, excess nitrogen (N*), primary
production, organic C export, N2 fixation and N loss in the ETNA and
ETSP upwelling regions.
ETSP – shelfETSP – offshoreETNA – shelfETNA – offshoreO2 min (µmol kg-1)0 (sulfidic)02540N* (mol m-2)-1.9 to (-5.98)aPrimary production (mmol C m-2 d-1)101–122b73–94b68.5c137c61,4d167dOrganic C export (mmol C m-2 d-1)10.6–75.3b2.6–11.1b6.4–9.3e0.67–2.6eN2 fixation (µmol N m-2 d-1)25–657f24–140g% contribution of N20.2–4bfixation to primary production*0.2–6.4c0.2–0.7c0.3–7.1d0.1–0.6dN loss (mmol N m-2 d-1)1–10 to 7000 anammox denitrification(in presence of H2S)00
* Calculated based on the Redfield ratio of C : N = 106 : 16 using the primary
production and N2 fixation rates given in this table in consistency
with the % contribution given in Duce et al. (2008).
a Kalvelage et al. (2013); b Dale et al. (2015); c Behrenfeld
and Falkowski (1997); d Longhurst et al. (1995); e Iversen et al. (2010);
f Dekaezemacker et al. (2013) and Löscher et al. (2014); g Voss et al. (2004).
Franz et al. (2012a) reported in situ observations along an east–west
transect in the ETSP at 10∘ S stretching from the upwelling region
above the narrow continental shelf to the well-stratified oceanic section of
the eastern boundary regime. The study showed that new production in the
coastal upwelling was driven by large-sized phytoplankton (e.g., diatoms)
with generally low N : P ratios (< 16 : 1), thus speaking for
non-Redfield surface water primary production. A deep chlorophyll a
maximum consisting of nano- (Synechococcus, flagellates) and
microphytoplankton occurred within a pronounced thermocline in subsurface
waters above the shelf break. Here, intermediate particulate N : P ratios
were close to Redfield proportions. High PON : POP (> 20 : 1)
ratios were observed in a stratified open-ocean section, coinciding with a
high abundance of the picocyanobacterium Prochlorococcus. Excess P
was present along the entire transect but did not appear to stimulate growth
of N2 fixing cyanobacteria, as pigment fingerprinting and phylogenetic
studies did not indicate the presence of diazotrophic cyanobacteria at most
of our sampling stations (Franz et al., 2012a; Löscher et al., 2014).
These findings are mostly in accordance with other studies from this area
(Bonnet et al., 2013; Fernandez et al., 2011; Turk-Kubo et al., 2014). The
excess P generated within the OMZ seemed to be consumed by non-Redfield
processes, i.e., primary production by large phytoplankton found in shelf
surface waters, instead of stimulating surface N2 fixation. A possible
explanation can be deducted from the optimality-based model of N2
fixation by Pahlow et al. (2013). The model is based on the assumption that
natural selection should tend to produce organisms optimally adapted to their
environment. The competitive advantage of diazotrophs is most pronounced
under conditions of low dissolved inorganic N and increased dissolved
inorganic P (DIN, DIP) availability (Houlton et al., 2008). The ability to
compete for DIP is therefore less important at high DIP. Thus, high P
concentrations above the ETSP OMZ might actually reduce the selective
advantage of diazotrophs compared to non-Redfield primary producers. This
could partially explain why cyanobacterial N2 fixers were apparently not
stimulated by excess phosphate in surface waters of the abovementioned
transect.
The impact of changing N : P ratios as a result of ocean deoxygenation: a
mesocosm approach
A series of on-board mesocosm experiments and bioassay incubations were
performed in order to identify nutrient limitations in both areas and to
specifically address the impact of stoichiometry on primary production.
Despite the fundamental differences between the ETNA and ETSP with regard to
the N deficit, the results of short-term mesocosm experiments implied N
limitation of surface plankton communities in both areas (Franz et al.,
2012a, b). Further, the partitioning and elemental composition of dissolved
and particulate organic matter were investigated. Maximum accumulation of
particulate organic carbon (POC) and particulate organic nitrogen (PON) was
observed under high N supply, indicating that primary production was
controlled by N availability. Part of the excess P was consumed by
non-Redfield production, predominantly by diatoms, as also observed from
direct monitoring as described above. While particulate N : P of the
accumulated biomass generally exceeded the supply ratio (Franz et al.,
2012b), excess P of the dissolved nutrient pool was channeled into release of
dissolved organic phosphorus (DOP) by phytoplankton. These results
demonstrated that excess P upwelled into the surface ocean overlying
O2-deficient waters represents a net source for DOP and motivated
further dedicated mesocosm experiments in the ETNA to elucidate the fate of
DOP. While the direct monitoring and the results of mesocosm studies strongly
spoke for a shift to non-Redfield primary production due to changes in
N : P, a general stimulating effect of DOP on N2 fixation has been
observed (Meyer et al., 2016). This is in line with a recent modeling study
based on large-scale surface datasets of global DON and Atlantic Ocean DOP.
Here, the model suggests an important role of DOP for stimulating growth of
N2 fixing organisms (Somes and Oschlies, 2015). This model indicates
that the marine N budget is sensitive to DOP, provided that access to the
relatively labile DOP pool expands the ecological niche for diazotrophs.
Taken together, changes in N : P may lead to a combination of both
non-Redfield primary production and enhanced N2 fixation via DOP.
Besides direct effects of N : P ratios, primary production and N2
fixation, due to the comparably high Fe requirements of the diazotrophs
(Gruber and Sarmiento, 1997), are largely influenced by trace metal availability (Mills et
al., 2004). From the comparison of the ETNA and ETSP regions, an obvious difference with
regard to potentially limiting nutrients is related to the iron (Fe) source:
in the ETNA, Saharan dust input contributes 71–87 % of dissolved Fe to the
water (Conway and John, 2014). Several studies have highlighted the importance of
atmospheric Fe supply to the ETNA (Voss et al., 2004; Mills et al., 2004) as
a major factor of primary production. However, a comparable atmospheric Fe source is
missing in the ETSP (Baker et al., 2016). Previous studies (Scholz
et al., 2014) have identified the ETSP Fe supply as benthic; however, the
question of how much Fe is transported from the sediments to the sea surface
has not yet been fully clarified.
Results of bioassay incubations and correlation studies demonstrated that
primary production and N2 fixation in this region respond significantly
to Fe additions (Dekaezemacker et al., 2013). N2 fixation could be
directly limited by inorganic nutrient availability, or indirectly through
the stimulation of primary production and the subsequent excretion of
dissolved organic matter and/or the formation of microenvironments
favorable for heterotrophic N2 fixation (Dekaezemacker et al., 2013).
What is the role of N2 fixation for primary production in the ETNA
and ETSP?
Several studies (Voss et al., 2004; Mills et al., 2004; Langlois et al., 2005, 2008) have demonstrated the important role of N2 fixation for surface
primary production in ETNA waters. Voss et al. (2004) estimated an average
N2 fixation of 24–140 µmol m-2 d-1, translating into
a contribution of 0.1–0.7 % to primary production assuming Redfield
stoichiometry on the basis of the rates given in Table 1. This is below the
global average of 5.3 % (Duce et al., 2008), potentially due to the
relatively high deposition of reactive N via Saharan dust input.
For the ETSP, N2 fixation was higher compared to the ETNA with rates of
25–657 µmol m-2 d-1 (Dekaezamacker et al., 2013;
Löscher et al., 2014), while C fixation was rather lower (Table 1).
Here, theoretically, N2 fixation contributes 0.2–7.1 % of C fixation
(Table 1). However, while N loss does not play a role in the ETNA water
column (see, e.g., Bange et al., 2010), with the exception of O2-depleted mesoscale eddies (Löscher et al., 2015), high N loss removes
between 1 and 3 orders of magnitude more N (Kalvelage et al., 2013;
Table 1) than is made available by N2 fixation. This would decrease the
contribution of N2 fixation to C fixation to zero. When comparing
N2 fixation to N loss, it must be considered that first N loss has only
been detected on and close to the shelf, while N2 fixation rates were
detectable throughout the OMZ water column (Fig. 2). Second, while N2
fixation is measured via direct N2 incorporation and therefore mirroring
in situ rates, N loss is likely being overestimated as measured following addition
of the substrates, which may artificially stimulate the respective process
(up to 2–3 orders of magnitude, as discussed in Kalvelage et al., 2013). As
a result, an entirely correct budget of N2 fixation vs. N loss based on
rate measurements is difficult to obtain.
Co-occurrence of anammox as determined by rate measurements and
the key functional marker gene for N2 fixation, nifH, in the ETSP OMZ
(modified from Kalvelage et al., 2013, and Löscher et al., 2014).
In both areas, N2 fixation may, however, be considered important for the
productivity of the respective system. Still, given the previously described
observations of non-Redfield primary production, the contribution to C
fixation remains to be fully established.
From the comparison of the N2 fixation in the ETNA and ETSP, the
question arises of why there is such a strong difference between those systems.
A possible explanation may be found in the character of the diazotrophic
communities: while the classical view of oceanic N2 fixation mainly
attributed to phototrophic cyanobacteria, such as Trichodesmium or Crocosphaera (Capone et al., 1997;
Zehr and Turner, 2001), may be mostly true for the ETNA (e.g., Langlois et
al., 2005, 2007; Großkopf et al., 2012), a different community of
diazotrophs is present in the ETSP.
A growing number of different nifH sequences (the key functional gene of N2
fixation, encoding the α subunit of nitrogenase) detected within the
Peruvian OMZ (Bonnet et al., 2013; Dekaezemacker et al., 2013; Fernandez et
al., 2011; Löscher et al., 2014; Turk-Kubo et al., 2014) did not belong
to common oxygenic phototrophs but instead to some unknown diazotrophic
microorganisms that might be specifically adapted to O2-deficient
conditions.
These diazotrophs, as well as the extension of their habitat to deeper
waters, might be one reason for the possible underestimation of N gain
compared to N loss in the ocean (Codispoti, 2007). In combination with a
novel method for N2 fixation rate measurements (Mohr et al., 2010), up to 6-fold higher N2 fixation
rates were obtained when considering N2 fixation below the euphotic zone (Großkopf et al., 2012). When
extrapolated to all ocean basins this resulted in a N2 fixation rate of
177 ± 8 Tg N yr-1, which, depending on the assumed budget, may
balance 50–100 % of oceanic N loss (Codispoti, 2007; Gruber and Sarmiento,
1997).
To what extent is N2 fixation in the ETSP OMZ coupled to N
loss?
Model studies (Deutsch et al., 2007) assume that a N-deficit resulting from
N loss or enhanced P release (Ingall and Jahnke, 1994) provides a niche for
diazotrophs. A coupling of N loss in OMZs and N2 fixation in overlying
surface waters might restore the N : P ratio towards Redfield proportions.
In the ETSP OMZ, N is indeed continuously removed by the anaerobic oxidation
of ammonium (anammox) (Francis et al., 2007; Kuypers et al., 2003, 2005;
Thamdrup and Dalsgaard, 2002), which has been shown to be the dominant N
loss process in this region (Kalvelage et al., 2013; Lam et al., 2009), as
well as in other OMZ waters (off Namibia – Kuypers et al., 2005; Peru –
Hamersley et al., 2007; and Chile – Thamdrup et al., 2006). Moreover, N is lost by denitrification (the four-step reduction of NO3- to N2;
Devol, 2008), e.g., in the Arabian Sea OMZ (Ward et al., 2009), where
denitrification has been identified as the dominant N loss process. However, off
Peru, denitrification was only detectable in connection to sulfidic events
(Kalvelage et al., 2013; Schunck et al., 2013).
The prevalence of novel nifH genes and active N2 fixation, derived from
samples collected directly in the OMZ waters off Peru, where anammox
bacteria were abundant and active (Kalvelage et al., 2013; Löscher et
al., 2014), supports the view of a positive feedback between N loss and N
gain communities (Fig. 3). Evidence for co-occurrence of denitrification
and N2 fixation has previously only been documented for an anoxic lake
(Halm et al., 2009) and for cyanobacterial aggregates in the Baltic Sea
(Klawonn et al., 2015). Recent investigations from Baltic Sea sediments on
N2 fixation and diazotrophic abundance in sediments show, however, that
a very close spatial link between N loss and N2 fixation might exist
(Bertics et al., 2013). Still, too little is currently known about the
interactions among the stoichiometry of inorganic nutrient supply, primary
production, N2 fixation, and remineralization under anoxic conditions
to allow for a definite characterization of the conditions leading to
fixed-nitrogen exhaustion in the OMZs.
The marine nitrogen (N) cycle with the major onshore and offshore
processes in the ETSP OMZ, modified from Kalvelage et al. (2013). Numbers
indicate fluxes of N (Tg yr-1).
This coupling which seems to exist in OMZ waters may in fact have far-reaching consequences: while N loss may provide a niche for N2
fixation, model studies suggest that denitrification of N2
fixation-derived organic matter may lead to a net N loss that further
stimulates N2 fixation, because 120 mol of nitrate per mole of
phosphorus is used to remineralize Redfield organic matter via
denitrification (Landolfi et al., 2013). In contrast, N2 fixation fixes
only 16 mol of N (per mole of P). Because of those stoichiometric constraints,
any addition of fixed N to the surface ocean only exacerbates the problem
(Canfield, 2006) unless the corresponding primary production is prevented
from being remineralized in the underlying OMZ (Landolfi et al., 2013).
Indeed, Lipschultz et al. (1990) stated that N loss in the ETSP OMZ is high
enough to respire all produced organic material. Only by spatial or temporal
decoupling of N2 Fe limitation or dissolved organic matter cycling may the
N inventory stabilize; otherwise, the OMZ would become completely void of
fixed inorganic N. Whether these stoichiometric constraints are valid for
anammox as dominant N loss process instead of denitrification is, however, not
clear.
Concerning the stoichiometric aspects of ultimate N loss from OMZ waters, a
to date largely disregarded aspect should be taken into consideration: as
shown for the Gotland Basin (Jilbert et al., 2011), enhanced preferential P
release from organic matter remineralization was quantitatively important for
creating a N deficit. This preferential P release was present in the water
column and was further increased under O2-depleted, reduced conditions.
Although the quantitative contribution to the N deficit in the ETSP is not
yet entirely clear, it may act as a factor decoupling the “vicious” cycle
between N2 fixation and N loss (Landolfi et al.,
2013), because it may shift the abovementioned stoichiometric constraints.
Factors determining N loss
The net rate of N loss in OMZs is determined by the balance of
remineralization of sinking particulate organic carbon (POC) and O2
supply to the OMZ. Interestingly, recent studies have attributed the dominance
of either anammox or denitrification in a certain environment to organic
matter composition and availability (Babbin et al., 2014). While the supply
of O2 is mostly determined by physical transport, the rate of N loss
depends on the activity of the bacteria responsible for denitrification and
anammox as well as the POC export and sinking velocity.
The intensity of this feedback may be overestimated in current biogeochemical
models, owing to spurious nutrient trapping (Dietze and Loeptien, 2013). The
extent of the coupling between primary production at the surface and
denitrification in the OMZ, and hence the strength of the positive feedback,
is a strong function of the elemental (C : N : P) stoichiometry of the
exported primary production. Phytoplankton C : N : P stoichiometry in
turn is influenced by the stoichiometry of inorganic nutrients (Franz et al.,
2012a, b). Recently developed process models of primary production and
N2 fixation (Pahlow et al., 2013; Pahlow and Oschlies, 2013)
specifically address the response of phytoplankton elemental stoichiometry to
ambient nutrient concentrations and light.
It is generally assumed that both zooplankton and heterotrophic bacteria
vary much less in their elemental stoichiometry than phytoplankton (e.g.,
Touratier et al., 2001). In both cases, the heterotrophs appear to respond
to variable nitrogen content in their food by regulating their gross growth
efficiency for carbon (Anderson and Williams, 1998; Kiørboe, 1989). In OMZ
regions, this implies that strong nutrient limitation in the surface ocean,
which is associated with high C : N ratios in primary producers (e.g., data
used in Pahlow et al., 2013), should intensify denitrification in the OMZ
relative to the export flux from the surface. Higher surface nutrient
concentrations would then be expected to reduce C : N ratios in the export
flux and hence have a somewhat mitigating effect. Since denitrification and
anammox in the OMZ cause lower nitrate concentrations in upwelled waters,
the variable stoichiometry of phytoplankton could add to the positive
feedback between denitrification and N2 fixation by increasing C:N
ratios in response to decreasing surface nitrate concentrations.
Combined 15N-incubation experiments and functional gene expression
analyses indicate that anammox in the Peruvian OMZ benefits from other
N-cycling processes for reactive substrates (Kalvelage et al., 2011).
Excretion of ammonium and other reduced N compounds by diel vertical
migrators has also been proposed (Bianchi et al., 2014), but recent experiments
indicate that ammonium excretion of diel vertical migrators is strongly
reduced at anoxia (Kiko et al., 2015, 2016). Additionally, anammox activity has been described to
depend on export of organic matter (Kalvelage et al., 2013), potentially
resulting from the availability of ammonium recycled from particulate organic
N (Ganesh et al., 2015). In the absence of significant denitrification, these
results indicate that anammox relies on NH4+ oxidation and
NO3- reduction as NO2- source. Further, NH4+ may be
derived from remineralization of organic matter via NO3- reduction
with a possibly important role of microaerobic respiration (Kalvelage et al.,
2015). The overlap between aerobic and anaerobic N-cycling processes in
particular in the coastal shelf waters and the upper part of the OMZ is
supportive of microaerobic activity in the OMZ. As dissimilatory nitrate reduction to ammonium (DNRA) was insignificant in
the water column during our studies in the ETSP, sedimentary fluxes could be
an important ammonium source, particularly for the inner shelf sediments
(Bohlen et al., 2011; Kalvelage et al., 2013). However, it has been suggested
that sulfate reduction is more widespread in OMZ waters than previously
believed and could be responsible for substantial NH4+ production
(Canfield et al., 2010), and sulfate reducers have been detected in the
Peruvian OMZ (Schunck et al., 2013). However, direct evidence for the actual link
between sulfate reduction and NH4+ production is still
missing.
Organic matter export and remineralization in the ETSP OMZSinking of particles
Knowledge about particle fluxes in areas of tropical OMZs is scarce and
predominantly derived from deep moored traps (Honjo et al., 2008) or models
(Dale et al., 2015, Table 1). Only a few studies have addressed upper ocean
export fluxes and mesopelagic flux attenuation in tropical OMZs
(Martin et al. (1987), Devol and Hartnett (2001) and Van Mooy et al. (2002) for the
eastern tropical Pacific by means of surface tethered sediment traps;
Buesseler et al. (1998) for the Arabian Sea by means of 234Th; and
Iversen et al. (2010) at the northern edge of the ETNA OMZ by means of
particle camera profiling). In the eastern tropical North Pacific (ETNP)
(Martin et al., 1987; Van Mooy et al., 2002; Devol and Hartnett, 2001) and the ETSP (Martin et al. 1987; Dale et al., 2015) mesopelagic POC
fluxes were less attenuated with depth (Martin curve exponent “b” of
0.32–0.81) compared with the widely used “open-ocean composite” of
b= 0.86 (Martin et al., 1987). Those studies indicate that a greater
proportion of the sinking organic matter escapes degradation while sinking through the
eastern tropical Pacific OMZ. On the other hand, it has been shown that
microbial degradation of organic N and proteins under suboxia (< 20 µM O2)
is not strongly affected (Pantoja et al., 2004, 2009; Van Mooy et al., 2002). In addition, organic matter
degradation seems not to be significantly affected by decreased O2
(Dale et al., 2015).
Still, little is known about the microbial controls on the decomposition of
organic matter under lower O2 concentrations. Microorganisms are
generally considered responsible for most of the remineralization in the
ocean. This view is probably justified with respect to carbon, given the high
rates of microbial respiration (del Giorgio and Cole, 1998). Owing to the
relatively low N and phosphorous (P) content of dissolved organic matter,
however, bacteria may be less important for the remineralization of N and P
and in fact often compete with phytoplankton for inorganic nutrients in the
surface ocean (Anderson and Williams, 1998; Pahlow and Vézina, 2003).
Remineralization of N and P may thus be largely due to zooplankton activity
(Caron et al., 1988; Garber, 1984; Pahlow et al., 2008).
Classically, the most abundant organisms detected in OMZs belong to the
Proteobacteria, Bacteroidetes, Thaumarchaeota of the marine group A,
Actinobacteria and Planctomycetes (Schunck et al., 2013; Wright et al.,
2012). Several candidate clusters have previously been identified, among
which are the SAR11, SAR324 and SUP05 clusters (Schunck et al., 2013; Wright
et al., 2012). Most investigations of the microbial phylogenetic and
functional diversity resort to observing and correlating changes in oxygen
concentrations to changes in the microbial phylogenetic diversity. Indeed,
several studies, including our own datasets (NCBI accession number:
SRP064135), corroborate this idea: a combined statistical analysis of our
metagenomic data of the ETSP OMZ (Kalvelage et al., 2015) and datasets from
the Chilean OMZ (Canfield et al., 2010; Stewart et al., 2011) has resulted
in a partitioning of the OMZ into five different habitats, namely surface,
subsurface (defined as below the mixed layer and above waters with
O2 > 20 µmol kg-1), oxyclines, OMZ core
(O2 < 5 µmol kg-1) and sulfidic waters (Fig. 4).
High-resolution sampling in the ETNP OMZ has shown
that the microbial richness is highest at the base of the euphotic zone and
the upper oxycline (Beman and Carolan, 2013), often along with high organic
flux, low O2 concentrations and dynamic cycling of C, N, and sulfur
(S). This may be interpreted in a way that the upper oxycline is of higher
importance for remineralization than the OMZ.
Redundancy analysis ordination model of microbial taxa (vectors)
identified from pyrosequencing reads of multiple samples (points) in the
ETSP. Spherical k-means clustering revealed a 5-fold partitioning that
reflects distinct OMZ habitats (see legend). Each point is colored according
to the cluster that dominated the microbial population in the respective
sample.
The impact of zooplankton on organic matter export and
remineralization
An important consideration for explaining the lowered flux attenuation in
the OMZ could be deducted from the diminished abundance of metazoans in the
core of the OMZ. If particles are not repackaged, fed upon, or destroyed,
they might sink at greater speeds through the OMZ, which would result in
decreased degradation.
Zooplankton and nekton organisms are essential components of the biological
pump as they egest packaged organic matter as rapidly sinking fecal pellets.
Many zooplankton and nekton species also feed in surface waters during the
night and migrate to midwater depth at daybreak to avoid predation (Lampert,
1989) and to conserve energy (McLaren, 1963). This behavior is known as
diel vertical migration (DVM) and also contributes to the activity of the
biological pump as it enhances the export of organic matter from the photic
zone by continued respiration, excretion and egestion in midwater layers
(Burd et al., 2010; Hannides et al., 2009; Robinson et al., 2010; Steinberg
et al., 2000). In addition to changes in temperature with depth, DVM
organisms experience low O2 concentrations during the daytime in OMZ
regions (Brewer and Peltzer, 2009; Paulmier et al., 2011), and O2
concentrations below a certain threshold level can restrict DVM of most
zooplankton and nekton (e.g., Hauss et al., 2016). On a
regional scale, the upper boundary of the oxycline is the single most
critical factor structuring the habitat of most zooplankton organisms in the
Peruvian upwelling system (Escribano et al., 2009). Nevertheless, some
specifically adapted species are able to downregulate their metabolic
activity at low oxygen levels and can remain at OMZ depth (non-migrators) or
actively migrate into suboxic or anoxic OMZs (Seibel, 2011; Kiko et al., 2015, 2016).
The abundance and biomass of metazoans living permanently at extremely low
oxygen concentrations < 0.6 mL L-1 are rather low (Auel and
Verheye, 2007; Escribano et al., 2009; Fernández-Álamo and
Färber-Lorda, 2006; Saltzmann and Wishner, 1997; Wishner et al., 1998),
although animals have evolved physiological (such as metabolic suppression)
and/or morphological adaptations (such as increased gill surface area) that
allow them to cope temporarily or permanently with O2-depleted
conditions (e.g., copepods such as Eucalanus inermis: Flint et al.,
1991; euphausiids such as Euphausia mucronata: Antezana, 2009;
decapods: Pearcy et al., 1977; cephalopods such as Dosidicus gigas:
Rosa and Seibel, 2010; and teleosts: Friedman et al., 2012; Luo et al.,
2000). According to Seibel (2011), adaptations to low oxygen levels are
needed below approximately 40 µmol O2 kg-1. Strong
physiological adaptations thus seem necessary to thrive in the ETSP OMZ, but
not in the ETNA OMZ, where O2 concentrations are normally greater than
40 µmol kg-1 (Teuber et al., 2013).
Estimates of zooplankton- and nekton-mediated carbon fluxes in OMZ regions
are rare. For the northern Chilean upwelling in the ETSP, Escribano (2009)
found that migrations of only two key species (Eucalanus inermis and Euphausia mucronata) contribute
approximately 7.2 g C m-2 d-1 to the OMZ through respiration,
mortality, and production of fecal pellets within the OMZ. However, these
estimates are probably too high, as the reduction of respiration at low
oxygen levels (Kiko et al., 2015, 2016) was not accounted for in
the calculations. As stated above, a particular role of DVMs for the N cycle
could result from the secretion of ammonium: ammonium is an important
nutrient in the anammox reaction which represents nearly 30–50 % of N-loss
activity in the OMZ (Codispoti et al., 2001; Emery et al., 1955; Gruber,
2004). Bianchi et al. (2014) suggested that DVMs could supply as much as
30 % of the ammonium for the anammox reaction, assuming no reduction in
the rate ammonium excretion under OMZ conditions. This assumption is
unlikely to hold, however, as ammonium excretion is, for example, reduced 4-fold
in the squat lobster Pleuroncodes monodon (Kiko et al., 2015, 2016) and 6-fold
in the euphausiid Euphausia mucronata (Kiko et al., 2015, 2016) upon exposure to
anoxia at OMZ temperatures. Thus, the significance of excretion by
zooplankton as a source of ammonium for the anammox reaction remains to be
established.
The impact of viruses on primary production and organic matter
feedbacks
A recent model study quantifying the effect of viruses on ecosystem function
in the ocean demonstrated that viruses affect biological productivity and
remineralization (Weitz et al., 2015). In line with field studies (Breitbart,
2012), this model showed enhanced organic matter cycling, e.g. by cell lysis.
Viruses lyse ∼ 10–40 % of the present prokaryotes every day
(Suttle, 2005), which may – besides generally supplying nutrients to the
surrounding waters – impact stoichiometry on smaller scales. Specifically,
(cyano)phages in the ETSP have been shown to release micronutrients such as
Fe into surrounding waters at an estimated flux of
10 pmol L-1 d-1 (Poorvin et al., 2004). Likewise, virus-induced
bacterial lysis was calculated to contribute ∼ 1–6 Gt N a-1 to
bacterial primary production, which would significantly support phytoplankton
production (Shelford et al., 2012). The transfer of nutrients from living
organisms into the dissolved phase is called the “viral shunt” (Breitbart,
2012). Besides the “viral shunt”, the model showed a reduced transfer of
organic material to higher trophic levels, which was interpreted to stabilize
primary production. Quantitatively, net primary production was found
increased by ∼ 11 % in the presence of viruses. This strongly
speaks for a viral impact on the efficiency of the biological pump (Azam,
1998). On the other side, viruses were shown to influence particle formation
and disaggregation through discharging adhesive cell components (Peduzzi and
Weinbauer, 1993) and cell lysis (Weinbauer et al., 2011), respectively.
In OMZ waters, highly specific viral communities have been discovered which
show unusually low diversity and a low viral-to-microbial ratio (VMR)
(Cassman et al., 2012). Specific viruses appear to be only present in OMZ
waters as exemplarily shown by genomic studies of uncultivated SUP05
bacteria isolated from the ETSP OMZ (Roux et al., 2014). Interestingly,
various genes involved in the cycling of nitrogen and sulfur have also been
found in viromes of ETSP waters (see Tables S3 and S4 in Cassman et al., 2012; Roux et al., 2014).
Recent studies analyzing samples from the weaker ETNA OMZ indicated that one
of the most abundant archaeal nitrifiers in the ETNA OMZ (Thaumarchaeota,
Cand.Nitrosopelagicus brevis) contains several viral
genes in its genome arguing that this archaeon is infected by an OMZ-specific
hitherto uncharacterized virus (Neulinger and Schmitz, unpublished results),
thus confirming earlier studies from the global ocean dataset (Santoro et
al., 2015). Considering that Cand.Nitrosopelagicus brevis
is most likely the most important producer of the greenhouse gas nitrous
oxide in the ETNA and ETSP OMZs (Löscher et al., 2012), these findings
add a potential role for greenhouse gas production to the current picture of
viruses in the ocean.
Physical fluxes of DOM
Besides particle fluxes and organic matter export via DVM, dissolved organic matter (DOM) transport is
due exclusively to physical horizontal and vertical transport processes,
induced by mesoscale (horizontal scales of 10–100 km) and submesoscale
(100 m to 10 km) motion and vertical fluxes due to diapycnal mixing. As an
example of lateral eddy transport, elevated DOM concentrations have been
detected (+11 µmol C L-1) in the Canada Basin within an eddy
originating from the shelf region (Mathis et al., 2007). Lasternas et al. (2013)
suggested a mechanism for DOM accumulation within anticyclonic eddies,
where nutrient downwelling causes a progressive oligotrophication, enhanced
cell mortality and lysis, which results in additional DOM release. Numerical
model simulations of the Peruvian upwelling regime show that mesoscale
dynamics increase the downward and offshore export of nutrients and biomass
out of the coastal surface ocean (Lathuiliere et al., 2010). For the
understanding of remineralization processes and feedbacks in upwelling
systems, a quantification of the material that is lost to the open ocean is
critical as it may directly impact the system's productivity.
Gruber et al. (2011) found that mesoscale eddy activity in upwelling regimes results in a
net reduction of biological productivity. Additionally, submesoscale
upwelling filaments can enhance the off-shelf flux of labile DOM
(Alvarez-Salgado et al., 2001). Vertical velocities are higher at
submesoscale density fronts (Klein and Lapeyre, 2009; Levy et al., 2012;
Thomas et al., 2008), which are prominent features in eastern boundary
upwelling systems (Durski and Allen, 2005). These vertical velocities often
extend to below the mixed layer (Klein et al., 2008), where they can drive
sizeable vertical fluxes of solutes. Mahadevan (2014) proposes the subduction
of organic-matter-rich surface water into the subsurface layers within
submesoscale cold filaments as a new export mechanism, which differs strongly
from export via particle sinking. In filaments the organic matter is
subducted together with large amounts of O2, which then can directly be
used for decomposition of organic matter. Vertical mixing of DOM from the
euphotic into to the upper mesopelagic zone is another important transport
mechanism in (sub)tropical waters (Hansell, 2002). The Bermuda Atlantic
Time-Series Study provides a well-documented example of this process (Carlson
et al., 1994). The efficiency of the downward DOM transport depends on the
concentration gradient of DOM between the surface layer and the OMZ, as well
as on the activity of the microbial population along this gradient. Produced
by high primary production in upwelling regions, DOM can accumulate in the
euphotic zone with maximum concentrations of
100–300 µmol C L-1 off Peru (Franz et al., 2012a;
Romankevich and Ljutsarev, 1990). Due to the vicinity of the DOM-rich surface
layer to the shallow and sharp oxycline of the Peruvian OMZ, as well as the
O2-depleted waters below the oxycline, physical vertical transport may
bring large amounts of labile organic matter to the OMZ, where it may be
utilized by heterotrophic communities (Hoppe et al., 2000; Hoppe and Ullrich,
1999; Pantoja et al., 2009). DOM supply via (sub)mesoscale vertical transport
processes and diapycnal mixing may therefore contribute importantly to
sustaining microbial activity in the Peruvian OMZ and may thus largely impact
biogeochemical cycles.
Sulfidic events in the ETSP
Oceanic sulfidic events are extreme cases of anoxia following periods of
enhanced primary production and organic matter export. They are understood
to mostly originate from sulfide production in sediments (Fig. 5) and have
been documented sporadically since the 19th century for the ETSP OMZ
(Burtt, 1852; Dugdale et al., 1977). To date sulfidic events have been
reported from the eastern tropical South Pacific, the Arabian Sea and the
Benguela upwelling system by only a handful of studies and hence our current
understanding of their regulation, initiation and termination is still
limited. Possible analogs for oceanic events are permanently sulfidic areas
in enclosed basins of the Baltic Sea (Brettar et al., 2006; Brettar and
Rheinheimer, 1991; Glaubitz et al., 2009), the Black Sea (Glaubitz et al.,
2010; Jørgensen et al., 1991; Sorokin et al., 1995), the Cariaco Basin
off Venezuela (Hayes et al., 2006; Taylor et al., 2001; Zhang and Millero,
1993) and Saanich Inlet in Canada (Tebo and Emerson, 1986; Walsh et al.,
2009). Here, sulfide accumulates to millimolar concentrations under O2
and nitrate-free conditions and is released by a diffusive flux into the
overlying pelagic water column, where it reaches low micromolar
concentrations (Lavik et al., 2009; Schunck et al., 2013). These events are
then terminated or detoxified in the pelagic water column by a community of
sulfide-oxidizing bacteria. This occurs when sulfide and nitrate are both
present thus stimulating sulfide-oxidizing nitrate-reducing bacteria
(SONRB). SONRB re-oxidize sulfide back to sulfate or elemental sulfur while
reducing nitrate to either N2 via autotrophic denitrification or
NH4+ via dissimilatory nitrate reduction to ammonium (Lam and
Kuypers, 2011). If nitrate is limiting, sulfur is the more likely end
product of sulfide oxidation, which occurs in the following reaction
stoichiometry for the denitrification pathway, 2NO3-+ 5HS-+ 7H+→ N2+ 5S0+ 6H2O. A steady state is
reached when the diffusive fluxes (mmol m-2 d-1) of nitrate and
sulfide are in a 1 : 2.5 ratio. If the sulfide flux exceeds the nitrate flux
by more than a factor of 2.5, then sulfide will diffuse into the oxic layer
(Lam and Kuypers, 2011). Importantly, the activity of SONRB help to detoxify
sulfide to sulfur, preventing it from reaching overlying productive surface
waters; hence, most sulfidic events likely go unnoticed (Lavik et al., 2009).
However, with the increase in eutrophication and the expansion of OMZs in
both the Atlantic and Pacific (Stramma et al., 2008), sulfidic events are
expected to become more frequent, as already demonstrated for a time series
station in the Baltic Sea (Lennartz et al., 2014).
Schematic representation of the dynamics of a sulfidic event
occurring in an oxygen minimum zone, e.g. in the ETSP. The sulfide and
nitrate fluxes are shown in steady state. Sulfate-reducing bacteria produce
sulfide from the sediment while the complementary detoxification process
occurs in the water column at overlapping profiles.
The first quantitative measurements and detailed profiles of a sulfidic
event in the Peruvian upwelling came from Schunck et al. (2013). During RV
Meteor cruise M77/3 in January 2009 sulfidic waters covered > 5500 km2
and contained approximately 2.2 × 104 t of sulfide,
making it one of the largest plumes recorded. A total of nine stations were
taken along the coastal transect from Lima to Pisco, which showed a
∼ 80 m thick sulfide-rich layer extending at times just below the
oxycline. At this interface oxygen (< 1 µmol kg-1),
nitrate (< 1 µmol kg-1) and nitrite
(2 µmol kg-1) profiles overlapped with detectable sulfide
concentrations. Stable isotope rate measurements and targeted gene assays
using quantitative PCR indicated that various oxidants could have been used
by the microbial community to oxidize sulfide at the time of sampling. The
most abundant sulfide oxidizers identified from the 16S rRNA diversity
belonged to the phylum Proteobacteria within the subphylum
γ-Proteobacteria, including the SUP05/ARCTIC96BD-19 clade,
Candidatus Ruthia magnifica, and Candidatus Vesicomyosocius okutanii, but also ϵ-Proteobacteria such as Sulfurovum
spp. Metagenomics confirmed that all were capable of sulfide or sulfur
oxidation, either with nitrate and oxygen (facultative SONRB) or exclusively
with oxygen. Indeed, both subphyla appear to be ubiquitous in other
seasonally oxic/anoxic waters and OMZs (Canfield et al., 2010; Lavik et al.,
2009; Stevens and Ulloa, 2008; Stewart et al., 2011, 2012; Swan et al., 2011;
Walsh et al., 2009). Both γ- and ϵ-Proteobacteria members are
known chemolithoautotrophs, which assimilate carbon dioxide as the carbon
source without the use of sunlight. Subsurface C-assimilation rates were
between 0.9 and 1.4 µmol C L-1 d-1 during this
sulfidic event. In this study, “dark” primary production had contributed up
to 25 % of the total CO2 fixation in the Peruvian upwelling region
at the time of sampling, which is comparable to values observed in the Baltic
and Black seas (Schunck et al., 2013, and references therein). Paradoxically,
some of these studies showed that measured rates of CO2 assimilation
exceed rates possible by chemolithoautotrophic processes alone. Thus, while
chemolithoautotrophic CO2 fixation is considered a significant process,
the specific activity and main contributors of CO2 fixation during
sulfidic events (down to the genus level) still remain unknown.
What is different from our current knowledge of OMZ sulfur cycling is whether the
production of sulfide can originate from pelagic waters as well.
Simultaneous reduction of different electron acceptors (like NO3-,
SO42- and CO2) can occur in defined niches where particle
aggregates have formed and are sinking through the water column (Wright et
al., 2012). These aggregates, more commonly known as marine snow, contain
microscale redoxclines under anoxic conditions (Alldredge and Cohen, 1987;
Karl and Tilbrook, 1994; Woebken et al., 2007). Moreover, aggregate
communities appear to be distinct from bulk water collected samples
(Fuchsman et al., 2011). These communities were suggested to have active
manganese reduction, sulfate reduction and sulfide oxidation at the interior
of the aggregates. How much sulfide is generated in the water column during
a sulfidic event is not well resolved. Nevertheless, in situ incubation experiments
done in the Chilean upwelling have shown the capacity for sulfate reduction
in the offshore OMZ occurring under thermodynamically unfavorable
nitrate-rich conditions. In separate incubations, measured rates of potential
sulfide oxidation were larger than rates of sulfate reduction, indicating
that any produced sulfide is immediately re-oxidized (Canfield et al.,
2010). The authors intriguingly suggested an active but cryptic sulfur cycle
linked to nitrogen cycling in the pelagic OMZ. From a biogeochemical
perspective large-scale sulfate-reduction coupled to organic matter
remineralization releasing inorganic nitrogen could represent a significant
supply of ammonium for anammox bacteria.
Distributions of N2O, NH4-, NO2-,
NO3-, H2S, and water temperature during December 2008/January
2009 (R/V Meteor cruise M77/3) on the shelf along the coast of Peru. Max
N2O concentrations have been detected right above the sulfidic zone,
where a sharp oxycline is present and ammonium and nitrate are available.
Trace gas production in OMZ waters
The upper 1000 m of the ocean (including the euphotic zone) is the key region
where the production of climate-relevant trace gases such as carbon dioxide
(CO2), nitrous oxide (N2O), methane (CH4) and dimethyl
sulfide (DMS) occurs (see, e.g., Liss and Johnson, 2014). While the
pathways of CO2 and DMS are dominated by phytoplankton in the oxic
euphotic zone, N2O and CH4 pathways are dominated by microbial
processes at midwater depth (i.e., in the OMZ). This is especially important
since some OMZs are connected to coastal upwelling regions where OMZ waters
– enriched in both nutrients and trace gases such as CO2, N2O
and CH4 – are brought to the surface, fueling phytoplankton blooms
and releasing trace gases to the atmosphere (see, e.g., Capone and Hutchins, 2013).
Thus, although they are usually not in direct contact with the
atmosphere, OMZs play an important role for oceanic emissions of
climate-relevant trace gases (see, e.g., Arévalo-Martínez et al., 2015).
Nitrous oxide (N2O) in OMZ
A comprehensive overview of both nitrous oxide (N2O) distributions and
pathways in OMZ has been published in Naqvi et al. (2010). Therefore, we
concentrate here on recent findings from the ETNA and ETSP.
N2O production in the ocean is dominated by microbial nitrification and
denitrification processes. It is formed as a by-product during nitrification
and as an intermediate during denitrification. The paradigm that N2O is
exclusively produced by bacteria has been challenged by the discovery of
nitrifying (i.e., NH4+ oxidizing) archaea (e.g., Cand.Nitrosopelagicus brevis; see above)
dominating N2O production in the ETSP and ETNA (Löscher et al.,
2012), which is supported by results of a culture study (Löscher et al.,
2012) and a marine microbial enrichment experiment (Santoro et al., 2011).
The production of N2O by archaea (and bacteria) depends on dissolved
O2 and increases with decreasing O2 concentrations (Frame and
Casciotti, 2010; Löscher et al., 2012). Denitrifying bacteria do not
produce N2O in the presence of O2 (> 10 µmol kg-1);
however, when O2 concentrations are approaching 0 µmol kg-1,
N2O is consumed during denitrification. There is no
N2O production under anoxic conditions. The significance of N2O
production during anammox (Kartal et al., 2007) and DNRA (Giblin et al.,
2013) in OMZs (see Sect. 5) remains to be proven.
The detailed investigation of ΔN2O/AOU
(i.e., excess N2O/apparent oxygen utilization) and ΔN2O/Δ15NO3- relationships from the ETNA and ETSP revealed
two facts (Ryabenko et al., 2012): (i) the lower O2 concentrations
found in the core of the OMZ of the ETSP (< 5 µmol kg-1)
favor N2O consumption by denitrification, which is not observed in the
ETNA because of its comparably high O2 concentrations, and (ii) the
maximum observed N2O concentrations were higher in the ETSP than in the
ETNA. This is in line with the results of two model studies of N2O in
the ETSP by Zamora et al. (2012) and Cornejo and Farias (2012), which
suggested that the switching point between N2O production and N2O
consumption occurs at higher O2 concentration (∼ 8–10 µmol kg-1) than previously thought.
In contrast to the open ocean, OMZs in coastal (i.e., shelf) regions show a
higher spatial and temporal variability: seasonally occurring suboxic or
even anoxic/sulfidic OMZs have been observed in coastal regions worldwide
(see, e.g., Diaz and Rosenberg, 2008). One of the most prominent areas where
widespread sulfidic conditions have been recently observed is the shelf off
Peru (Schunck et al., 2013) (Sect. 5). Figure 6 shows the distribution of
N2O, water temperature, nutrients and H2S during the sulfidic
event described by Schunck et al. (2013) on the shelf off Peru during
December 2008/January 2009. Here, extreme N2O concentrations are found
at the boundary to the H2S containing bottom waters. No N2O is
found in the core sulfidic layer. This suggests again that there is a narrow
range of low O2 concentrations which is associated with exceptionally
high N2O production. As soon as the O2 concentrations are close to
zero (anoxic/sulfidic conditions), N2O production turns into N2O
consumption. Similar N2O distributions during anoxic/sulfidic events
were found off the west coast of India, in the Gotland Deep (central Baltic
Sea) and in Saanich Inlet (Brettar and Rheinheimer, 1991; Cohen, 1978; Naqvi
et al., 2000). Brettar and Rheinheimer (1991) suggested a close coupling
between H2S oxidation and NO3- reduction in a narrow layer
where NO3- and H2S coexist. This is in line with recent
findings from the anoxic event off Peru by Schunck et al. (2013) and similar
to the suggestion of a cryptic sulfur cycle where sulfate reduction is
coupled to rapid H2S oxidation by NO3- proposed for the OMZ
off Chile by Canfield et al. (2010).
The role of OMZs in trace gas emissions
In OMZs with O2 concentrations below 20 µmol kg-1, N2O
production does not take place in the core of the OMZ. Instead, N2O
production is found at the oxycline. Exceptionally high N2O
concentrations have so far only been found in temporarily occurring
anoxic/sulfidic regions off Peru/Chile and western India (Farías et al.,
2015; Naqvi et al., 2010). Stagnant sulfidic systems such as in the Baltic
and Black seas as well as the Cariaco Basin have shown only slightly
enhanced N2O concentrations at the oxic–anoxic interfaces (Bange et
al., 2010, and references therein). This implies that significant pulses of
N2O emissions to the atmosphere occur only when a shallow coastal
system rapidly shifts from oxic to anoxic/sulfidic conditions and vice versa
(Bange et al., 2010). This can be explained by a lag of N2O reduction
by denitrifiers when they switch from oxygen to nitrogen respiration
(Codispoti, 2010) or N2O production during the reestablishment of
nitrification after O2 ventilation (Schweiger et al., 2007).
Scheme of the (a) ETNA and (b) ETSP OMZs with major processes
identified. The O2 background is taken from SOPRAN cruise P399,
along 18∘ N in the ETNA, and from SFB754 cruise M77/3, along
10∘ S in the ETSP.
CH4 production is also tightly connected to OMZs (see overview in Naqvi
et al., 2010). Similar to N2O, upwelling areas are considerable
hotspots for CH4 emissions, although organic-material-enriched shallow
coastal zones such as estuaries and mangroves or shallow sediments with
geological CH4 sources show higher emissions (Bakker et al., 2014).
Since DMS is produced by phytoplankton in the euphotic zone, an accumulation
of DMS in OMZs appears unlikely. However, measurements at the Candolim
Time-Series Station (CaTS) on the shelf off Goa (India) revealed an
unprecedented 40-fold increase in DMS concentrations in the sulfidic layers
during an anoxic event (Shenoy et al., 2012). These high concentrations
could not be explained by any known pathways and may imply an unknown –
most likely microbial – DMS production pathway under anoxic conditions
either in the water column or in the underlying sediments (Shenoy et al.,
2012). Only recently it was shown that phytoplankton communities
exposed to anoxic conditions increase their DMS production significantly
(Omori et al., 2015). This implies a potential accumulation of DMS at
oxic–anoxic boundaries of coastal OMZs which, in turn, might result in high
DMS emissions from shallow coastal zones during anoxic/sulfidic events.
Trace gas production in OMZ and environmental changes
Trace gas production in OMZs is expected to be influenced primarily by
deoxygenation (Naqvi et al., 2010; Stramma et al., 2012). It is also
well known that eutrophication, warming and supply of limiting nutrients
(e.g. iron) will increase subsurface respiration of organic material, which
leads to deoxygenation in open-ocean and coastal OMZs (Bijma et al., 2013;
Gruber, 2011). Acidification of the upper ocean may result in a decrease in
calcium carbonate (produced by calcifying organisms), which can act as
ballast material for sinking organic matter. Less ballast means a reduction
in the sinking speed of organic particles, which could increase the
residence time of organic material and cause higher respiration rates
(Riebesell et al., 2009). Ongoing environmental changes such as
deoxygenation, eutrophication, warming and acidification have both direct
and indirect effects on trace gas production in OMZs. In general, we might
expect enhanced production of N2O, CH4 and DMS in OMZs because of
the ongoing loss of O2.
Deoxygenation in open-ocean and coastal environments may lead, on the one
hand, to enhanced N2O production when approaching the N2O
production–consumption switching point (see above), but, on the other hand,
when O2 concentrations fall below the switching point this may lead to
a consumption of N2O (Zamora et al., 2012). Moreover, we do not know
whether the frequency of coastal anoxic events will continue to increase and
how this may affect the coastal net N2O production/consumption. A
recent modeling study on the influence of anthropogenic nitrogen aerosol
deposition on N2O production revealed that the effect is small on a
global scale but that the OMZ of the Arabian Sea is especially sensitive to
atmospheric nitrogen deposition resulting in an enhanced N2O production
(Suntharalingam et al., 2012).
Conclusions
While there is a growing amount of data on primary production and the
pelagic N cycle in and associated with OMZ waters, quantitative estimates of
microbial production and respiration, particularly at ultra-low O2
levels, are still not fully explored. This translates into an uncertainty
concerning the origin of the N deficit. While it had been clearly
demonstrated that N loss processes respond sensitively to minimal changes in
O2 (Dalsgaard et al., 2014), a potential uncertainty may result from
additional processes, such as preferential P release directly in the water
column, may be important to create the N deficit in the water column. In this
context, the character and size of particles were shown important (DeVries
et al., 2014), linking P release from particles to the character of N loss
(Babbin et al., 2014). The character of the N loss/N deficit term is,
however, highly important, as it determines the extent of N depletion of the
entire OMZ due to the above-explained stoichiometric discrepancy between N
loss and N2 fixation. Interestingly, a strong impact of decadal climate
variations on respiration rates, primary production and the intensity of N
loss has been described for the South Pacific (Deutsch et al., 2011). This
may directly link to the character of N loss derived from our and other
measurements and has to be taken into consideration for future studies.
A coupling via the proposed primary production chain may indeed act in OMZs
associated with upwelling systems (an overview of major processes in the ETNA
and ETSP is depicted in Fig. 7). The important term of organic matter
export, either horizontally or vertically, needs more dedicated
investigations: to date, a quantification is missing of DOM supply via (sub)mesoscale
vertical transport processes out of the OMZ area and diapycnal mixing
sustaining microbial activity in the Peruvian OMZ. Further, for
POM supply to the OMZ, DVM seems to play a key role, despite some
quantitative uncertainties. Although some organisms performing DVM have
certain strategies to cope with anoxic conditions, mostly by down-regulating
their aerobic metabolism, there are limits for zooplankton and nekton. Thus,
a reduction of OM export by DVM may result in a further expansion and
deoxygenation of OMZs. Deutsch et al. (2014) describe in this context that a
decrease in the habitat caused by global warming and ocean deoxygenation
increases competition among species and may even result in a loss of
metabolic functionality by 20 %.
A quantification of DOM and POM import and export rates to and from the ETNA
is currently not available; an extensive discussion of POC dynamics from the
ETSP OMZs is provided in this issue (Dale et al., 2015). However, information
on the character of microbial processes responsible for POM degradation
within the OMZ is missing. First studies (e.g., Ganesh et al., 2014, 2015)
indicate a key role of particulate organic matter acting as microniches for
microbes and thus a host for certain processes such as microaerobic
respiration in OMZ waters. By containing strong redox gradients in relatively
narrow proximity, and by providing nutrients and trace metals, particles
might strongly influence biogeochemical cycles. It is well known that a
pronounced POM/particle-enriched turbid layer (a so-called intermediate
nepheloid layer) exists in the core of OMZs adjacent to coastal upwelling
regions, such as those found off Peru, Mauritania and the Arabian Sea (see,
e.g., Stramma et al., 2013; Naqvi et al., 1993; Fischer et al., 2009).
With regard to sulfidic events, which represent the lower limit of anoxia,
the positive feedback coupling could be thought to stabilize itself: while a
direct toxic effect of H2S on primary production is mostly mitigated by
the respective detoxifying community, decoupling of the supply of benthic
nutrients to the sea surface might decrease primary production. This may be
of particular importance in areas such as the ETSP, where the benthic supply
of, for example, trace metals is dominant. Resulting decreased respiration in the OMZ
could be thought to subsequently lead to regeneration to non-sulfidic, less
pronounced anoxia, which may stabilize the OMZ to a certain extent. However, whether
this hypothesis is valid needs to be resolved.
A critical consequence of ocean deoxygenation is visible from the comparison
of the ETSP and ETNA regions: massive supersaturation of N2O, connected
to sulfidic plumes, has been detected repeatedly in the ETSP. OMZs are
important sites of enhanced production of climate relevant trace gases such
as N2O, CH4, and DMS. N2O production is significantly
enhanced at oxic–anoxic boundaries of OMZs and we suggest that it mainly
results from habitat compression, where in extreme cases (such as sulfidic
events, sharpening gradients) nitrification and denitrification can occur
simultaneously. Maximum N2O concentrations and subsequent emissions to
the atmosphere have been observed in dynamic coastal systems that rapidly
shift from oxic to anoxic conditions and vice versa. Although OMZs are
usually not in direct contact with the atmosphere, their vicinity to coastal
upwelling systems plays an important role for oceanic emissions of
climate-relevant trace gases such as N2O, CH4, and DMS with
potential feedbacks on global warming, which then may again impact on ocean
deoxygenation. Our studies from the ETSP (Arévalo-Martínez, 2015, 2016; Kock
et al., 2016) confirm intense production of N2O in the coastal
upwelling. This is in line with an increase in N2O production from OMZ
areas as concluded from forced climate models. However, the same model
describes a global decrease in N2O formation by 4–12 %, mostly linked
to the western basins of the Pacific and Atlantic oceans (Martinez-Rey et
al., 2015).
Marine ecosystems and biogeochemical cycles are increasingly impacted by a
growing number of stress factors, some of which act locally, such as
eutrophication and pollution, while others act globally. Global stressors are
associated with anthropogenic carbon dioxide (CO2) emissions and affect
the ocean either directly through CO2-induced acidification or
indirectly through climate-change-induced ocean warming and deoxygenation
(Ciais et al., 2013). How these stressors will impact marine ecosystems and
biogeochemistry, individually or in combination, is still largely unknown.
Ocean warming, acidification and deoxygenation occur globally and
simultaneously, although with distinct regional differences. Through
increased stratification and decreased nutrient supply to the surface layer,
ocean warming is expected to decrease the biological production in the
already stratified low to midlatitudes.
While research on ocean warming is relatively advanced, far less is known
about the impacts of ocean acidification and deoxygenation on marine
organisms and ecosystems. Because the three stressors have mostly been
studied in isolation, knowledge on the combined effects of two or more of
them is scarce. In principle, additive, synergistic (more than additive) and
antagonistic (less than additive, i.e., compensatory) interactions of effects
are possible, but it is impossible to judge a priori what the combined effects will
be. One example of a synergistic effect is that of ocean acidification
narrowing the thermal tolerance window of some organisms, amplifying the
impact of warming (Pörtner and Farrell, 2008). However, we consider
interactions among stressors in marine communities largely understudied.
Outlook
Major issues remaining unresolved, in addition to those highlighted above,
concern (1) a mechanistic understanding of organic matter degradation and
nutrient cycling at low or variable oxygen concentrations in the water
column and the role of DVM for organic matter supply to the OMZ, (2) the
sensitivities of heterotrophic microbes and their sensitivity to low-oxygen
conditions, and (3) biogeochemical feedback processes in oxygen minimum
zones and their impacts on local to global scales.
Future studies in the framework of the SFB754 will combine measurements of
particle flux, zooplankton abundance, microbial activities and O2
concentrations in order to answer the following key questions:
What is the effect of low-oxygen conditions (below 20 µmol kg-1)
on organic matter degradation, and what is the partitioning between DOM and
POM in OMZ waters?
How do the rates of nutrient cycling and loss in OMZs relate to particles
and associated microniches?
What are the rates of oxygen supply and consumption in the upper OMZ, and
what is regulating respiration rates?
Do small-scale processes (e.g. viral lysis) affect fluxes on larger
scales, and how can models represent these important processes?
Acknowledgements
We thank IMARPE and INDP for close collaboration and support. We further
thank the authorities of Peru, Cape Verde and Mauritania for the permission
to work in their territorial waters. We acknowledge the support of the
captains and crews of R/V Meteor and the chief scientists. We thank
A. Dale for discussion of the benthic perspective of the manuscript.
Financial support for this study was provided by the DFG
Sonderforschungsbereich 754 (www.sfb754.de), the Max Planck Society (MPG) and the European Union (Marie Curie IEF to
C. R. Löscher, grant #704272). Edited
by: B. Currie
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