Anthropogenic Forcing and Global Carbon Cycle

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Annu. Rev. Mar. Sci. 2017.9:151-172. Downloaded from www.annualreviews.org
Richard Keil
School of Oceanography, University of Washington, Seattle, Washington 98195-5351;
email: rickkeil@uw.edu
Annu. Rev. Mar. Sci. 2017. 9:151–72 Keywords

First published online as a Review in Advance on organic carbon, carbonate, global carbon cycle, climate change,
November 2, 2016
Anthropocene, preservation, anthropogenic, sediment
The Annual Review of Marine Science is online at
marine.annualreviews.org Abstract
This article’s doi: Carbon preservation in marine sediments, supplemented by that in large
10.1146/annurev-marine-010816-060724
lakes, is the primary mechanism that moves carbon from the active sur-
Copyright c 2017 by Annual Reviews. ficial carbon cycle to the slower geologic carbon cycle. Preservation rates
All rights reserved
are low relative to the rates at which carbon moves between surface pools,
which has led to the preservation term largely being ignored when evalu-
ating anthropogenic forcing of the global carbon cycle. However, a variety
of anthropogenic drivers—including ocean warming, deoxygenation, and
acidification, as well as human-induced changes in sediment delivery to the
ocean and mixing and irrigation of continental margin sediments—all work
to decrease the already small carbon preservation term. These drivers affect
the cycling of both carbonate and organic carbon in the ocean. The overall
effect of anthropogenic forcing in the modern ocean is to decrease delivery of
carbon to sediments, increase sedimentary dissolution and remineralization,
and subsequently decrease overall carbon preservation.
151
INTRODUCTION
The ocean currently absorbs approximately 30% of the anthropogenic CO2 released each year to
the atmosphere (Heinze et al. 2015, Le Quéré et al. 2013). The fate of this carbon is to change
the acidity and alkalinity balance of the oceans (Doney et al. 2014, Heinze et al. 2015, Honisch
et al. 2012) and to be mixed into the deep ocean by circulation (Feely et al. 2004, Gruber et al.
2009, Sabine et al. 2004) or delivered to depth as carbonate mineral or organic carbon via the
biological pump (Berelson et al. 2007). Ultimately, it is either rereleased to the atmosphere or
buried in sediments (Ridgwell & Zeebe 2005). The burial of carbonates is the long-term (millennia
and longer) counterpoint to the volcanic release of CO2 to the atmosphere from geomorphic
decarbonation and is an important control on atmospheric CO2 over geologic time (Archer et al.
1998, Ridgwell & Zeebe 2005). Similarly, the burial of organic carbon is the counterpoint to
respiration and the burning of fossil fuels, and it influences the long-term carbon and oxygen
budgets of the earth (Blair & Aller 2012, Burdige 2007, Hedges & Keil 1995). The rock record
contains hundreds of times more carbonate than organic carbon, illustrating the unequal control
the two forms have over the long-term geologic carbon cycle (Morse & Mackenzie 1990, Ridgwell
& Zeebe 2005).
The factors and mechanisms that enhance or diminish carbonate and organic carbon burial
in sediments thus represent important valves that control the flow of carbon from the active or
surficial carbon cycle back into the long-term geologic cycle. There have been many reviews of
these mechanisms (Archer 1996, Blair & Aller 2012, Burdige 2007, De La Rocha & Passow 2007,
Goni et al. 2009, Hales 2003, Ridgwell & Zeebe 2005), especially for organic matter, but few treat
the two carbon components simultaneously or evaluate the influence of anthropogenic change
on various carbon preservation mechanisms. Burdige (2007), Blair & Aller (2012), and Ridgwell
& Zeebe (2005) have provided concise reviews of modern marine organic carbon preservation,
terrestrial carbon in the ocean, and the geologic carbonate cycle, respectively. In this review, I
broadly outline the path that marine carbon must take in the ocean in order to be preserved in the
rock record and explore hypotheses about how preservation mechanisms might be responding to
anthropogenic change.
Two fundamental questions to begin with are, What proportion of the anthropogenic CO2
entering the ocean is from carbonate mineral weathering as opposed to fossil fuel burning, and do
the earth’s natural processes attempt to balance sinks in equal measure to the sources? Humans
alter the inorganic rock weathering cycle largely via cement production, which accounts for ∼6%
of all CO2 emissions (Le Quéré et al. 2013), and by altering the landscape and promoting erosion
and rock weathering (Beaulieu et al. 2010, Regnier et al. 2013, Roy et al. 1999). One effect of
weathering is to remove CO2 from the atmosphere, which does very little to offset anthropogenic
emissions. Approximately half of the CO2 released from cement production is due to fossil fuel
combustion that powers cement production, and the other half is CO2 directly released from
carbonates (limestone) during the heating process that produces the calcium oxide needed to
make cement. Thus, only approximately 3% of CO2 emissions are from alterations of the carbonate
system, and 97% are from fossil fuel burning (or other organic carbon–related components, such as
deforestation). Even though the earth contains most of its carbon in inorganic form, anthropogenic
forcing is largely through organic carbon cycling. One impact of this is that both the carbon and
oxygen cycles are being measurably perturbed (Keeling et al. 1996, 2010).
Does the ocean bury anthropogenic carbon in this same proportion of approximately 30 organic
carbons per 1 carbonate carbon? To answer this question, one needs to understand the manner
in which carbonate and organic carbon reach ocean sediments (e.g., the biological pump) and
the mechanisms promoting preservation within sediments. These are among the great challenges
152 Keil
facing oceanographers today (Doney et al. 2014, Heinze et al. 2015). Studies that have evaluated
carbonate and organic carbon transfer to the deep sea generally show a dominance of organic
carbon in the near-surface sinking flux (Chikamoto et al. 2009, Klaas & Archer 2002, Lamborg
et al. 2008, Mekik et al. 2007). However, the ratio near the sediment bed is often closer to 1:1
than it is to 30:1 (Klaas & Archer 2002, Mekik et al. 2010, Wilson et al. 2012), suggesting at first
glance that the modern ocean might bury carbonate in response to the anthropogenic burning
of organic carbon. Delivery to sediments does not guarantee preservation, though, and a myriad
of mechanisms acting at a variety of scales in time and space combine to control carbonate and
organic carbon preservation in marine sediments.
A MARINE CARBON BURIAL MAP AND BUDGET

The amount of seafloor available to sequester carbonate and organic carbon is vast. For a variety
of reasons, the locations where inorganic and organic carbon are concentrated do not significantly
overlap (Figure 1).
The organic carbon contents of sediment rarely exceed 5 wt%, and the majority of sediments
enriched in organic carbon occur in relatively shallow water along continental margins or in shadow
areas underneath oxygen-poor waters (Burdige 2007) (Figure 1). In sediments, organic carbon
preservation is largely a battle between protection via mineral interactions and remineralization
via microbial activity (with some important exceptions that lead to the development of oils and
shales) (Keil & Mayer 2014). In shallow sediments where the delivery of both organic carbon and
protective minerals is high, a larger percentage of the organic matter can be preserved. Similarly,
in areas where the mechanical and microbial attack of organic carbon is minimized (quiescent
oxygen-poor environments), more organic carbon can be preserved (Hartnett & Devol 2003,
Kennedy et al. 2006, Sánchez et al. 2013). That is, the ocean is very effective at organic carbon
remineralization, and only certain locations bury significant amounts of organic carbon. These
locations are predominately along active margins accumulating sediment and under the ocean’s
permanent oxygen-deficient zones (Figure 1).
Carbonate cycling is somewhat the opposite; preservation is the norm, but certain locations
in the ocean overcome the inherent stability of carbonates and force dissolution. Production of
carbonate minerals (largely calcite and aragonite) in the modern ocean is strongly dominated by
biological processes and occurs both in overlying waters and in sediments (Morse & Mackenzie
1990). Dissolution is related to the relative stability of the carbonate crystalline structure, with
aragonite being less stable than calcite. Stability is determined by the ambient concentrations
(activities) of calcium ions (Ca2+ ) and carbonate ions (CO3 2− ) in the solution surrounding the
mineral, expressed as a saturation state or solubility ratio, , defined as [Ca2+ ] × [CO3 2− ]/Ksp ,
where Ksp is a solubility constant for each mineral phase (Ridgwell & Zeebe 2005). In addition,
depth in the ocean is an important constraint on because Ksp increases with pressure. Carbonate
phases are thermodynamically stable when > 1 and prone to dissolution when < 1. Approx-
imately 70% of the sediments at the ocean floor currently lie under supersaturated (stable) water
with respect to carbonates.
The major basins of the ocean (e.g., the North Pacific) have roughly equal maximal depths and
proportional depth distributions (Morse & Mackenzie 1990), meaning that the effect of pressure on
carbonate dissolution ought to be more or less constant from ocean basin to ocean basin. However,
the other driver of carbonate stability, namely the CO3 2− concentration in seawater, increases
along the path of deepwater circulation. This is because as deep water moves along the conveyor
belt from the North Atlantic through the Southern Hemisphere and Indian Ocean on its way to the
www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 153

a Carbonate
b Organic carbon
Figure 1
Areas with a high weight percent of (a) carbonate and (b) organic carbon in marine sediments. Data from
Seiter et al. (2004) were imported into Ocean Data View 4.7.6 and then redrawn to highlight the highest
20% of data. In panel a, the orange regions have sediments that are ∼70% or more carbonate; in panel b, the
orange regions have sediments that are ∼1.5% or more organic carbon. Note that the organic carbon
contents of sediments can rise as high as 20 wt%.
North Pacific, it receives a continuous rain of organic carbon that is undergoing remineralization,
resulting in carbonic acid (H2 CO3 ) production. The addition of acid shifts the carbonate system
of seawater away from CO3 2− and thus lowers . The result is that deep water in the North
Pacific is undersaturated, and carbonate preservation does not occur. Global maps of sedimentary
carbonate concentrations reflect low sediment accumulation rates, the relative lack of the mineral
materials to dilute carbonates in the open ocean, and the effects of dissolution (Figure 1).
When looking at the large swaths of seafloor that are carbonate rich relative to the continental
margins (∼20% of the area of the ocean) containing organic carbon, it is tempting to infer that
154 Keil
the modern ocean is preserving carbonate far in excess of organic carbon. This view is consistent
with the fact that the interior of the earth contains many times more carbonate than fossil fuel
carbon and with observations that carbonate preservation in sediments is an important buffer on
climate and atmospheric CO2 over geologically short (millennial) periods of time. However, the
modern ocean does not conform to this expectation.
Estimates of total carbon preservation in ocean sediments vary widely, and there is concern
that budgets are not well constrained (Burdige 2007). Adding together carbonate and organic
carbon preservation yields global total carbon preservation ranges of 0.06–3.5 Pg C y−1 (Burdige
2007, Regnier et al. 2013, Sarmiento & Gruber 2002, Sarmiento et al. 2010). Most global budgets
for carbonate and organic carbon suggest that burial of organic carbon is equal to, or higher
than, that of carbonate (Archer et al. 2002, Burdige 2007, Hedges & Keil 1995, Middelburg et al.
1997). With the addition of fjords and other marine coastal embayments as major sinks for carbon
(Nuwer & Keil 2005, Shields et al. 2016, Smith et al. 2015), and after taking into consideration
the accounting efforts of Burdige (2007), I estimate that organic carbon preservation in the ocean
is 0.35 Pg C y−1 . Similar numbers are obtained for freshwater systems (0.35 Pg C y−1 ), which
can preserve organic carbon for tens of thousands of years or longer (Dean & Gorham 1998).
Complicating these estimates is that anthropogenic forcing shifts approximately 1 Pg C y−1 from
land to sea (Regnier et al. 2013), and the fate of this carbon is largely unconstrained (Blair & Aller
2012, Hedges et al. 1997).
Carbonates are not produced or stored in freshwater systems to any discernible degree (Morse
& Mackenzie 1990, Ridgwell & Zeebe 2005). Assessments for marine waters are on the order of
0.30 Pg C y−1 (Berelson et al. 2007, Berner et al. 1983, Morse & Mackenzie 1990), split equally
between slow preservation spread out over the open-ocean floor and faster preservation along
the margins (especially reef communities). Thus, total carbon preservation in aquatic systems is
∼1 Pg C y−1 , with large uncertainty. In terms of total preservation, approximately 80% of both
carbonate and organic carbon occurs in shallow coastal or fresh waters.
In reflecting back on our initial question, the modern carbon cycle seems to bury organic matter
in aquatic ecosystems at a 2:1 preference over carbonate, and in marine systems at a ratio of 1:1,
well below the 30:1 ratio at which humans are extracting the two components from the geologic
cycle.
PROCESSES IN OCEAN WATER
Production
Nothing can be preserved if nothing is produced; thus, carbon preservation ultimately must relate
back to production. Carbonate and organic carbon production far exceeds their preservation, and
on average, <10% of the carbonate and <1% of the organic carbon produced in the ocean are
preserved in sediment (Archer 1996, Dunne et al. 2007, Hedges & Keil 1995). The major fate of
carbon is therefore to be remineralized. Nonetheless, carbonate and organic carbon preservation
can be approximated, to a first degree, from estimates of primary production and assumptions about
processing, sinking, and burial (Berelson et al. 2007, Dunne et al. 2007, Müller & Suess 1979).
Consequently, although direct control of preservation by production is weak at best (Burdige
2007), there is the possibility that anthropogenic alterations of oceanic primary production also
change carbon preservation.
Although much remains to be learned (a general theme of this review), primary production
in the oceans seems to be responding negatively to climate change, with production decreasing
overall and shifting seasonally (Dave & Lozier 2013, Henson et al. 2013, Laufkotter et al. 2015)

Diminishes preservation
Enhances preservation
Shifts to smaller Nitrogen deposition

primary producers
Warming
Decreased sinking speeds Deoxygenation and eutrophication

Decreased
sediment Increasing rain ratio Oxygen-deficie
delivery nt zone
Ocean acidification cline

Lyso
Shoaling lysocline
Benthic trawling
Diminished benthic communities ?
Carbon burial
Figure 2
Various identified impacts of anthropogenic change on carbon preservation in the ocean.
(Figure 2). This may be largely due to warming of the oceans leading to enhanced stratification,
which chokes upwelling and creates nutrient stress for phytoplankton. The size of nutrient-poor
ocean deserts in the Pacific and Atlantic increased by 15% from 1998 to 2006 (Polovina et al. 2008).
All else being equal, a decrease in annual primary production of 0.4% (0.19 Pg C y−1 out of an
oceanic average of 50 Pg C y−1 ) (e.g., Behrenfeld et al. 2006) might result in a similar reduction in
carbon preservation. However, other forms of anthropogenic forcing enhance production. Fixed
nitrogen deposition to the ocean surface has increased substantially since the beginning of the
mass Haber reduction of N2 for industrial and agricultural purposes (Kim et al. 2014), and this
nutrient input may offset a portion of the production lost because of changes in stratification and
nutrient regeneration (Figure 2).
It may be that the major influence of production is in determining the types of carbonate and
organic carbon created, which is governed by the composition of phytoplankton and zooplankton
communities (Mekik et al. 2007, Moore et al. 2012, Prahl et al. 2000). For organic carbon, some
plankton make unusual organic compounds that can be difficult for microorganisms to effectively
degrade in sediments (e.g., algaenans; Gelin et al. 1996), leading to enhanced preservation (Burdige
2007). It is not known whether algaenan-type production in the modern ocean is being positively
or negatively affected by anthropogenic change, but a best guess would be that algaenan production
156 Keil
is reduced, because anthropogenic forcing is associated with shifts in community structure toward
smaller autotrophs that are not known to make algaenan-type structures.
For carbonates, biomineral production is either the more soluble aragonite (∼15% of ocean-
wide carbonate production) or the less soluble calcite (∼85% of carbonate production) (Morse &
Mackenzie 1990), with wide variations in molecular-level mineralogy (e.g., strontium and magne-
sium contents). Climate models and field data suggest that a warming and acidifying ocean results
in an altered food web containing fewer aragonite-producing organisms (Ridgwell & Zeebe 2005).
Whether this directly affects carbonate preservation is unclear because aragonite is not normally
well preserved in marine sediments.
The role of community structure in determining the sinking flux is complex and may be more
important than the exact carbonate mineral or organic matter produced (Hedges et al. 2002,
Kortzinger et al. 2001). Anthropogenically forced shifts in primary production away from larger
algae to picophytoplankton (Doney et al. 2014, Heinze et al. 2015) and secondary consumers
(Purcell et al. 2007) have the potential to dramatically alter carbon preservation (Hoegh-Guldberg
& Bruno 2010, Morán et al. 2010) because they alter the way in which carbon is packaged and
sent to the ocean floor.
Sinking Particles
After carbonates and organic carbon are produced, they need to reach the sediment to be pre-
served in the geologic record. This, it turns out, is a difficult path, filled with microbial attack,
remineralization, and dissolution. It is here that the vast majority of sinking carbon is remineral-
ized back into the dissolved inorganic carbon pool (Buesseler & Boyd 2009, Collins et al. 2015,
Lam & Marchal 2015, Lutz et al. 2002, Marsay et al. 2015). Because of this, small changes in the
efficiency of particle transport can have large impacts on the preservation of carbon in sediments
(Abramson et al. 2010, Buesseler et al. 2007b, Iversen & Ploug 2013, Vidya et al. 2013) (Figure 2).
For example, changing sinking speed or remineralization rates by as little as 5% can change the
e-folding depth for carbon export by hundreds of meters (DeVries et al. 2012).
The transfer of carbon to the interior of the ocean and toward the seafloor is dominated by
the biological pump (DeVries & Deutsch 2014, DeVries et al. 2012, Henson et al. 2011, Lam
& Marchal 2015, Sanders et al. 2014, Wilson et al. 2012), in which material produced in the
surface mixed layer is packaged into sinking particles. The biological pump is quite complex and
performs other functions as well, including regulating to some extent the pCO2 content of the
atmosphere, regenerating nutrients to support further primary production, and creating dissolved
organic carbon that can be advected throughout the ocean. Respiration and dissolution of carbon
delivered to the ocean’s interior also produce acidity and consume oxygen, making the biological
pump one of the most fundamentally important components of the ocean with regard to carbon
cycling (Buesseler & Boyd 2009, Burd et al. 2010, Honjo et al. 2014).
The export of carbon from surface waters is characterized by rapid remineralization of carbon-
ate and organic carbon in shallow subsurface waters (to 1,000 m, the so-called twilight zone) and
slower remineralization in deeper waters. On an ocean-average basis, alkalinity budgets show that
remineralization of carbon in the twilight zone is ∼90% organic carbon, and in deep water the
split is roughly 60% organic carbon and 40% carbonate (Emerson & Hedges 2008). The result
is that, although the material exported from the surface is rich in organic carbon, the material
reaching the sediment is much less so (Chikamoto et al. 2009, Lamborg et al. 2008, Mekik et al.
2007, Seiter et al. 2010).
Once primary production and secondary production have been packaged into sinking material,
the two main drivers controlling delivery to sediments are how fast the material sinks and how

fast it is remineralized (Buesseler & Boyd 2009, Buesseler et al. 2007a, Burd et al. 2010). Neither
of these parameters is easy to directly measure. Complicating things is the fact that the primary
computational tool used to evaluate sinking fluxes has been the Martin curve (Martin et al. 1987), in
which the two terms are combined into a single unit-less exponent of a power function (Buesseler
et al. 2007b). There are a number of reasons why oceanographers are slowly pulling away from
the Martin curve, one being that it is somewhat insensitive to changes in flux within the twilight
zone, where the majority of the organic carbon remineralization occurs. Buesseler et al. (2007a,b)
began calculating transfer efficiencies, which are the percentages of the flux leaving the mixed
layer that make it to a designated depth, usually 500 m. They found that transfer efficiencies for
organic carbon vary by as much as three times over short spatial and temporal scales (kilometers
and days), showing great variability in flux attenuation in the upper ocean.
Part of the variability is related to the sinking speed, which is strongly dependent on source
compositions, zooplankton repackaging, and additions of lithogenic material to the flux (wind-
derived or nearshore nepheloid layers) (Berelson 2002, Chikamoto et al. 2009, Klaas & Archer
2002, Kriest & Oschlies 2008, Villa-Alfageme et al. 2014). Sinking speeds are correlated with
carbonate and other ballast materials that have relatively high densities and promote relatively fast
sinking (McDonnell & Buesseler 2010). Sinking velocities range over several orders of magnitude
(meters to thousands of meters per day), and a single sinking velocity typically cannot be assigned to
the flux because different particle sizes have different sinking speeds (Kriest & Oschlies 2008, Villa-
Alfageme et al. 2014) and because particles can undergo a variety of packaging, disaggregation,
and repackaging processes during settling (De La Rocha & Passow 2007, Wilson et al. 2008).
Interestingly, sinking speeds generally increase with depth, implying that at depth the sinking
speed is a primary driver of flux attenuation, whereas in surface waters it is less important (Berelson
2002). High sinking speeds have been related to packaging of material into discrete zooplankton
pellets and to mass sinking of diatoms and calcareous plankton (McDonnell & Buesseler 2010),
suggesting that community structure plays an important role in controlling the composition and
delivery of carbon to the deep sea. If anthropogenic forcing is moving community structures
away from larger phytoplankton and decreasing zooplankton distributions (Hays et al. 2005),
the effect could be lower sinking speeds for carbon through the ocean (see also Schneider et al.
2008). Slower sinking provides more time for remineralization within the water, which reduces
preservation (Figure 2).
Organic carbon remineralization rates are difficult to directly measure, but estimates made
using sensor-equipped sediment traps and by directly evaluating or probing discrete fecal material
provide rate constants that vary widely, from 0.01 to 0.5 d−1 (Belcher et al. 2016, Boyd et al.
2015, McDonnell et al. 2015). The causes of this great variability are unknown but may be re-
lated to temperature (Iversen & Ploug 2013, Marsay et al. 2015), protection by mineral phases
(Armstrong et al. 2002, Lee et al. 2009a), or the inherent lability of different organic carbon
molecules (Wakeham et al. 1997).
Temperature effects on the sinking flux of organic carbon (Iversen & Ploug 2013, Marsay et al.
2015) indicate more effective remineralization at higher temperatures. Given the anthropogeni-
cally induced rise in surface water temperatures, it is expected that organic carbon remineralization
in the upper water column is increasing, leading to less delivery to sediments and less preservation
(Bopp et al. 2013, Chavez et al. 2011, Doney et al. 2012, Iversen & Ploug 2013, Marsay et al.
2015, Somero 2012) (Figure 2).
Oxygen-deficient waters can also influence sinking particle organic carbon remineralization
(Hartnett et al. 1998, Keil et al. 2016, Van Mooy et al. 2002). This appears to be a threshold
effect, with little impact when oxygen is above ∼20 µM (Keil et al. 2016). However, once oxygen
158 Keil
levels drop below this level, the ecosystem changes, with many aerobic organisms avoiding the
low-oxygen waters (Wishner et al. 2008, 2013) and changing particulate microbial communities
(Ganesh et al. 2014, Parris et al. 2014, Ulloa et al. 2012). The result is that the efficiency of
transfer to depth increases for organic carbon under low-oxygen conditions (Hulthe et al. 1998,
Keil et al. 2016, Roullier et al. 2014). Anthropogenic forcing is leading to reduced oxygen content
in the ocean and expanding oxygen minimum zones (Keeling et al. 2010), which, if the above
mechanisms stand, will lead to enhanced delivery of organic carbon to the seafloor and perhaps
increased preservation (Figure 2).
As carbonate minerals sink through the water column, conditions within the sinking material
can promote dissolution (Berelson et al. 2007; Chikamoto et al. 2009; Feely et al. 2002, 2004;
Hales 2003; Lee et al. 2009b). This dissolution is largely due to the simultaneous remineralization
of organic carbon in the sinking particles, which produces H2 CO3 , reduces CO3 2− concentra-
tions, and lowers the saturation state of the water surrounding the carbonate mineral. Carbonate
dissolution associated with organic carbon remineralization accounts for at least 50% of the car-
bonate dissolution that occurs within the water column (Berelson et al. 2007, Feely et al. 2004).
As the oceans assimilate anthropogenic CO2 , the extent of dissolution will likely increase be-
cause surface waters will be nearer to saturation as a particle journeys through the water. This
ocean-acidification-enhanced dissolution in the upper water column will add to the dissolution
that occurs below the carbonate saturation depth. The overall impact of anthropogenic forcing
(warmer water, fewer carbonate-producing organisms, and increased acidity of shallow waters) will
be to increase carbonate dissolution in open-ocean waters and decrease carbonate preservation in
sediments (Fabry et al. 2008, Orr et al. 2005) (Figure 2).
Ocean acidification has an additional effect: It shoals the lysocline, the depth at which un-
dersaturation begins to have a significant impact on carbonate dissolution (Boudreau et al. 2010,
Chikamoto et al. 2009, Hales 2003). The lysocline of the North Atlantic, where deep water forms,
is being affected first, and it is anticipated that by the year 2100 much of the ocean will be near or
below the saturation values for both aragonite and calcite (Feely et al. 2004, 2009; Honisch et al.
2012) (Figure 2).
It is important to note that if no CO2 were added to deep seawater via organic carbon re-
mineralization, then virtually none of the seafloor would be overlain by undersaturated water
(Morse & Mackenzie 1990). This serves as a reminder of how intimately organic and inorganic
carbon cycling are related. This interrelation is often expressed as the rain ratio, or the ratio of
organic to inorganic carbon in sinking particles (Lamborg et al. 2008, Mekik et al. 2007). The
rain ratio is important for oceanic regulation of atmospheric pCO2 over millennia (Mekik et al.
2012). Quantifying changes in the rain ratio over space and time reveals how ecosystems respond
to anthropogenic forcing. For example, changes in community structure and thus in the rain ratio
might be driven by variation in the chemistry of upwelled waters or the supply of aeolian mi-
cronutrients. Alternatively, the rain ratio can remain relatively constant if carbonates act as the
dominant ballast for sinking organic carbon.
The rain ratio influences ocean chemistry and atmospheric pCO2 via its importance in deter-
mining the sedimentary dissolution of carbonate. The saturation state of sedimentary pore waters
is influenced not only by the saturation state of the overlying water, but also by the amount of
metabolic CO2 released during remineralization of organic matter (Ridgwell & Zeebe 2005). Sim-
ply put, any change in the ratio of organic carbon to carbonate alters the fraction of carbonate that
dissolves. Models predict an atmospheric CO2 sensitivity of approximately 1.6 ppm per percent
reduction in carbonate or organic carbon rain (Ridgwell & Zeebe 2005). Thus, atmospheric CO2
can be modulated by changes in the rain ratio to marine sediments.

AT THE SEAFLOOR
Once carbon reaches the seafloor, its chances of being preserved go up dramatically if it is organic
carbon and go down if it is carbonate. Organic carbon burial efficiencies for material that hits the
seabed average approximately 10–20% (Burdige 2007), 10–40 times higher than that for material
leaving the surface. The reason for this, generally speaking, is that the organic matter reaching the
sediment has already undergone extensive remineralization, and consequently its overall reactivity
has decreased substantially—the degradation-resistant material has survived the transition through
the water column. The factors controlling reactivity remain poorly known; in a compilation of
250 data sets, Arndt et al. (2013) found no overlying mechanisms (delivery rate, water depth,
etc.). The other factor promoting preservation is that the organic carbon mixes and interacts with
mineral grains in ways that help protect the organic carbon from degradation (Keil & Mayer 2014,
Reimers et al. 2013).

Preservation of carbonate does not follow such a (relatively) simple rule. Carbonate preservation
varies dramatically depending on three things: water depth, water chemistry, and organic carbon
reactivity (Berelson et al. 2007, Chikamoto et al. 2009, Gattuso et al. 1998, Hales 2003, Huettel
et al. 2014, Ingalls et al. 2004).
Organic Carbon Preservation

Many mechanisms can lead to organic carbon preservation, and they can be placed into three
categories: mechanisms that prevent the remineralization of carbon that is otherwise reactive,
mechanisms that transform reactive organic carbon into enzymatically unrecognizable (and thus
hard-to-degrade) geopolymers, and properties that inherently prevent specific organic carbon
from being degraded. Burdige (2007) and Keil & Mayer (2014) have provided expansive reviews
on this subject. One aspect of organic carbon preservation not treated extensively here is the fate
of terrestrial carbon delivered to the sea; the recent review by Blair & Aller (2012) provides an
excellent overview of this issue.
The majority of sediments in the ocean that contain 2% or more organic carbon by weight carry
that carbon in proportion to the mineral surface area available to sorb to or interact with (Mayer
1994, Mayer et al. 2004). This, in and of itself, strongly argues that the mechanisms that ultimately
lead to organic carbon preservation are related to some sort of interaction with inorganic phases.
Because much of the inorganic material accumulating in the ocean is of terrestrial origin, organic
carbon preservation is likely tightly coupled with interactions at the land-sea interface (Blair &
Aller 2012, Hedges et al. 1997, Keil et al. 1997) (Figure 3).
Physical protection. Physical protection is, for the most part, the dominant mechanism that
leads to organic carbon preservation, especially in nearshore locations (Arnarson & Keil 2007,
Keil & Mayer 2014, Mayer 2004, Mayer et al. 2004). Protection can take on a variety of forms
and can be broken by a variety of mechanisms.
Organic matter can encapsulate other organic matter within hydrolysis-resistant matrices such
as pollen grains or algaenans (Knicker & Hatcher 1997). Similarly, biominerals often contain and
protect organic matrix materials such as template proteins and long-chain polyamines (Bridoux
& Ingalls 2013, Bridoux et al. 2012). Carbonates protect intercrystalline organic carbon (Ingalls
et al. 2004). Another form of physical protection is via chelation with, or coprecipitation with,
iron (Lalonde et al. 2012, Shields et al. 2016).
Sorption to mineral grains (either biominerals or lithogenic minerals) can significantly re-
duce remineralization rates (Arnarson & Keil 2005, Keil & Mayer 2014, Schneider et al. 2010).
160 Keil
a OC b OC:SA
Strait of Juan de Fuca
Columbia River
Figure 3
Impact of terrestrial sediment delivery and transport on carbon preservation along the Washington margin of the North Pacific.
(a) Areas with a high weight percent of organic carbon (OC) in the margin sediments, showing depocenters along the canyons where
terrigenous lithogenic materials flow and are deposited. The orange regions have sediments with an OC content above ∼2.4 wt%.
(b) Relationship between OC content and mineral surface area (SA). A normal continental margin relationship would be an OC:SA
ratio of ∼1.0 (i.e., ∼1.0 mg OC m−2 ) (Keil et al. 1994, Mayer 1994); the orange regions have a ratio above ∼1.25. Only sediments
along the transport path contain typical loadings, and the remainder have lower OC loading caused by enhanced oxygen exposure.
These images highlight the dynamic nature of the continental margin, its role in moving carbon offshore, and the importance of
terrestrially derived minerals for the preservation of marine carbon. Adapted from Nuwer (2008).
Resistance to degradation may be imparted by the strong covalent bond associated with sorption
(Schneider et al. 2010), via protection from enzymatic attack when sorption occurs within meso-
pores (Mayer et al. 2004), or by stabilization of macromolecules on surfaces where multiple points
of contact flatten the macromolecule and make it both resistant to enzymatic attack and highly
unlikely to desorb (Keil & Mayer 2014).
Selective preservation. Selective preservation consists of three known types: production of

algaenan-like biochemicals in the water column that are effectively transferred and buried
within sediments (Gelin et al. 1996), secondary production of bacterial necromass in sediments,
and reburial of organic matter that has passed through the geologic cycle (e.g., black carbon;
Dickens et al. 2004). Selective preservation remains somewhat of an unknown; analytical con-
straints prevent a deeper understanding of macromolecules because many defy current identifica-
tion approaches, necromass is more a concept than an identifiable component of organic carbon,
and variable amounts of black carbon are remineralized prior to reburial, making budgeting of
black carbon fluxes difficult (Blair & Aller 2012).
Algaenan organic matter consists of insoluble, nonhydrolyzable, highly aliphatic biomacro-
molecules in protective tissues of some microalgae and higher plants. Their presence in marine
sediments in nearly intact condition (based on electron microscopy) suggests that they are selec-
tively preserved and subsequently enriched in sedimentary organic matter during burial, despite
their relatively small concentrations in the original biomass (de Leeuw et al. 2006, Gelin et al.
1999). This organic carbon produces n-alkanes, which make up the bulk of high-wax crude oils in
reservoirs, suggesting that selective preservation of organic carbon may be geologically important
and may be responsible for the fossil fuel being consumed today (de Leeuw et al. 2006, Gelin et al.
1997).

In sediments, when bacteria die, their biomass turns to necromass (Lomstein et al. 2012). This
organic carbon is not necessarily intact cells but is composed of cell lysis products, membranes,
and cell walls. Although most necromass is likely derived from sediment bacterial biomass, some
of this material may also come from sinking particles (Burdige 2007).
Finally, the third type of selective preservation—and it is a bit of a cheat to place this material
here—is organic material that has already passed through the geologic process and has been
reweathered (Blair & Aller 2012, Burdige 2005). This fossil organic carbon, sometimes called
black carbon or kerogen (though these terms also have specific meanings), is refractory via its
geologic history. Part of that history includes humification.
Humification. Humification is the term typically used by oceanographers to identify geopoly-

merization reactions that occur during early diagenesis (where “early” means within the first
∼100–1,000 years). During microbial processing of organic material, low-molecular-weight ma-
terials may be removed from the system as dissolved organic carbon, after which they may react
together to form chemically complex macromolecules broadly referred to as humic substances

(Collins et al. 1995). Some organic carbon may undergo abiotic condensation reactions, whereas
other material may be retained by ionic and chelation reactions. These hydrophilic and amorphous
forms of organic carbon are resistant to biological decay and thus potentially constitute a major
form of preserved (and reweathered) organic carbon. Unfortunately, there is little direct evidence
to support the occurrence of humification in marine systems during early diagenesis, and under
most conditions, the abiotic reactions proceed at such a slow rate that they are best described as
postpreservational processes (Burdige 2007, Derenne & Largeau 2001, Keil & Mayer 2014).
Breaking Organic Carbon Protective Mechanisms

Once organic carbon is in a sediment and is mixing with lithogenic and biomineral phases, most
of which are delivered laterally via river flow rather than from above, many of the protective
mechanisms described above kick in. Thus, the questions at hand are, What processes override
organic carbon protections, and is anthropogenic forcing likely to change them?
For a host of direct and indirect reasons, the major determinant that overrides sedimentary
organic carbon preservation is exposure to oxygen (Arnarson & Keil 2007, Burdige 2007, DeVries
& Deutsch 2014, Hartnett et al. 1998). Oxygenic systems add an entire array of processes that work
to remineralize organic matter. Benthic macroorganisms process sedimentary material through
their guts, releasing and remineralizing organic carbon (Mayer et al. 1997). Benthic organisms
also bioturbate sediments and renew pore waters (Aller et al. 2008), both of which can lead to
enhanced remineralization (Hulthe et al. 1998). Redox oscillations can lead to changes in iron
chemistry and release organic carbon bound to iron (or manganese); can mix organic materials of
different reactivities, leading to an effect called priming; and can introduce oxygen into sediments,
where the oxygen can react directly with organic carbon (Blair & Aller 2012, Burdige 2007).
Anthropogenic forcing is altering organic carbon preservation in sediments in ways that have
yet to be quantified and placed into global carbon cycles. There are currently four main effects:
decreased delivery of lithogenic mineral to the sea (Syvitski & Milliman 2007, Yang et al. 2007),
decreased abundance of benthic macroorganisms ( Jones et al. 2014), increased irrigation and
sediment mixing caused by benthic trawling (Thrush & Dayton 2002, Watling & Norse 1998),
and eutrophication (Daskalov 2002, O’Neil et al. 2012, Purcell et al. 2007, Smith 2003) (Figure 2).
Damming of rivers has decreased the delivery of lithogenic mineral to the ocean by at least
30% per year (Syvitski & Milliman 2007). Because organic carbon preservation is so intimately
linked to sediment delivery and transport, decreased sediment discharge to the ocean leads to
162 Keil
decreased burial of carbon in the ocean (e.g., Figure 3). Assuming an average surface area of
25 m2 g−1 (Adams & Bustin 2001, Hedges et al. 1999, Mayer et al. 2004), an equivalence of 1 mg
of organic carbon per square meter of surface area (Bock & Mayer 2000, Keil et al. 1994, Mayer
1994), and a decrease in sediment delivery of 1.4 × 1015 g y−1 (Syvitski et al. 2005), each year the
oceans preserve 0.04 Pg C less than they otherwise would. Interestingly, retention of sediment
behind dams is estimated to bury perhaps as much as 0.1 Pg C y−1 (Aufdenkampe et al. 2011),
but it is unlikely that sediment trapped behind dams will ultimately be sent to the geologic cycle
intact.
Anthropogenic forcing alters benthic communities and leads to decreased abundances of
macroorganisms ( Jones et al. 2014). Given predictions of diminished carbon fluxes, future ocean
sediments are expected to adapt by favoring smaller benthic organisms, lower energy transfer,
less bioirrigation, and less sediment mixing. It is estimated that as much as 80% of the potential
deepwater biodiversity hot spots known around the world, including canyons, seamounts, and
cold-water coral reefs, will experience negative changes in biomass. The effect of this will likely
be minimal in terms of carbon storage and preservation, as remineralization and dissolution in the
deep sea are not known to be strongly sensitive to changes in macroorganism activity (e.g., Murray
& Grundmanis 1980). An alternative impact is that organic carbon preservation in the deep sea
will be enhanced. Because biomechanical action, pore-water irrigation, and sediment mixing are
critical components that promote organic carbon remineralization, reduction in these variables
might lead to a small enhancement in organic carbon preservation (Figure 2).
Another anthropogenic process that affects benthic communities negatively is benthic trawling
for seafood (Thrush & Dayton 2002). This has been likened to clear-cutting a forest (Watling &
Norse 1998) and has two conflicting impacts on carbon preservation. On the one hand, removal
of benthic organisms should increase carbon preservation; on the other hand, large-scale mixing
of sediments should promote redox oscillation and organic matter priming (where the presence of
easily degraded organic carbon promotes the further degradation of recalcitrant material), both
of which should reduce carbon preservation. Because the majority of carbon remineralization in
sediments is microbially mediated, the repeated scouring of the seafloor will most likely stimulate
bacterial activity and diminish carbon preservation, similarly to how tilled soils rapidly lose carbon
(Keil & Mayer 2014) (Figure 2).
Eutrophication and deoxygenation affect organic carbon preservation at the seafloor. Decreased
exposure to oxygen leads to enhanced organic matter burial (often in a nonlinear form) (Burdige
2007, DeVries & Deutsch 2014, Hedges et al. 1999). This is a positive influence on carbon
preservation derived from the negative anthropogenic effects of deoxygenation and eutrophication,
and it represents one of the negative feedback loops of the global carbon cycle over geologic
time (Berrocoso et al. 2013, Kennedy & Wagner 2011, Piper & Calvert 2009). Throughout the
Cretaceous and Jurassic periods, the earth saw a series of widespread ocean anoxia events that
resulted in the burial of tremendous amounts of organic carbon in the ocean (Keeling et al.
2010, Kennedy & Wagner 2011). In one sense, this can be thought of as the earth’s ultimate
tipping point: If greenhouse gases become sufficiently prevalent, then the earth’s solution to a
hyper-greenhouse world is to create anoxic oceans that bury organic carbon until a new balance is
established.
The correlation between the oxygen content of the ocean and the organic carbon content of
the underlying sediments has been noted for decades (Richards 1965). Although the correlation
is not directly causal (as discussed in detail in Burdige 2007) and not particularly robust along the
margins—where sediment delivery seems to be the dominant factor promoting organic carbon
preservation—the expansion of oceanic oxygen minimum zones is expected to eventually reach
a tipping point, both for aerobic organisms within the water column and for benthic organic

carbon preservation (Keeling et al. 2010). Nonetheless, for the moment, the overall impact of
anthropogenic effects seems to favor diminished organic carbon preservation (Figure 3).
Carbonate Preservation
At the seafloor, the story for carbonates is intimately related to, but quite different from, that for or-
ganic matter. Instead of sedimentary conditions favoring preservation, the cards are stacked against
most carbonate preservation during early diagenesis (except shallow basins). This is especially true
in sediments with active organic carbon remineralization, in the deep sea, and in the North Pacific.
The first factor controlling carbonate preservation is acidity produced from the remin-
eralization of organic carbon. In most sediments, the CO2 released from organic matter remin-
eralization dissolves available carbonate in a 1:1 ratio (Morse & Mackenzie 1990) and also reduces
the saturation state of the water, which may lead to further dissolution. This is especially impor-
tant along continental margins and slopes, where as much as 50% of modern carbonate deposition
occurs (Archer 1996, Morse & Mackenzie 1990). It is only after most of the sulfate is reduced in
an anoxic sediment that the effect of increased alkalinity begins to raise the saturation state of the
water. As with organic carbon, bioturbation and mixing enhance the dissolution of carbonate by
titrating the alkalinity via oxidation of sulfide in the pore water (Aller 1982, Green et al. 1993). In-
terestingly, the dance between organic and carbonate carbon does not favor only remineralization;
just as sorption to mineral surfaces can protect organic carbon from degradation, so too can it
protect underlying carbonate from dissolution (Morse & Mackenzie 1990, Zullig & Morse 1988).
The second factor working against carbonate preservation is the change in the saturation state
of the water as a function of CO2 and pressure (salinity and temperature effects are generally small)
(Boudreau et al. 2010, Ridgwell & Zeebe 2005). As deep water travels along the ocean conveyor
belt, the CO2 added via organic matter remineralization, combined with the great depth of the
ocean, results in deep-sea sedimentary pore waters becoming less saturated as water moves from
the North Atlantic to the North Pacific (e.g., Feely et al. 2009). This change in saturation defines
where deep-sea carbonate deposits can and cannot stably form (Figure 1).
Shallow-water systems that are oversaturated with respect to different carbonate phases oc-
casionally contain carbonate cements or overgrowths on mineral surfaces (Morse & Mackenzie
1990). Today, the surface of the ocean is oversaturated nearly everywhere with respect to the solid
carbonate phase, with a mean value of calcite of 4.8. That is, the minimum thermodynamic
requirement for calcite to precipitate is exceeded by a factor of almost 5 (for aragonite, is 3.2)
(Ridgwell & Zeebe 2005). Despite this, the spontaneous precipitation of carbonate from the water
column is not observed in the ocean, because the initial step of crystal nucleation is kinetically
unfavorable. Although carbonate precipitation occurs abiotically as cements and coatings in the
marine environment, it is associated primarily with the activities of living organisms, particularly
corals, benthic shelly animals, plankton species such as coccolithophores and foraminifera, and
pteropods (Ridgwell & Zeebe 2005).
The main anthropogenic forces influencing shallow-water carbonate preservation are eutroph-
ication, warming, and ocean acidification, all of which decrease coral growth and diminish car-
bonate formation and preservation (Doney et al. 2009, Lowe & Falter 2015). By the middle of the
next century, an increased concentration of CO2 will decrease the aragonite and calcite saturation
states in the tropics by 30% (Feely et al. 2009). Coral reefs are particularly threatened because
reef-building organisms secrete metastable forms of carbonate, but the biogeochemical conse-
quences for other calcifying marine ecosystems will likely be equally severe (Hoegh-Guldberg
& Bruno 2010, Kleypas et al. 1999, Lowe & Falter 2015). The overall impact of anthropogenic
forcing is to diminish carbonate preservation.
164 Keil
SUMMARY
Virtually every aspect of climate change presently favors remineralization over preservation, and it
is not until the oceans reach a critical tipping point of widespread anoxia that any significant carbon
preservation mechanisms can be expected to kick in. Most ocean models do not explicitly include
carbon preservation, under the assumption that its magnitude is too small to matter. However,
Kriest & Oschlies (2013) showed that including a preservation term improves model predictions,
suggesting that better quantification of the mechanisms and rates of carbon preservation in the
modern ocean will help improve predictions of future climate scenarios. Thus, a complete and
well-constrained budget for the changing rate of carbon burial in the geologic record remains a
worthy goal.
DISCLOSURE STATEMENT
The author is not aware of any affiliations, memberships, funding, or financial holdings that might
be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
I thank Miles Logsdon for help with spatial analyses of various data sets, Jaqui Neibauer for help
editing the manuscript, the University of Washington’s Aquatic Organic Geochemistry group and
the editing team at Annual Reviews for helpful reviews, and the National Science Foundation’s
Chemical Oceanography Program for supporting a majority of this work.
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Annual Review of
Marine Science
Volume 9, 2017 Contents

Venice and I: How a City Can Determine the Fate of a Career
Paola Malanotte-Rizzoli p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Biogeochemical Transformations in the History of the Ocean

Timothy M. Lenton and Stuart J. Daines p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p31
Advances in the Application of Surface Drifters

Rick Lumpkin, Tamay Özgökmen, and Luca Centurioni p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p59
The Atlantic Meridional Overturning Circulation and Abrupt
Climate Change
Jean Lynch-Stieglitz p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p83
Marine Hydrokinetic Energy from Western Boundary Currents
John M. Bane, Ruoying He, Michael Muglia, Caroline F. Lowcher,
Yanlin Gong, and Sara M. Haines p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 105
Natural Variability and Anthropogenic Trends in the Ocean
Carbon Sink
Galen A. McKinley, Amanda R. Fay, Nicole S. Lovenduski, and Darren J. Pilcher p p p 125
Anthropogenic Forcing of Carbonate and Organic Carbon
Preservation in Marine Sediments
Richard Keil p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 151
Fukushima Daiichi–Derived Radionuclides in the Ocean: Transport,
Fate, and Impacts
Ken Buesseler, Minhan Dai, Michio Aoyama, Claudia Benitez-Nelson,
Sabine Charmasson, Kathryn Higley, Vladimir Maderich, Pere Masqué,
Paul J. Morris, Deborah Oughton, and John N. Smith p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 173
Plastics in the Marine Environment
Kara Lavender Law p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 205
SAR11 Bacteria: The Most Abundant Plankton in the Oceans
Stephen J. Giovannoni p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 231
Quorum Sensing in Marine Microbial Environments
Laura R. Hmelo p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 257
MA09-FrontMatter ARI 21 November 2016 21:4
Coccolithophore Cell Biology: Chalking Up Progress

Alison R. Taylor, Colin Brownlee, and Glen Wheeler p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 283
Mixotrophy in the Marine Plankton
Diane K. Stoecker, Per Juel Hansen, David A. Caron, and Aditee Mitra p p p p p p p p p p p p p p 311
Dining in the Deep: The Feeding Ecology of Deep-Sea Fishes
Jeffrey C. Drazen and Tracey T. Sutton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 337
How Baleen Whales Feed: The Biomechanics of Engulfment
and Filtration
J.A. Goldbogen, D.E. Cade, J. Calambokidis, A.S. Friedlaender, J. Potvin,
P.S. Segre, and A.J. Werth p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 367

The Physiology and Ecology of Diapause in Marine Copepods
Mark F. Baumgartner and Ann M. Tarrant p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 387

Zooplankton and the Ocean Carbon Cycle
Deborah K. Steinberg and Michael R. Landry p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 413
Multiple Stressors and the Functioning of Coral Reefs
Alastair R. Harborne, Alice Rogers, Yves-Marie Bozec, and Peter J. Mumby p p p p p p p p p p 445
Climate, Anchovy, and Sardine
David M. Checkley Jr., Rebecca G. Asch, and Ryan R. Rykaczewski p p p p p p p p p p p p p p p p p p p p 469
Errata
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MA09CH07-Keil ARI 8 November 2016 10:33

Annu. Rev. Mar. Sci. 2017. 9:151–72 Keywords

A MARINE CARBON BURIAL MAP AND BUDGET

www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 153

PROCESSES IN OCEAN WATER

www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 155

Shifts to smaller Nitrogen deposition

Decreased sinking speeds Deoxygenation and eutrophication

Ocean acidification cline

www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 157

www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 159

Reimers et al. 2013).

Organic Carbon Preservation

Strait of Juan de Fuca

Selective preservation. Selective preservation consists of three known types: production of

www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 161

Humification. Humification is the term typically used by oceanographers to identify geopoly-

together to form chemically complex macromolecules broadly referred to as humic substances

Breaking Organic Carbon Protective Mechanisms

www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 163

www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 165

origin, and fate in soils and sediments. Soil Sci. 166:833–47

www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 167

quences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–20

www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 169

in the eastern equatorial Pacific. Deep-Sea Res. II 54:706–21

www.annualreviews.org • Anthropogenic Forcing of Carbon Preservation 171

Volume 9, 2017 Contents

Biogeochemical Transformations in the History of the Ocean

Advances in the Application of Surface Drifters

Coccolithophore Cell Biology: Chalking Up Progress

P.S. Segre, and A.J. Werth p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 367

Mark F. Baumgartner and Ann M. Tarrant p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 387

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