Coupling carbon and energy fluxes in the North Pacific Subtropical Gyre
Coupling carbon and energy fluxes in the North Pacific Subtropical Gyre
Ricardo M. Letelier 0 1
Edward A. Laws 0 2 3
David M. Karl
0 Daniel K. Inouye Center for Microbial Oceanography: Research and Education (C-MORE), University of Hawaii at Manoa , Honolulu 96822 HI , USA
1 School of Ocean and Earth Science and Technology, University of Hawaii at Manoa , Honolulu 96822 HI , USA
2 College of Earth, Ocean and Atmospheric Sciences, Oregon State University , Corvallis 97331 OR , USA
3 College of the Coast & Environment, Louisiana State University , Baton Rouge 70803 LA , USA
The major biogeochemical cycles of marine ecosystems are driven by solar energy. Energy
that is initially captured through photosynthesis is transformed and transported to great
ocean depths via complex, yet poorly understood, energy flow networks. Herein we show that
the chemical composition and specific energy (Joules per unit mass or organic carbon) of
sinking particulate matter collected in the North Pacific Subtropical Gyre reveal dramatic
changes in the upper 500 m of the water column as particles sink and age. In contrast to
these upper water column processes, particles reaching the deep sea (4000 m) are
energyreplete with organic carbon-specific energy values similar to surface phytoplankton. These
enigmatic results suggest that the particles collected in the abyssal zone must be transported
by rapid sinking processes. These fast-sinking particles control the pace of deep-sea benthic
communities that live a feast-or-famine existence in an otherwise energy-depleted habitat.
T component of the global carbon (C) cycle, largely responsible
he ocean?s biological carbon pump (BCP) is an integral
for the long-term sequestration of carbon dioxide (CO2) into
the mesopelagic and abyssal zones1. Because nearly all biological
and biogeochemical processes in the sea, including the BCP, are
solar-powered with light energy initially transformed into chemical
potential energy via the process of photosynthesis, there is an
inextricable, yet poorly characterized, linkage between C fluxes and
energy fluxes in the sea2. In marine ecosystems, pigments (e.g.,
chlorophylls, carotenoids, and biliproteins) contained within
phototrophic prokaryotic and eukaryotic microorganisms absorb solar
energy through a complex series of light-dependent reactions, and
transfer electrons (e?) from donor to acceptor molecules. During
this process, water (H2O) is the e? donor being oxidized to
molecular oxygen (O2) in stoichiometric proportion to photon
capture (i.e., 2H2O ? 4H+ + 4e? + O2). In a second,
lightindependent series of reactions, carbon dioxide (CO2) is reduced
to carbohydrate3, a form of potential energy that is ultimately used
to build other biomolecules and to sustain heterotrophic processes
throughout the water column and into the abyssal sediments. In
marine ecological studies, photosynthesis is typically estimated by
measuring O2 production or CO2 reduction per unit volume and
per unit time during incubation experiments4,5. However, these O2
or CO2 fluxes alone are insufficient to track energy within the
surface ocean, or to quantify potential energy export from the sunlit
zone of maximum production into the mesopelagic and abyssal
zones in the form of sinking particulate matter (SPM).
We have recently estimated gross primary production using
18O-H2O (refs. 4,5) and the total photosynthetic pigment
absorption of solar energy6 in the surface waters at Station
ALOHA in the North Pacific Subtropical Gyre (NPSG)7. The
calculated quantum yield of ~0.1 mol O2 evolved per mol quanta
absorbed by photosynthetic pigments6 is in excellent agreement
with laboratory-derived values8, and equates to a mean
photosynthetic energy capture of ~33 kJ m?2 d?1 (see Methods). In
September 2013, we deployed a free-drifting array of sediment
traps to collect SPM over a range of 12 depths (100?500 m) for a
period of 9.1 days. Particle mass, C (organic [OC], inorganic [IC],
and black [BC]), hydrogen (H), nitrogen (N), phosphorus (P) as
well as total potential energy were used to calculate downward
fluxes and to determine changes as particles sink from the sunlit
region of the water column and are remineralized during transit
through the mesopelagic zone. Potential energy was measured as
heat released upon combustion using an oxygen bomb
calorimeter. In 2016, we deployed a bottom-moored, sequencing
sediment trap to collect SPM at 4000 m (800 m above the seabed)
during both winter and summer seasons. In addition, we also
sampled the Station ALOHA sediment trap archive to measure
the chemical composition and total potential energy of deep-sea
SPM from winter and summer seasons in 1998 and 2000 (ref. 9).
Measurements of heats of combustion (enthalpy, measured in
Joules) should provide upper constraints of total potential energy
in the SPM collected at various depths in the water column.
Although the Gibbs energy of combustion that is available to
microorganisms is expected to be less than the measured
enthalpy, a review of relevant literature on the thermodynamics
of aerobic microbial growth concluded that enthalpy changes are
generally close to the Gibbs energy changes10. Therefore,
measurements of the enthalpy of SPM can provide reasonable
estimates of the total energy (measured in Joules), specific energy
(J mg?1 mass or J mg?1 OC) and downward energy transport
(J m?2 d?1) associated with SPM collected at different depths in
the water column.
We present several lines of evidence showing that much of the
energy is lost in the upper mesopelagic zone via selective
remineralization as particles sink and age, leaving behind an
energydepleted organic matter pool containing black carbon. The SPM
collected at the 100 and 500 m reference depths contain ~6.5%
and ~2.6%, respectively, of the total energy that is produced
through photosynthesis in the overlying water column. The
chemical composition and specific energy content of the SPM at
500 m is consistent with highly oxidized, low-potential energy
organic matter. While the flux of total energy to the abyss
(4000 m reference depth) is very low (<0.5% of total energy
captured via photosynthesis), the OC-specific energy for abyssal
particles is on par with near-surface energy-replete particles.
These observations support the existence of two fundamentally
different classes of sinking particles, namely energy-deplete,
slowsinking particles and energy-replete, fast-sinking particles. These
BCP energy flux data, connecting the euphotic zone to
mesopelagic and abyssal habitats, are the first of their kind for any
Elemental fluxes in the upper ocean. The fluxes of SPM mass
and C were highest at 100 m and decreased with increasing water
depth (Fig. 1 and Table 1), in accordance with previous field
observations at or near Station ALOHA11?13. The flux profiles
were fit to a normalized power function of the form, Fz = F100 (z/
100)b, where z is water depth (m) and F and F100 are fluxes at
reference depths zm and 100 m, respectively (ref. 11; see
Supplementary Fig. 1 for individual plots). The total C (TC) fraction was
comprised of three separate components: OC, the major fraction
of which decreased significantly (~75%) over the 100?500 m
depth range, and two less abundant (<5% by mass at the 100-m
reference depth) C components (IC and BC), which both increase
with depth as percentages of TC (Fig. 1 and Table 1). IC (i.e.,
calcium carbonate) is produced by a variety of marine organisms
and is expected to be present in SPM, whereas BC is most likely
derived from allochthonous sources as a by-product of
incomplete combustion of organic matter14,15. While BC is technically
part of the OC pool, it has a pyrogenic origin and is more
resistant to thermal and chemical degradation than the
autochthonous OC fraction (see Methods). The elemental composition
of SPM also changed systematically with increasing depth,
becoming more OC-enriched relative to N and P (Table 1 and
Supplementary Fig. 2). A comparison of the elemental
composition of SPM at 100 m to that at 500 m indicates that the loss of
mass from sinking particles to the water column over this depth
range had a mean molar stoichiometry of OC162H271N28P1,
despite the changing stoichiometry of the residual SPM (Table 1).
This indicates a selective remineralization of SPM, presumably by
aerobic microbial decomposition, as particles sink and age.
Energy fluxes in the upper ocean. The downward flux of energy
associated with SPM, expressed as J m?2 d?1, also displayed a
significant decrease with depth (Fig. 2 and Table 2). The
downward energy flux measured at 100 m is equivalent to ~6.5% of the
solar energy captured via photosynthesis at Station ALOHA (i.e.,
2138 J m?2 d?1 compared to 33,054 J m?2 d?1; Figs. 2 and 3, and
Table 2). These data provide direct evidence for an efficient
energy-dissipative, remineralization-intensive euphotic zone
(0?100 m) where ~95% of the solar energy captured and stored
during the process of photosynthesis is locally transformed,
assuming steady-state conditions. The energy contained within
the SPM that does escape the upper euphotic zone exhibits a
significant depth-dependent decrease to a downward flux of ~125
J m?2 d?1 at 500 m (Fig. 2 and Table 2). This observed loss within
the 100?500 m region of the water column is equivalent to ~95%
of the energy that is exported from the euphotic zone via SPM
Mass flux (mg m?2 d?1)
TC flux (mg m?2 d?1)
OC flux (mg m?2 d?1)
OC (% of TC)
IC (% of TC)
BC (% of TC)
Both the mass- and OC-specific energy of the residual SPM
decrease significantly with depth between 100 and 500 m. This
systematic trend toward an increasingly more energy-depleted
residual SPM is consistent with the changes in bulk elemental
stoichiometry and the higher BC content with depth. However,
there are important distinctions between the depth-dependent
changes in mass fluxes versus changes in SPM specific energy.
Whereas the C:N and C:P ratios change continuously throughout
the flux profile, the specific energy of the residual SPM exhibits a
more abrupt change below 250 m, especially for the OC-specific
energy (Figs. 2 and 3, and Table 2). SPM collected above the
compensation irradiance, the depth where net photoautotrophic
solar energy capture is zero over a 24-h period (equal to a solar
energy flux of 0.054 mol photons m?2 d?1 or a depth of
approximately 175 m; ref. 16) has a nearly constant mass- and
OC-specific energy with mean values of 11.83 (s.d. = 1.28, n = 8)
J mg?1 and 47.53 (s.d. = 2.18, n = 8) J mg?1, respectively (Fig. 2).
However, below the compensation irradiance (>175 m), there is a
(mg m?2 d?1)
(mg m?2 d?1)
(mg m?2 d?1)
8.18 ? 0.21
7.15 ? 0.13
6.93 ? 0.30
6.42 ? 0.16
5.36 ? 0.03
4.95 ? 0.20
4.98 ? 0.09
3.60 ? 0.11
3.84 ? 0.07
2.52 ? 0.06
2.38 ? 0.12
1.50 ? 0.04
0.62 ? 0.01
0.48 ? 0.01
0.44 ? 0.02
0.43 ? 0.01
0.35 ? 0.01
0.32 ? 0.02
0.31 ? 0.02
0.21 ? 0.01
0.23 ? 0.00
0.14 ? 0.01
0.13 ? 0.01
0.09 ? 0.01
(Joules m?2 d?1)
Mass 0.25 0.5
Normalized flux 0.75 1
significant and systematic decrease in the mass- and OC-specific
energy of the residual SPM to much lower values. This pattern
may reflect a selective light- and depth-dependent utilization of
energy-replete organic compounds from the SPM pool as
particles age. Based on these observations, we estimate that the
SPM remineralized in the 100?500 m region of the water column
has an average specific energy of ~60 J mg?1 OC. This value is
slightly higher than the mean value for SPM collected at 100 m
(Table 2), but is nearly identical to the OC-specific energy of
carbon fixed in photosynthesis observed during the peak of a
natural phytoplankton bloom17. These results, along with the
observed changes in the elemental composition, suggest that
much of the freshly produced SPM is selectively and rapidly
remineralized as particles age while sinking. Although the
molecular composition of SPM in the mesopelagic zone is largely
unknown, the OC-specific energy at 500 m, 11.09 J mg?1
(Table 2), is indicative of an extremely energy-depleted residual
SPM compared to near-surface values. In addition, the percentage
increase in the contribution of BC to total SPM carbon with
depth, from ~2% of TC in the euphotic zone to >5% at the 500 m
Photosynthetic energy capture
CO2 + H2O ? OC + O2
~33 kJoules m?2 d?1 (total E)
Energy export to mesopelagic zone
(~6% total E)
via slow sinking
(>5% total E)
(<1% total E)
Benthic community processes
OC + O2 ? CO2
reference depth (Fig. 1 and Table 1), indicates preferential BC
preservation relative to OC.
Only one previous study reported BC in sinking particles15; our
report is the first to quantify the BC flux profile in the upper water
column. BC refers to a broad spectrum of refractory materials (e.g.,
graphite, soot, char; ref. 14) that are formed during incomplete
combustion of fossil fuels, wood, and other organic matter. BC is
ubiquitous, and has been reported as a component of both dissolved
and particulate matter in the ocean18?21. Because we used a
conservative method to estimate BC in our samples (see Methods),
our reported concentrations are probably lower bounds on BC
concentration. The source(s) of marine BC are poorly known, but it
appears that there are multiple components, some with radiocarbon
ages of >20,000 years22. Regardless of BC sources and dynamics, the
low mass- and OC-specific energies of SPM collected at 500 m are
indicative of SPM that may be at or near the lower limit for further
Nominal oxidation state of carbon and Gibbs energy of SPM.
LaRowe and Van Cappellen23 have shown that the standard
molar Gibbs energies of the oxidation half reactions for a variety
of organic compounds is inversely proportional to the nominal
oxidation state of carbon (NOSC) and approaches a value of zero
at NOSC >2.2. Although there are no direct measurements of
oxygen in SPM, previous studies have estimated oxygen by
difference between the total mass flux and all other major
constituents (organic matter, carbonate, silicate24). If we assume a
late summer opal (SiO2) flux of 3 mg Si m?2 d?1 (ref. 25), and
assign oxidation numbers to H(+1), O(?2), N(?3), and P(+5),
we derive a NOSC estimate of 2.19 for SPM collected at 500 m,
which supports our hypothesis of an oxidized, energy-depleted
organic matter pool. In addition, when comparing the enthalpies
of combustion and Gibbs energies of combustion for a broad
range of organic compounds under standard conditions, we
found that nearly all of the values (83 of the 91 organic
compounds) for the enthalpies and Gibbs energies agreed to within
?10% (Supplementary Fig. 3), a result that is consistent with the
conclusion that aerobic metabolisms are enthalpy-driven with
little contribution from entropy10. We further developed a
multiple linear regression model to estimate the standard Gibbs
energy of combustion of these same 91 organic compounds based
on their elemental composition ratios (H:C, N:C, O:C, and S:C;
Mass flux (mg m?2 d?1)
Carbon flux (mg m?2 d?1)
Hydrogen flux (mg m?2 d?1)
Energy flux (J m?2 d?1)
(J mg?1 mass)
(J mg?1 OC)
Supplementary Fig. 4). The result of this analysis can be used to
provide an independent estimate of the Gibbs energy of
combustion based on the elemental composition of organic matter.
The standard Gibbs energy of combustion for SPM collected at
500 m estimated from our stoichiometric model is ?21 J mg?1
OC compared to an average of ?31 J mg?1 OC in the upper
100?175 m portion of the water column. The actual in situ Gibbs
energy would depend on the activities of substrates and products,
as well as on temperature and pressure. Consequently, the
apparent recalcitrant nature of the mesopelagic SPM may be due
to kinetic as well as thermodynamic constraints. While these
approaches are only approximations, the results emphasize the
importance of a comprehensive stoichiometric and energetic
analysis of SPM.
Our data for the downward energy flux and specific energy of
SPM are the first reports of their kind for the BCP. Previously,
Platt and Irwin26 reported proximate analyses, bulk C:N ratios,
and energy estimates for the spring bloom of phytoplankton in St.
Margaret?s Bay, Nova Scotia. They concluded that the dry weight
percent C and N of suspended particles could be used to estimate
its energy content. We applied their model to our SPM samples
where direct bomb calorimetric analyses have also been made. As
expected, the Platt and Irwin26 approximation yields an
overestimation of the measured energy content of SPM at 500 m,
likely due to the fact that the chemical compositions and energy
contents of mesopelagic SPM are different from those of living
phytoplankton, and they change significantly over the 100?500 m
region of the water column as particles sink and age, as
Abyssal energy fluxes. Pioneering sediment trap studies in the
deep sea have documented rapid, short-lived pulses of organic
matter following the spring bloom of surface phytoplankton27.
Distinct seasonal variations in the amount and composition of
SPM collected at 4000 m have also been reported at Station
ALOHA9. Based on a 13-year climatology, Karl et al.9
documented a relatively low and nearly constant flux of OC, N, P, and
biogenic silica (opal) that was overprinted by a prominent peak in
export, especially for OC and N, for a brief period that they
referred to as the summer export pulse. Changes in the bulk
elemental, biochemical, and molecular composition of SPM
during late summer were attributed to the rapid export of
symbiotic nitrogen-fixing cyanobacteria in association with diatom
hosts, and the summer export pulse was hypothesized to be
triggered by a response of the surface plankton to daylength9. We
collected additional deep-sea sediment trap samples in 2016 to
measure the elemental stoichiometry and specific energy of SPM
during winter and late summer periods (Table 3). As expected,
the fluxes of total mass, OC, H, N, and P in winter were lower
than in summer. The wintertime energy flux was also significantly
lower (Table 3), with values that are ~2% of those measured at
100 m (Fig. 3). In contrast, the summertime energy flux at 4000 m
is more than twice the wintertime value (Table 3). Whereas the
mass-specific energy in both winter and summer is relatively low
(3.00 and 3.43 J mg?1) and similar in magnitude to the
300?500 m SPM, the OC-specific energy values for SPM collected
at 4000 m during both the winter and late summer periods are
higher than any measured in the water column and are on par
with the estimates measured in phytoplankton blooms (Fig. 3 and
Table 3). We resampled our abyssal SPM archive from Station
ALOHA to measure the OC-specific energies for SPM collected in
both winter and summer periods in 1998 and 2000. These results
conform to the 2016 data, with wintertime values of 60.26 (s.d. =
6.77) and 64.13 (s.d. = 5.88) J mg?1 OC and summertime values
of 64.09 (s.d. = 10.48) and 51.21 (s.d. = 1.88) J mg?1 OC for 1998
and 2000, respectively. The mean OC-specific energy content for
all 4000 m SPM samples analyzed to date is 56.56 (s.d. = 7.79)
J mg?1 OC. This value is not significantly different from the mean
value of 60.67 J mg?1 OC reported above for SPM that is
remineralized in the 100?500 m region of the upper water column and
to the OC-specific energy stored during photosynthesis (ref. 17
Fig. 3a). Consequently, while abyssal environments appear to be
limited with respect to the total flux of potential energy, the SPM
that arrives there has a very high OC-specific energy, regardless of
All life processes on Earth, including human economic and social
systems, exist within a complex network of energy flow2. In
oceanic systems, photosynthesis is the primary source of both
organic carbon and energy, but the subsequent pathways and
mechanisms for carbon cycling and energy dissipation are less
well understood. For example, in the present study, we observed
that the elemental compositions and specific energy values for
SPM collected in the upper mesopelagic zone (300?500 m) were
fundamentally distinct from SPM collected at an abyssal (4000 m)
depth. The relatively high OC-specific energy of SPM collected at
4000 m can be explained by several possible mechanisms that are
not mutually exclusive. First, vertically segregated zones of new
particle production deep within the water column could serve to
repackage surface-derived organic matter, resulting in the flux of
a smaller mass of more energy-replete particles28. This
repackaging process may be facilitated by diel, vertically migrating
zooplankton that transport fresh organic matter to depths of
800?1000 m at Station ALOHA29. In addition, the flux of
relatively energy-replete SPM to 4000 m could be a result of the
selective preservation of lipids30 or other energy-rich organic
compounds during transit to the deep sea. However, the relatively
energy-depleted SPM collected at 300 and 500 m (17.3 and
11.1 J mg?1 OC, respectively) argue against lipid preservation
with increasing water depth, at least for the upper portion of the
mesopelagic zone. Finally, the mechanism which may best explain
the OC and energy flux patterns that we observe for SPM, is the
control by large, rapidly sinking particles that escape the
combined processes of disaggregation, dissolution, solubilization, and
microbial decomposition en route to the deep sea31 (Fig. 3c). The
relatively high total mass-to-OC ratios of the 4000 m SPM (~15;
Table 3) are at least three times greater than those measured in
near-surface waters, suggesting an important role for biogenic
mineral ballast32. Indeed, ~50% of the SPM collected at the 300 m
reference depth at Station ALOHA during the VERTIGO
expedition in June 2004 had sinking speeds greater than 100 m d?1
and >15% of the material was sinking at rates >820 m d?1
(ref. 33). This rapidly sinking and presumably energy-replete SPM
would reach the seabed in less than 1 week. Previous studies at
Station ALOHA9 have documented the significant role of diatoms
in controlling particle flux to the deep sea. A peak in opal and
intact diatoms coincided with the summer export pulse of organic
matter9. Herein, we also present evidence for a significant
contribution of calcium carbonate with deep-sea IC representing
nearly half of the total C flux (Table 3). These high proportions of
opal and calcium carbonate, the two most important ballast
biominerals34, are not observed in the upper water column SPM,
thereby providing strong evidence for a distinctive class of
fastsinking energy-replete particles in the deep-sea samples (Fig. 3
and Table 3). The 4000 m SPM is also characterized by low BC:
OC ratios that are more similar to the euphotic zone SPM
(100?175 m) than to the BC:OC ratios of the SPM collected
deeper in the water column (300?500 m; Table 1). By our
analysis, ~10% of the OC exported from the euphotic zone and
~0.4% of the total energy initially captured via photosynthesis
reaches the abyssal benthic community at Station ALOHA while
the remaining ~90% of the exported OC is remineralized to
carbon dioxide en route to the seafloor (Fig. 3b). Predicted future
states of a warmer, more acidic, and more nutrient-depleted
NPSG35,36 may alter the phytoplankton community structure and
select against opal- and calcium carbonate-containing
organisms37,38. Under this environmental scenario, the flux of
carbon and energy to the deep sea will be reduced due to a
decrease in the proportion of mineral-ballasted SPM. A
disruption in food supply to the deep sea would have a significant effect
on the structure and metabolism of abyssal benthic
communities39. While we have focused our discussion on the role of OC
and energy fluxes, other components of the SPM pool, such as
ammonium and sulfide, might also contribute to the total energy
flux40,41 and should be considered. While the data presented in
this study derive from only a single station in the NPSG, the flux
attenuation patterns, role of ballast minerals and changes in
organic matter stoichiometry of SPM with depth appear to be
common features throughout large portions of the global ocean.
Quantitative studies of these and other linkages between the C
cycle and the pathways of biological and detrital energy flow will
be required to develop a comprehensive understanding of the
ocean?s BCP and its role in C sequestration.
Energy capture via photosynthesis. A previous study of light absorption by
phytoplankton at Station ALOHA during 2006?2012 reported that the mean
0?200 m depth-integrated value in summer was 0.79 (s.d. = 0.19) mol quanta m?2
d?1, and approximately 20% lower (0.64 (s.d. = 0.16) mol quanta m? d?1) in
winter6. Assuming blue light (? = 475 nm), we calculated absorbed energy (E) as
E = hv, where h = Planck?s constant (6.63 ? 10?34 J s?1), v = frequency defined as
speed of light (C) divided by ?. This resulted in a photosynthetic energy capture of
33,054 J m?2 d?1 for the period of our upper ocean sediment trap experiment.
SPM collection and processing. Sinking particles were collected during the
HOEPhoR II expedition in September 2013 at Station ALOHA (22?45?N, 158?W)42. A
free-drifting sediment trap array, identical to that described by Knauer et al.43
consisting of eight individual particle interceptor traps (PITs) on PVC crosses
positioned at twelve depths ranging from 100 to 500 m was employed. Prior to
deployment, each PIT was filled with a filtered, buffered formalin brine solution
consisting of filtered surface seawater containing 50 g l?1 sodium chloride and 1%
(vol/vol) formalin. The array was deployed over a 9.1-day period. Following
recovery, individual PITs were capped and placed in a cool, dark area. The
interface between the high density trap solution and the overlying seawater was
marked, and the overlying seawater was removed to within 5 cm above the
interface. All samples were passed through a 335 ?m Nitex? screen to remove
zooplankton and micronekton, as previously described12. Each sample was
vacuum filtered onto a tared 47 mm diameter, 0.8 ?m porosity polycarbonate
membrane. In order to remove salts, the filtered samples were rinsed six times,
each with 5 mL of deionized water (DI), allowing each rinse to re-suspend the
particles before filtration. The filters were stored frozen until further analysis. The
filters were subsequently dried at 60 ?C for 12 h, stored in a dessicator and
periodically weighed to achieve constant weight in order to calculate mass flux from
PIT collection area (0.0039 m2) and deployment time (9.1 days). Each filter was
then placed into a vial containing 5 mL of DI, and the particles were continuously
mixed on a shaker table for 1 h. Finally, any particulate matter remaining on the
filter was rinsed into the vial with additional DI, and the entire volume was
evaporated in a SpeedVac?, leaving the dried particles behind. The sediment was
pulverized and dried at 60 ?C for 8 h. This powdered material was used for all
Elemental analysis. Various amounts of sample from each depth were sealed in
tared tin cups and weighed on a microbalance. The C, H, and N contents were
determined using an Exeter Analytical Elemental Analyzer using a combustion
temperature of 1020 ?C. Acetanilide was used as a standard and the Hawaii Ocean
Time-series (HOT) plankton sample was used as a quality control reference
material between sample runs. This value of C represents total C (TC) consisting of
inorganic (IC), black (BC), and organic (OC) components. Aliquots of each sample
were also used to measure IC and BC. For IC (calcium carbonate) determinations,
subsamples (~0.4 mg) were placed into a glass vial and sealed with a gas-tight
stopper. Phosphoric acid (200 ?l of an 8.5% vol/vol solution) was added and the
sample was incubated for 1 h after which time the entire headspace of the vial was
flushed through an infrared detector to measure total carbon dioxide by peak
integration. Various volumes of a 410 ppm carbon dioxide in air standard were
used for calibration and reagent grade calcium carbonate was also analyzed as a
check standard. For BC determinations, we employed the CTO-375 method of
Gustafsson et al.44. A recent laboratory intercomparison of BC quantification in 12
different source materials using 7 different analytical methods45 provides a
comprehensive evaluation of the strengths, weaknesses, and limitations of each method.
The method that we selected specifically targets the most highly condensed
aromatic structures (e.g., soot), and therefore provides a lower bound on total BC in
our samples. Our analysis (n = 17 samples) of National Institute of Standards and
Technology marine sediment (SRM 1941b), which represents BC in a sediment
matrix similar to our SPM, yielded the following: BC = 0.58% (s.d. = 0.02) of total
dry weight, 3.09% OC of total dry weight and 18.70% BC as a % of total OC. OC in
our study is reported as: OC = TC ? [IC + BC]. Particulate P content was
determined by high-temperature ashing and colorimetric analysis12. Elemental fluxes
were estimated from the respective analyses, PIT collection area, and deployment
time. Replicate PITs deployed on the same array were also processed for C and N
using procedures developed in the HOT program that employed direct filtration of
particles onto glass fiber filters12 which are incompatible for measurements of mass
and total energy content. The two independent methods for C and N were not
Total energy content. Energy content was determined by measuring the amount
of heat released by combustion in an oxygen bomb calorimeter (Parr Instrument
Company Semimicro Calorimeter) following the manufacturer?s recommended
procedures with only slight modifications. This instrument is a constant-volume
calorimeter designed specifically for small sample sizes ranging from 25 to 200 mg.
A press was utilized to prepare a compact pellet of each sample prior to
combustion. Duplicate or triplicate (dependent on amount of available sample) pellets
(5?9 mg each) from each depth were measured in this study. Due to our sample
size limitation and the instrument?s requirement of at least a 25 mg sample, an
exact amount of benzoic acid (heat of combustion 26,435 J g?1) was added to each
sample. The addition of benzoic acid ensured complete combustion of the sample.
The ideal weight for spike addition was determined to be ~30 mg by testing
numerous amino acids and plankton samples in the 5?9 mg range. Replicate
samples containing variable benzoic acid-to-sample ratios (from 2 to 7) returned
identical estimates of the sample caloric content within the approximately 3?6%
reproducibility of the bomb calorimetric assay. Pure benzoic acid pellets were used
to determine the heat capacity of the calorimeter-standardization prior to sample
analysis, and were also used as check standards during each sample run. Formation
of nitric acid46,47 was routinely assessed by postcombustion rinsing of the bomb
chamber with DI and titration with 0.0725N sodium carbonate. Assuming that all
acid produced was nitric acid, we determined that, on average, the acid correction
was <4% of the total heat of combustion for our samples, so it was ignored in our
subsequent calculations. Paine48 previously reported an endothermy value of
?0.573 J mg?1 calcium carbonate. While our SPM samples contained various
amounts of calcium carbonate (i.e., deep-sea samples had IC:OC molar ratios ~1:1),
the use of benzoic acid as a filler decreased the IC:OC ratios to below the threshold
where interference (endothermy) was significant in the determination of total
energy content of our samples. Consequently, no correction was required for
calcium carbonate endothermy.
Data files are available at hahana.soest.hawaii.edu/GBMF/index.html under project
?Coupling carbon and energy fluxes in the North Pacific Subtropical Gyre?.
The Matlab? code for the thermodynamic calculations is available at hahana.soest.hawaii.
edu/GBMF/index.html under project ?Coupling carbon and energy fluxes in the North
Pacific Subtropical Gyre?.
We thank Blake Watkins, Tara Clemente, Karin Bj?rkman, Dan Sadler, Lance Fujieki,
and Lisa Lum for their assistance in the field and in our shore-based laboratories. This
research was supported by the National Science Foundation (EF-0424599; DMK), the
Gordon and Betty Moore Foundation (#3794; DMK) and the Simons Collaboration on
Ocean Processes and Ecology (SCOPE #329108; DMK).
Journal peer review information: Nature Communications thanks the anonymous
reviewers for their contribution to the peer review of this work. Peer reviewer reports are
Publisher?s note: Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
D.M.K. and E.G. designed and conducted the field study. E.G. processed and analyzed the
sediment trap samples. E.A.L. wrote and executed the Matlab code. D.M.K. wrote the
initial draft of the paper. D.M.K., E.G., R.M.L. and E.A.L. discussed and interpreted the
data, and contributed to preparation of the final paper.
Supplementary Information accompanies this paper at
Competing interests: The authors declare no competing interests.
Reprints and permission information is available online at http://npg.nature.com/
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