BGBiogeosciencesBGBiogeosciences1726-4189Copernicus GmbHGöttingen, Germany10.5194/bg-12-2641-2015Peruvian upwelling plankton respiration: calculations of carbon flux, nutrient retention efficiency, and heterotrophic energy productionPackardT. T.theodoretrainpackard@gmail.comOsmaN.Fernández-UrruzolaI.CodispotiL. A.ChristensenJ. P.GómezM.Marine Ecophysiology Group (EOMAR), Universidad de Las Palmas de Gran Canaria, Campus Universitario de Tafira 35017, Las Palmas de Gran Canaria, SpainHorn Point Laboratory, University of Maryland, 21613-0775 Cambridge, MD, USAGreen Eyes LLC, Easton, MD 21601, USAT. T. Packard (theodoretrainpackard@gmail.com)6May20151292641265422October201426November20149April201514April2015This 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/12/2641/2015/bg-12-2641-2015.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/12/2641/2015/bg-12-2641-2015.pdf
Oceanic depth profiles of plankton respiration are described by a power
function, RCO2= (RCO2)0(z/z0)b, similar
to the vertical carbon flux profile. Furthermore, because both ocean
processes are closely related, conceptually and mathematically, each can be
calculated from the other. The exponent b, always negative, defines the
maximum curvature of the respiration–depth profile and controls the carbon
flux. When |b| is large, the carbon flux (FC) from the
epipelagic ocean is low and the nutrient retention efficiency (NRE) is high,
allowing these waters to maintain high productivity. The opposite occurs when
|b| is small. This means that the attenuation of respiration in ocean water
columns is critical in understanding and predicting both vertical
FC as well as the capacity of epipelagic ecosystems to retain
their nutrients. The ratio of seawater RCO2 to incoming
FC is the NRE, a new metric that represents nutrient regeneration
in a seawater layer in reference to the nutrients introduced into that layer
via FC. A depth profile of FC is the integral of
water column respiration. This relationship facilitates calculating ocean
sections of FC from water column respiration. In an FC
section and in a NRE section across the Peruvian upwelling system we found an
FC maximum and a NRE minimum extending down to 400 m, 50 km off the
Peruvian coast over the upper part of the continental slope. Finally,
considering the coupling between respiratory electron transport system
activity and heterotrophic oxidative phosphorylation promoted the calculation
of an ocean section of heterotrophic energy production (HEP). It ranged from
250 to 500 J d-1 m-3 in the euphotic zone to less than
5 J d-1 m-3 below 200 m on this ocean section.
Introduction
Respiration is as ubiquitous in the ocean as the microorganisms that
cause it . It is controlled by the respiratory
electron transport (ETS) activity in eukaryotic mitochondria and prokaryotic
cell membranes and is responsible for
the bulk of oceanic O2 consumption . It
is driven by the degradation of dissolved and particulate organic carbon,
generates CO2, acidifies seawater , and
produces energy in the form of ATP (heterotrophic energy production)
. Even in anoxic seawater, respiration degrades
organic matter, produces CO2, and generates ATP while reducing nitrogen
oxides to N2 or SO4- to H2S .
Plankton community respiration in ocean water columns is a key variable
in calculating net community productivity in developing
oceanic carbon models, in resolving the autotrophic–heterotrophic states of
ocean ecosystems , and in understanding vertical ocean
FC rates . The research team led by Sarah
Giering demonstrated that, contrary to previous efforts
but in accord with classical oceanographic understanding
, zooplankton and microplankton
(prokaryote and eukaryote) respiration balance vertical carbon flux
. All these findings support the use of
plankton respiration in assessing vertical FC in the ocean water
column. Conceptually, the reciprocal relationship between the water column
respiration and the FC, from the ocean's epipelagic zone, is
clear . However, describing this reciprocal
relationship mathematically, as a function of ocean depth in the forms,
R=f(z)andFC=∫z1z2Rdz,
was delayed until the helium–tritium studies of Jenkins ,
the sediment trap studies of VERTEX program , and
respiratory electron transport system (ETS) measurements in the Gulf of Maine
. In the latter, microplankton ETS measurements were used to
build power function models of respiratory CO2 production
(RCO2) and FC. Here, we extend this approach to
calculate a microplankton respiration section across the Peruvian upwelling
system ( and Fig. 1a) and to model FC on
this transect. We focused our measurements on microplankton because its
biomass and metabolism dominate ocean water columns . The section was made at a time of regime change when
the Peruvian upwelling system and the El Niño–Southern Oscillation
(ENSO) underwent a shift . Here we document some of the
biological phenomenon that occurred at that time. With the FC and
the RCO2 models we calculate the nutrient retention efficiency
(NRE)
, a new metric that quantifies the ability of an
ocean layer to retain its nutrients (Fig. 2c). Conceptually, the NRE is the nutrient remineralization rate within an
ocean layer normalized by nutrients entering that layer via carbon flux.
Below the euphotic zone, it can be calculated as the inverse of the
FC transfer efficiency , but we show
here that it can also be calculated from a profile of plankton respiration.
In addition, using different limits to the FC integration, we
calculate the sum of the benthic respiration and carbon burial (Fig. 3a) that
occurs on the sea floor. Finally, we use the respiration models and the
coupling between ETS activity and oxidative phosphorylation to calculate
light-independent heterotrophic energy flow . This energy is
generated in the form of ATP by ATP synthase, an enzyme motor coupled to a
heterotrophic respiratory process such as O2 utilization or NO3-
reduction . In all types of respiration, the ATP synthase
senses the pH and electromotive force gradient across the membrane in which
the ATP synthase is embedded , and when the gradient is
sufficiently strong (∼ 225 mV), the molecular motor that is the ATP
synthase starts its rotary production of ATP . Heterotrophic
ATP generation in any ecosystem is largely based on exploiting the Gibbs free
energy (ΔG) released during the oxidation of different organic
compounds. The biochemistry of ATP and the ETS was unknown in 1925, but even
then the idea of capturing biologically useable energy from respiration was
appreciated by . A generation later, Odum built on this concept
to describe energy flow in freshwater streams . Reviewing this
earlier work, Karl recently argued that biological energy production in the
ocean should be assessed to provide insight into the variability of ocean
productivity . Here, we address his concern by calculating
Heterotrophic energy production (HEP) in a C-line section (Fig. 2d). This HEP
is the energy produced while ATP is generated by respiratory O2
consumption (RO2) in the microplankton community composed of
phytoplankton, bacteria, archaea, and protozoans in the epipelagic layer and
by the RO2 and NO3- reduction in microbial communities
of bacteria, archaea, and protozoans in the meso- and bathypelagic waters of
the Peruvian current upwelling system.
(a) C-line section orthogonal to the Peruvian coast at
15∘ S. The innermost C-line position, C1, was 2.7 km from the coast
between Cabo Nazca and Punta Santa Ana. The outermost position, C14, was
located west of the Peru–Chile trench 185.2 km from the coast. Depth along
this transect ranged from 63 m at C1 to 4755 m at C12. C14 was in 2680 m
of water on the gently rising abyssal plain seaward of the trench (inset
upper left). (b) Density (σt), NO3-
(µM) and phytoplankton chlorophyll (mg m-3) sections
along the C-line from C1 to C14 (top, middle and bottom panels,
respectively). All sections represent the upwelling from 13 to
20 September 1976. Scale brakes avoid interpolation over a 90 km data gap.
The high phytoplankton biomass over the shelf break occurs between C5 and C8,
15 to 35 km from the coast. (c) NO3-, NO2-, and
O2 depth profiles through the mesopelagic waters over the trench at C12
(top) and over the outermost station at C14 (bottom). The vertical plot at
C12 documents the first step in denitrification (shaded area), NO3-
reduction to NO2-, at the foot of the oxycline, in the oxygen minimum zone (OMZ) between 150
and 300 m. In contrast, the vertical profiles at C14, 185 km off the coast,
show the absence of denitrification in mesopelagic waters.
Oceanographic characteristics of Peruvian upwelling C-line stations
during Duke University's JASON-76 R/V Eastward cruise no. E-5H-67. Ez
depth is the 1% light level. Original data are in CUEA data reports
.
Sections for the upper 500 m along the C-line. (a)RCO2; the dark shadow delimits denitrification in the OMZ. In
the Ez, RCO2 is calculated directly from ETS-based
RO2 (Table 3). In the mesopelagic waters below,
RCO2 is modeled from the respiration equations in Table 4.
(b)FC is calculated by integration of the respiration
models (Table 4) to the ocean bottom according to Eqs. (2) and (3).
(c) NRE, as a percentage, is determined from models in Tables 4 and 6 as
100×(RCO2/FC). (d) HEP is
either derived directly from ETS activity in the surface waters or from
calculated RO2 or RN2 for depths below the Ez
(as in Fig. 2a).
MethodsResearch site
The site of this Coastal Upwelling Ecosystem Analysis (CUEA) investigation at 15∘ S off Pisco, Peru
(Fig. 1) was chosen because the upwelling is strong, persistent, and well
known . It was the focus of the R/V Anton Bruun
cruise 15 , the R/V T.G. Thompson Pisco expedition
in 1969 , and others before it was
the focus of the CUEA–JOINT II program of which the
JASON Expedition was a part . However, in spite of the
many previous expeditions to this site most of them took place in the austral
fall (March–April–May). The JASON-76 expedition was unique because it took
place in the late winter and austral spring (August, September, October, and
November) when the southeast trade winds would be at their strongest
. In this way it was thought that the results might be more
comparable with results from upwelling studies made in the Northern
Hemisphere's spring-time upwelling off NW Africa . The results presented here are from the September 10 to September
24 leg of JASON-76 on board Duke University's Oceanographic ship, R/V
Eastward, cruise no. E-5H-67 .
Sampling
All sampling was conducted along the C-line (Fig. 1a) that extended seaward
from the coast at position C1, just south of Cabo Nazca (Pisco), across the
deep trench to position C14, 185 km offshore . Hydrographic
sections were made at the beginning of the expedition (10–11 September) and
again after a lapse of 10 days (20–21 September). The endpoint coordinates
were from 15∘3.2′ S, 75∘26.0′ W to
15∘55.8′ S, 75∘31.4′ W . In
addition, between 10 and 24 September, productivity stations, that focused on
the biological, nutrient chemistry, and biochemical properties at depths
where the light was 100, 50, 30, 15, 5, 1, and 0.1 % of the surface
incident radiation (light depths), were established at C-line positions
. These productivity stations were not made in order along the
C-line section, hence the irregularity of the their numerical sequence in
Tables 3–7. In addition, some locations along the C-line were occupied
several times. For this reason, as well as to coordinate the results
presented here with the results of other CUEA reports , both
the C-line location and the station number are given through the paper. The
productivity casts were made each morning before 10:00 LT with 30 L Niskin PVC
bottles to six light depths (1, 5, 15, 30, 50, and 100 %). Each Niskin
bottle was flushed at depth in yo-yo fashion both by the action of the ship's
roll and by meter oscillations with the winch. On deck it was drained
immediately, without prefiltration, into a well-rinsed carboy for subsampling
and returned to depth for the next sample. The six samples were taken within
1 h. Subsamples were drawn for phytoplankton productivity, inorganic
nutrient salts, (ammonium, reactive phosphorus, NO3-, NO2-,
and silicate), ETS and NO3- reductase activities, and particulate
protein . Station coordinates are given in Table 1. The
inorganic nutrient salts, salinity, temperature, and O2 can be found in
CUEA data reports 38 and 45 . Chlorophyll and
phytoplankton productivity (14C uptake) are reported in CUEA data
report 49 . The 14C uptake data were calculated on an
hourly basis (Table 1) from the 24 h productivity data .
Light was measured as daily total solar radiation with an Eppley Model 8–48
pyranometer placed above the ship's bridge . Below the
mesopelagic zone, the seawater was sampled for ETS activity with 30 L Niskin
PVC bottles down to 2000 m, depending on the depth of the water column
(Tables 2 and 3).
Step-by-step calculations of FC from ETS activity at
C-line position C12 (station 35). Potential R (Φ), RO2,
N2 production from denitrification (RN2) and
respiratory CO2 production (RCO2) were first
determined from temperature-corrected ETS activity values. Φ is
stoichiometrically related to electrons by a factor of 4
(O2+4e-+4H+→2H2O).
RO2 is 0.26 of Φ. RN2
relates to ETS activity according to . Here, denitrifying
waters occur between 93 and 233 m (values in bold).
RCO2 was calculated from both RO2 and
RN2 (see Sect. 2). Column 7 shows the modeled
RCO2 values below the R maximum (13 m), obtained
from the depth-normalized power function
(RCO2=Rm(z/zm)b) fitted to the data
in Column 6. FC was determined by integrating either to the
bottom (Ft-s, Column 8) or to infinity (F∞, Column 9).
The first represents the C consumed by R from the Ez (21 m) to the
bottom, while the second includes benthic R and C burial. The difference
between F∞ and Ft-s equals benthic R and the C burial
rate (Column 10). Column 11 represents the C flux determined by trapezoidal
approximation, which relates to Ft-s through the regression
Ft-s=0.85Fctrap-0.54 (r2=0.99, p<0.001).
DepthETSΦRO2RN2RCO2RCO2 modeledFC to bottomFC to infinityBenthic respirationC-Flux to bottomzActivity(µmolO2(µmolO2(µmolN2(µmolCO2(µmolCO2Ft-s (mmol CF∞ (mmol Cand burialTrap Calc(m)(neqmin-1L-1)h-1m-3)h-1m-3)h-1m-3)h-1m-3)d-1m-3)d-1m-2)d-1m-2)F∞ - Ft-s(mmol Cd-1m-2)0.537.10556.56144.71–102.74–––––337.81567.14147.46–104.69–––––535.69535.39139.20–98.83–––––933.65504.68131.22–93.16–––––1339.19587.87152.85–108.521629.67––––2115.34230.1659.84–42.49707.3919.7120.070.3625.49318.79131.8134.27–24.33359.1814.6815.040.3620.16930.44––0.250.4453.096.316.670.367.382330.35––0.200.3510.743.023.380.363.384650.050.750.19–0.143.231.662.030.361.766980.010.140.04–0.031.591.141.500.361.209300.020.230.06–0.040.970.851.210.360.9013950.010.210.05–0.040.480.540.900.360.5718600.010.130.04–0.020.290.360.730.360.404755–––––0.0600.360.360
RO2 as µmolO2h-1m-3 profiles
in the microplankton along the C-line section in September 1976 (roman font values). At the OMZ
depths (values in bold), NO3- was the electron donor and
N2 was produced during denitrification (RN2 as
µmolN2h-1m-3). C-line position as well as JASON
station number (in parentheses) are given. Depth (z) is in meters and R
refers to either RO2 or RN2 depending on the
font. Calculations are explained in the text.
Power functions for microplankton R
(mmolCO2d-1m-3) as functions of normalized depth,
RCO2=Rm(z/zm)b, where
RCO2 is the respiratory CO2 production at any
depth (z), Rm is the R maximum
(mmolCO2d-1m-3) in the water column, z/zm is the depth normalized by the depth at
Rm, and b is the maximum curvature of the power
function. Both z/zm and b are unitless. Δz
represents the depth range of the R values considered. The table
includes the r2 from the least-square regression analysis of the
R models (SigmaPlot vs. 12.5) and the number of data considered
(n). The significance level of the regressions is indicated by
superscript letters a, b, and c. The last four columns represent the
linear regression of the respiration model verification analysis. The
slope, the intercept and the r2 are given. The n value for each
verification analysis is the same as the n used for each R model
(column 7). These R models are based on ETS activity data taken
during R/V Eastward JASON-76 expedition, along the C-line.
Microplankton respiration in epipelagic, mesopelagic, and bathypelagic waters along the C-line across the Peruvian current upwelling system at 15∘ S. Calculations are based on the R models in Table 4. Shoreward of C5, the bottom limits the lower depth boundary. Note the 1000-fold shift in the rates expressed per area (columns 3–7) and per volume (columns 8–10).
Carbon flux models FC at C-line positions deeper than
500 m in the Peruvian upwelling system in Sep 1976. From these models,
FC at four different depths were determined. NRE and
FC transfer efficiency (Teff) for the upper
mesopelagic waters (150–500 m) are also given. NRE was calculated as
100×RCO2/Fc150, where the RCO2
represents the integrated R between 150 and 500 m; Teff
was calculated as 100×FC500/FC150 according to
.
HEP as ATP production in epipelagic, mesopelagic, and bathypelagic waters of the C-line section, September 1976. Shoreward of C5 the bottom limits the lower depth boundary.
Respiratory ETS activity in the euphotic zone (Ez) was measured according to
as described in . In deeper waters it was
measured according to and multiplied by 3.35 to render the
two data sets comparable as explained in . Here, ETS activity
is used as a direct measure of potential respiration and a proxy for
respiration. Both potential respiration and respiration were calculated from
the combined ETS data set according to and .
Tables 2 and 3 explain the calculations in detail. Table 3 presents the
calculations as RO2 in units of µmol O2 m-3 h-1 for oxic waters. Using ETS activity as a proxy
for RO2 requires the selection of a ratio of potential respiration
(Φ) to RO2. Since direct measurements of
RO2 can not be made below the euphotic zone, a true
calibration can not be made. The Φ to RO2 ratio should
be around 0.5 if Φ represents Vmax of the ETS and standard
physiological rates, governed by enzyme activities, operate close to one-half
of their potential capacity . With our methodology and by our analysis
we calculated a Φ to RO2 ratio, 0.26
(Table 2), that successfully predicted RO2 in the epipelagic
and the mesopelagic waters of the Nansen Basin of the Arctic Ocean
. In that study, RO2 was a long-term average
RO2 calculated by the apparent oxygen utilization (AOU)–He–tritium method of
as used by W. Roether in . We have
chosen to use the same Φ-to-RO2 ratio of 0.26 here
(Tables 2 and 3). RCO2 (Fig. 2a) was then calculated from
RO2 using a Redfield ratio (C / O2) of 0.71 from
. This is the best available way to calculate seawater
respiration from our water column ETS measurements.
In waters where respiration is based on using oxides of nitrogen
(NO3-, NO2-, N2O, or NO) in place of O2,
calculations are different. Since microbial respiratory NO3-
reduction to nitrogen gas (denitrification) occurs in the water column
between 47 and 400 m between positions C3 to C12
(Fig. 2a), Table 3 presents denitrification rates from these depths (shaded
numbers) as RN2 in units of µmol N2 m-3 h-1. In these oxygen-deficient waters we used a
Redfield ratio, C / N2, from . To apply it, one first
has to calculate RN2 based on the fact that the ETS for
RO2 and RN2 differ only in the terminal
electron acceptor . This was done in Tables 2 and 3
according to and . The approach has recently
been corroborated by . RN2 in units of
µmol N2 h-11 m-3 is calculated in Table 2, column 2, by
multiplying nanoeq min-1 L-1 by 60. The product is equivalent to
µmol e- h-1 m-3. Then, dividing this by
105 mol e- per mol N2 yields RN2. The constant,
105 mol e- per mol N2, is the equivalent of the
RN2/ ETS ratio in , 2.4 µL
O2 L-1h-1/ (gN2 m-3 yr-1). The
RCO2 calculation is as follows. RCO2 equals
[106/60 mol carbon (mol N2)-1× ETS activity
(mol e- h-1 m-3)] / [105 mol e- (mol
N2)-1]. The ratio, 106/60 mol C (mol N2)-1, is the
Redfield ratio, mentioned above, for the carbon (as CO2) produced during
denitrification from NO3. Note that both
RO2 and RN2, from Table 3 were converted to
RCO2 before being used in the Ez part of Fig. 2a.
R modeling
To generate R models as depth functions (Table 4), the ETS-based R was
plotted against depths (z) normalized by the depth of the R maximum
(zm) as we did in . From these plots, power
functions of the form R=Rm (z/zm)b were
fitted to the data using SigmaPlot (version 12.5) according to
. Note that Rm is the depth of the respiration
maximum and b, the exponent, is always negative. The exponent b represents
the maximum curvature of the respiration–depth profile. Note that R
in the Ez of Fig. 2a is based directly on the ETS measurements (Table 3),
while the R in the mesopelagic zone of Fig. 2a is based on the R models in
Table 4.
(a) Fate of the carbon fluxing out of the Ez
(FcEZ) into the water column and
seafloor below (as a percent of the total flux) along the C-line (top panel). In
the water column, the carbon is remineralized through R. In the benthos,
part of the carbon is remineralized and returned to the water column above and part is
buried. The bottom panel shows the different efficiencies with which carbon is
remineralized through respiration in four different zones of the water column
along the C-line. (b) Top panel: variability of the NRE and the
Teff in the upper mesopelagic waters (150–500 m) along the
C-line. Bottom panel: NRE and Teff as a function of the maximum
curvature b (absolute value) in the RCO2 models
from Table 4.
FC, NRE, and HEP calculations
The FC was calculated (Table 2) from depth-normalized water
column R. Power functions
(RCO2=Rm (z/zm)b) were selected
over logarithmic or exponential functions because they better described the
data as previous studies found . Conceptually,
planktonic RCO2 in a seawater cube is considered equivalent
to the difference between the total FC1 through the top of the
cube and total FC2 through the bottom of the cube, where total
carbon flux refers to the sum of the dissolved organic carbon (DOC) and the particulate organic carbon (POC) flux. We deduce,
on the basis of , that R based on DOC and
lateral POC flux, compared to the R based on the vertical flux of labile
POC, is less than 30 % of the total R. Note that if organic matter, in
any form, is resistant to oxidation , its flux through the
water column will not be detected by respiration measurements. The flux will
be transparent to our ETS measurements. However, the dissolved organic matter
in the ocean, at least, appears to be oxidizable . In all
cases, to a first approximation, one can express our conceptual model using the
expression, RCO2=FC1-FC2. In
other words, in the vertical, one-dimensional case, the changes in the
FC between depths in a water column are equal to the
RCO2 between those depths. Extrapolating this conceptual model
to the deep ocean water column, using continuous mathematics, and assuming
seafloor carbon burial to be small, the FC into the top of a water
column (FCt) can be calculated by integrating all the
R below the top boundary (zt) to the ocean bottom
(zs).
FCt=∫ztzsRCO2dz
All FC calculations here are based on depth-normalized power
functions of R (RCO2=Rm (z/zm)b,
Table 4; only if depth is normalized does the equation achieve balance with
units of nmol CO2 min-1 L-1). For the carbon flux
(Ff-s) through any depth layer in the water column (zf) down
to zs, we use Eq. (2) and its integrated version in Eq. (3). Note
that these carbon-flux calculations represent the flux at the time the
CTD–Niskin cast was made. They are fine-scale calculations of C-Flux.
Ff-s=∫zfzsRCO2dz=∫zfzsRm(z/zm)bdzFf-s={Rm/[(b+1)zmb]}(zsb+1-zfb+1)
Note that zf is any depth between zt and
zs (zt⩽zf⩽zs) and that Ff-s is associated with the microplankton
respiration, the greater fraction of water column respiration
.
The NRE is equivalent to R (mol
CO2 d-1 m-3) within an ocean layer (Δz) divided by
the FC (mol C d-1 m-2) into the volume of that layer
expressed as a percent. Note that the calculation is (R×Δz)/FC. Since the Redfield N / C or P / C ratio is applied
to both parts of the ratio, the C, N, or P units cancel out, leaving the
ratio unitless. NRE is also related to the carbon flux transfer
efficiency through the same layer
. For Fig. 2c, it was calculated for 20 m layers below the Ez
to the ocean bottom from the R models in Table 4 and the FC
models in Table 6.
HEP (Fig. 2d, Table 6) was calculated from
RO2 and RN2, derived from the ETS
measurements, from the modeled RO2, or from RN2.
For oxic seawater HEP =2×2.5×48×RO2,
where 2 represents the number of electron pairs required to reduce O2 to
2H2O, 2.5 represents the ATP /2e- ratio , 48 is the
ΔG in J per mmol of ATP , and
RO2 is the respiratory O2 consumption rate as mmol
O2 d-1 m-3. For NO3-, R in anoxic waters, HEP =5×1.0×48×RN2, where 5 is the number of
electron pairs required to reduce NO3 to N2, 1.0 is the ATP /2e-
ratio , 48 is the ΔG as before, and
RN2 is the respiratory NO3- reduction rate as mmol
N2 d-1 m-3.
Results
Oceanographic properties (Table 1) on a C-line transect at 15∘ S
across the Peruvian current upwelling system (Fig. 1a) in mid-September of the
ENSO transition year, 1976, were measured on the R/V Eastward during
the JASON-76 cruise of the CUEA–JOINT II expedition. Classic upwelling was
evident during this period. Seawater density (σt) and
NO3- sloped surface-ward close to the coast (Fig. 1b). From 25 m,
σt rose from 26.0 to 26.1, and NO3- rose from 12 to
16 µM. As these dense nutrient-rich waters rose, they fertilized the
sunlit surface waters at the upwelling center C3,, and flowed offshore towards C5 and C8, phytoplankton bloomed to
7 mg m-3 chlorophyll a and 18 mg carbon h-1 m-3 in
productivity (Table 1 and Fig. 1b). The dynamics of this process could be
seen in the variability of the Ez depth. It ranged from a
low of 21 m at C5, the maximum biomass and metabolism position, to twice the
depth, 43 m, at the offshore position, C14 (Table 1). Temporal variability
was exemplified at the trench position (C12), where over 1 week, the Ez depth
decreased from 40 to 21 m. Minimal variability occurred at position C8,
where over 6 days, the Ez depth remained at 29 m (Table 1). In general, a
shallow Ez is caused by high plankton biomass with a high potential for
metabolism and contrary conditions associated with a deep Ez.
Sea surface RO2 ranged 6-fold from a low of 24.1 µmol O2 m-3 h-1 at the upwelling center to a high
of 144.7 µmol O2 m-3 h-1, 93 km offshore at the
trench position, C12 (Table 1). Within days, RO2 could change
3-fold both inshore and offshore (Table 3). During the week between C3
stations 15 and 21, RO2 rose from 24.1 to 84.0 µmol
O2 m-3 h-1 and RO2 at C12 rose from 47.1 µmol O2 m-3 h-1 (station 17) to
144.7 µmol O2 m-3 h-1 (station 35, Table 2). This
high respiration (R) at station 35, occurred in a diatom bloom of
Chaetoceros compressus and Ch. lorenzianus. The documentation of such temporal
variability in seawater RO2 has only recently begun
. Similar increases were seen in the chlorophyll
and net productivity at C3 and C12 (Table 1). The co-occurrence of this rise
in RO2, chlorophyll and net productivity suggests seawater
RO2 being driven by phytoplankton. Below the immediate sea
surface, microplankton RO2 usually increased to a subsurface
maximum within the Ez and then decreased dramatically towards the bottom of
the Ez and into the dark ocean below (Tables 2 and 3). RCO2
(Fig. 2a) ranged in the Ez from 0.4 mmol CO2 m-3 d-1 in the
upwelling center (C3, station 15) to 3 mmol CO2 m-3 d-1 at C5,
the shelf edge station 20. The lowest epipelagic RCO2 (Table 5)
compares with the RCO2 range of 22–27 mmol
CO2 m-2 d-1 reported recently in eddy-upwelling in the South
China Sea . In the denitrifying waters, RCO2
was in the µmol range from a low of 4 µmol
CO2 m-3 d-1 at C5 (station 37) to 133 µmol
CO2 m-3 d-1 at C3 (station 21). In the mesopelagic waters below
500 m (Table 5), RCO2 ranged from 0.4 to 6.1 µmol
CO2 m-3 d-1 over 1 week at C-line position C8, at other
locations RCO2 fell in between this range. Deeper in the water
column, over the trench and beyond, bathypelagic RCO2 ranged
from 0.3 µmol CO2 m-3 d-1 at C10 over the trench
to 3.7 µmol CO2 m-3 d-1 at C8 over the continental
slope (Table 5). Benthic RCO2 and C burial (Table 5 and
Fig. 3a) ranged from a high of 90 mmol CO2 m-2 d-1 at C3,
the upwelling center, to a low of 0.09 mmol CO2 m-2 d-1 at
trench position, C10, with a depth of 4300 m. The RCO2
section in Fig. 2a clearly shows the strength of R and its associated
remineralization in the upper 50 m of the water column and a tongue of high
R descending deeper into the water column at position C8, 50 km off the
coast. FC along the C-line transect is shown in Fig. 2b. In order
to include the inshore stations, FC, in Fig. 2b, only represents
that part of the C-flux that supports the water column respiration. It does
not include benthic R and C burial. To scale our FC
calculations, FC at 150 m, seaward of C8, ranging from 3 to
6 mmol CO2 m-3 d-1 (Table 6) are comparable
to the range of 2.5 to 6.2 mmol CO2 m-3 d-1 recently
measured at 100 m by .
As one would expect with strong FC at C8, even at 1000 m, the
carbon flux transfer efficiency (Teff) at this station (19) is high and the NRE low (Table 6, Fig. 3b). Teff
between 150 and 500 m (Teff500) is 82 and the NRE is only 18 %
(Table 6). Unexpectedly, despite the decrease in FC throughout the
water column at C8 between 17 and 23 September, Teff500 only
decreased by less than a factor of 2 to 45 % (Table 6). The impact on the
NRE was greater, increasing 3-fold to 55 % (Table 6).
Teff500 at other locations ranged from 28 at C10 to 47 at C14
(Fig. 3b). In addition to this unique documentation of the temporal
variability of FC from Table 6, Fig. 2b demonstrates its
mesoscale spatial variability. That transect shows a maxima occurring
throughout the water column, 50 km from the coast at the upper slope
position, C8. As Table 5 and Fig. 3a show, the benthic R and burial are
also high at this location. Figure 3b highlights the importance of the
maximum curvature of the respiration–depth profile. As |b| increases
towards 2 the NRE increases towards 70 % and the
Teff150-500 decreases towards 30 %.
HEP in the Ez (Fig. 2d and Table 7) ranges from a
high of 555 J d-1 m-3 at the R maximum at C5 (station 20) to a low
of 69 J d-1 m-3 at the bottom of the Ez at C3 (station 21). It drops
slightly over the continental slope, but further offshore over the trench
(C12) high values of 880 J d-1 m-3 can be found (Fig. 2d). In
the far offshore, the Ez HEP only reaches values of
315 J d-1 m-3. As an example of low HEP values, at 4755 m in the
trench it decreases to 0.02 J d-1 m-3. Thus the range of HEP by
all the respiratory ETS and oxidative phosphorylation coupling in the
microplankton of this part of the Peruvian current upwelling system spans 4
orders of magnitude from 0.02 J d-1 m-3 in the abyssopelagic
waters of the trench to 880 J d-1 m-3 in the Ez above. This is
the first time such calculations have been made. Integrating the epipelagic
HEP (Table 7) over the upper 150 m yields a range from a low of
6.6 × 10-3 MJ d-1 m-2 to a high of 0.39
MJ d-1 m-2, averaging 0.09 MJ d-1 m-2. This average
HEP is only 0.7 % of the average solar radiation (13.5 ± 4.0
MJ d-1 m-2) at the C-line sea surface between 12 and 24 September
during the JASON-76 cruise .
Discussion
Here we have demonstrated the calculation of RCO2,
FC, NRE, and HEP in an ocean section from microplankton ETS
activity measurements. We have previously explained how ocean water column
RCO2 determines FC of labile organic matter by
oxidizing sinking POC and mineralizing phosphate and nitrate
. Fig. 3b shows that the maximum curvature of the
respiration–depth profile determines NRE as well as FC transfer
efficiency. The offshore RCO2 section (Fig. 2a) shows the
variability of R with depth and location in the upwelling area. Fig. 2a also
shows how seawater respiration is displaced seaward to C8 from the
chlorophyll maximum at C5 (Fig. 1b). The FC section (Fig. 2b)
demonstrates the power of using R to calculate spatial variability of
FC by revealing an FC maximum over the upper part of
the continental slope. The NRE section (Fig. 2c) reveals its inverse
relationship to FC as well as its variability in the water
column. This ability of the water column to retain nutrients would not have
been detected without the original ETS activity profiles. The HEP section
(Fig. 2d), showing the energy production by the ATPases in microbial
mitochondrion and plasmalemma membranes of bacteria and archaea in the water
column, is a new representation of ATP production in oceanographic analysis.
Because a major purpose of all forms of respiration is to make ATP, HEP
should reflect RCO2 in any given section or profile. The similarity
of the RCO2 pattern in Fig. 2a and the HEP pattern in Fig. 2d
confirms this.
Ocean RCO2 filters sinking labile POC and should vary
inversely with benthic R and carbon burial. However, the relationship
between the two variables is more complicated (Figs. 2a and 3a). We can see
this in the R maximum 50 km off the Peruvian coast at C-line position C8. One
might expect low benthic R and carbon burial here (Table 5), but that is
not the case (Fig. 3a). From the difference between integrating the R
function (Eq. 2) to infinity and integrating it to the ocean bottom (z=s), we calculate a high level of benthic R and carbon burial (Fig. 3a). The
minimum NRE at C-line position, C8, in Fig. 2c explains this discrepancy. The
delivery of labile POC to the bottom depends not directly on FC,
but on the ratio of the water column R (Fig. 2a) to FC
(Fig. 2b). Recent studies of the organic carbon preservation on the upper
parts of the Peruvian continental slope support these
calculations of high carbon burial (Fig. 3a.) They find high burial rates at
depths between 200 and 400 m (the upper part of the Peruvian continental slope)
and attribute it to the anoxia overlying these sediments. A C-line section of
the Teff, the difference between NRE and 1, would have revealed a
Teff maximum at C8. One can deduce this from Fig. 3b (lower panel).
ETS measurements can be used not only to calculate FC, NRE, and
HEP, but also to calculate biological heat production , age,
and flow rates of deep and bottom waters . In anoxic waters, if
the background chemistry is known, ETS measurements provide
proxy rate measurements for denitrification ,
NO2- production, nitrous oxide production, and sulfide production
, and even for iron and magnesium reduction rates
. All of these types of microbial metabolism are different forms of R, but they are controlled by
the same basic respiratory ETS with NADH dehydrogenase (Complex 1) as the
common gatekeeper. Furthermore, because the energy generation of
nitrification is based on a variation of this ETS, an ETS measurement is also
likely a proxy for nitrification.
HEP, as ATP generation in the ocean water column,
could have been calculated from RO2 since 1943, the time the
Nobelist Severo Ochoa first established the connection between ATP
production and R. However, until now, calculations of
biological energy production (shown in Fig. 2d), including HEP, in the ocean had not been made
. Now the time is appropriate to make such calculations with
recent research , documenting the
ubiquity of respiratory ETS in the biosphere, how it relates to
RO2, to all other ocean respiratory processes, and to HEP as
ATP production. As we have seen above, HEP and RCO2 in the
Peruvian upwelling system have similar time and space distributions (Fig. 2a and
d). The small difference in the ATP /2e- relationships between oxidative
phosphorylation and the rate of electron transfer in aerobic metabolism and
denitrification has minimal impact. In aerobic metabolism, the ATP /2e-
ratio is 2.5 and in denitrifying microbes ATP /2e- is 1.0
. At the rate anammox research is progressing
, its relative contribution will soon be known, too. In any
case, less ATP should be produced in anoxic waters resulting in a lower HEP.
It will be interesting in the future to look for this difference by comparing
HEP offshore sections made through oxic and anoxic sectors of upwelling
systems.
Conclusions
Organic carbon fluxes are critical components of reliable carbon budgets, but
they are so difficult to measure that rarely can enough measurements be
amassed to construct a synoptic section of FC. Here, from
plankton respiration models, we present an original mode of calculating
FC sections as well as benthic respiration and carbon burial. We
reveal the importance of plankton respiration in determining the capacity of
a plankton community in retaining water column nutrients, develop the concept
of NRE, and demonstrate NRE variability in an
ocean section. In addition, we show that the curvature of the respiration
profile (the exponent b of the power function) controls both the NRE and
FC. Finally, we use respiration to calculate the heterotrophic
energy production (HEP) and the rate of ATP generated by plankton metabolism, and
find an HEP maximum over the shelf break on the upper part of the Peruvian
continental slope.
Acknowledgements
We thank J. Ammerman, R. T. Barber, D. Blasco, R. C. Dugdale, N. Garfield,
and J. Kogelschatz for their collaboration. D. Bourgault uncovered the role
of depth normalization. The suggestions from the three reviewers led to many
improvements in this paper and for their diligence we are thankful. NSF (USA)
grant OCE 75-23718A01 (TTP) funded JASON-76. The Basque Government (NO and I
F-U), MEC (Spain) project BIOMBA, CTM2012-32729/MAR (MG), and CIE (Canary
Islands): Tricontinental Atlantic Campus (TTP) funded the analysis.
Edited by: G. Herndl
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