JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 112, C10011, doi:10.

1029/2006JC003706, 2007

Seasonal rhythms of net primary production and particulate organic

carbon flux to depth describe the efficiency of biological pump in the
global ocean
Michael J. Lutz,1 Ken Caldeira,2 Robert B. Dunbar,1 and Michael J. Behrenfeld3
Received 10 June 2005; revised 8 January 2007; accepted 2 February 2007; published 10 October 2007.

[1] We investigate the functioning of the ocean’s biological pump by analyzing the
vertical transfer efficiency of particulate organic carbon (POC). Data evaluated include
globally distributed time series of sediment trap POC flux, and remotely sensed estimates
of net primary production (NPP) and sea surface temperature (SST). Mathematical
techniques are developed to compare these temporally discordant time series using NPP
and POC flux climatologies. The seasonal variation of NPP is mapped and shows
regional- and basin-scale biogeographic patterns reflecting solar, climatic, and
oceanographic controls. Patterns of flux are similar, with more high-frequency variability
and a subtropical-subpolar pattern of maximum flux delayed by about 5 days per degree
latitude increase, coherent across multiple sediment trap time series. Seasonal
production-to-flux analyses indicate during intervals of bloom production, the sinking
fraction of NPP is typically half that of other seasons. This globally synchronous pattern
may result from seasonally varying biodegradability or multiseasonal retention of POC.
The relationship between NPP variability and flux variability reverses with latitude, and
may reflect dominance by the large-amplitude seasonal NPP signal at higher latitudes.
We construct algorithms describing labile and refractory flux components as a function of
remotely sensed NPP rates, NPP variability, and SST, which predict POC flux with
accuracies greater than equations typically employed by global climate models. Globally
mapped predictions of POC export, flux to depth, and sedimentation are supplied. Results
indicate improved ocean carbon cycle forecasts may be obtained by combining
satellite-based observations and more mechanistic representations taking into account
factors such as mineral ballasting and ecosystem structure.
Citation: Lutz, M. J., K. Caldeira, R. B. Dunbar, and M. J. Behrenfeld (2007), Seasonal rhythms of net primary production and
particulate organic carbon flux to depth describe the efficiency of biological pump in the global ocean, J. Geophys. Res., 112, C10011,
doi:10.1029/2006JC003706.

1. Introduction vertical flux of particulate organic carbon between oceano-

[2] The marine biosphere is a major component of the
global carbon cycle, responsible for roughly half of the
annual photosynthetic absorption of CO2 from the atmo-
sphere [Field et al., 1998]. However, the influence of
marine carbon cycle variability on atmospheric CO2 con-
centrations is poorly understood [Sarmiento and Le Quéré,
1996; Le Quéré et al., 2005]. In particular, there is little
basis to predict how potential alterations in upper ocean
ecosystems may influence the capacity of the ocean to store
carbon [Sarmiento et al., 1998]. Significant variability in the
1
Department of Geological and Environmental Sciences, Stanford
University, Stanford, California, USA.
2
Department of Global Ecology, Carnegie Institution of Washington,
Stanford, California, USA.
3
Department of Botany and Plant Pathology, Oregon State University,
Corvallis, Oregon, USA.
Copyright 2007 by the American Geophysical Union.
0148-0227/07/2006JC003706
graphic regions [Lutz et al., 2002; Neuer et al., 2002]
implies the potential for substantial biogeochemical con-
sequences resulting from alterations to upper ocean dyna-
mics. Changes in the efficiency of the marine organic
carbon cycle may contribute to variability of atmospheric
CO2 on glacial-interglacial timescales [Sigman and Boyle,
2000]. Understanding of the fate of biogenic carbon within
the ocean is essential for improved forecasts of future
atmospheric CO 2 concentrations and rates of global
warming, especially in the context of changing ocean
circulation [Sarmiento et al., 1998; Schmittner, 2005].
[3] The transport of biogenic elements from surface
waters to the deep ocean and sediments occurs through a
variety of processes collectively known as the ‘‘biological
pump’’ [Volk and Hoffert, 1985]. This biogeochemical and
physical system may be conceptually divided into four
interrelated components: production, export, flux to depth,
and sedimentation. During primary production, phytoplank-
ton incorporate dissolved nutrients and inorganic carbon
into particulate organic matter (POM), lowering the partial

C10011 1 of 26
C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP
pressure of CO2 in surface waters, thus enhancing the
ocean’s ability to absorb CO2 from the atmosphere. Much
POM is recycled within surface waters where associated
nutrients support regenerated primary production [Eppley
and Peterson, 1979]. A fraction this POM is exported
beneath surface waters and fluxes to depth within the
ocean’s interior where it is predominantly consumed and
regenerated by subsurface heterotrophs. The minor portion
of POM that reaches the seafloor is mostly remineralized in
support of benthic biological activity. Flux to the seafloor
escaping benthic regeneration is buried in the sediments.
[4] In general, the greater the depth at which sinking
organic carbon is regenerated, the longer time it takes to
return to the photic zone as dissolved CO2, where it may
reenter atmospheric carbon cycle. Organic carbon reaching
the deep ocean is entrained in water masses with longer
flow pathways back to the surface and smaller advective
velocities than in the upper ocean. Ventilation of subsurface
waters occurs on timescales ranging from annual to
hundreds of years in the upper ocean (
100– 1000 m) to
thousands of years in the deep ocean (>1500 m). Carbon
entering sediments may be geologically stored for hundreds
of millions of years. Thus to describe the storage of
biogenic carbon in the ocean, the depth of remineralization
must be known.
[5] This paper explores how global-scale environmental
parameters, sea surface temperature (SST) and the seaso-
nality of net primary production (NPP), relate to the
efficiency of the biological pump. The ability to infer SST
and NPP from remote observations allows for their synoptic
comparison to sediment trap data. This investigation intro-
duces methodology to facilitate the synthesis of these time
series. Our metadata analysis is used to describe the
seasonal efficiency of production-to-flux relationships, eva-
luate hypotheses regarding the functioning of the biological
pump, assemble new particle flux algorithms, and test
parameterization accuracy.
2. Surface Temperature and Seasonality of NPP
[6] Recent evidence indicates water temperature may be a
key environmental parameter influencing the proportion of
NPP exported from surface waters to the deep ocean [Laws
et al., 2000; Rivkin and Legendre, 2001]. This hypothesis
suggests the rate of organic matter recycling is influenced
by SST. Specifically, lower-water temperatures limit the
activity of microbial heterotrophic decomposers more than
the activity of autotrophic producers. This scenario implies
that in colder regions of the ocean, a greater fraction of
production is not remineralized and is therefore available for
export. Furthermore, due to the lack of surface recycling
where SST is colder, exported detritus may be more labile
than where SST is warmer. Laws et al. [2000] propose a
euphotic zone food web model describing biogenic export
relying heavily on this premise. In support of this rationale,
the authors demonstrate a strong near-linear correlation
between observed f ratios, the ratio of new to total produc-
tion [Eppley and Peterson, 1979], and those predicted by
their model. Water temperature alone explains most of the
f ratio variability found in the model by Laws et al. [2000].
[7] Another proposed control on biogenic carbon export
is variability in the efficiency of trophic transfer within the
2 of 26
C10011
upper ocean food web [Berger et al., 1989; Berger and
Wefer, 1990; Lampitt and Antia, 1997; Rühlemann et al.,
1999; Fischer et al., 2000]. This hypothesis suggests that
organic matter recycling is influenced by controls related to
variability of upper ocean ecosystem structure. In particular,
the fraction and biodegradability of production exported
from more variable ecosystems may be greater than from
stable ones. Where the supply of solar irradiation and
nutrients are relatively constant, environments are stable
throughout the year and activities of autotrophs and hetero-
trophs are balanced. Trophic transfer is efficient and recy-
cling dominates. The fraction of production exported is
minimal. Conversely, seasonal environments reflect time-
varying physical conditions, solar irradiation, and nutrients,
and are characterized by ‘‘leaky’’ food webs with tempo-
rally imbalanced components. New production dominates
and rapid autotrophic growth outpaces consumer feeding
and decompositional activity. Particulate matter has a grea-
ter opportunity to avoid surface heterotrophy and be
exported in a more labile or ‘‘fresh’’ state. Thus in variable
environments particulate matter has a greater opportunity to
escape the euphotic zone and be more biodegradable than in
stable environments.
3. Previous Flux Algorithms
[8] The empirical algorithms of Suess [1980], equation
(1) [Six and Maier-Reimer, 1996; Dymond et al., 1997;
Tyrell, 1999], and Martin et al. [1987], equation (2)
[Sarmiento et al., 1998; Hedges et al., 1999; Buesseler et
al., 2000; Fischer et al., 2000] are commonly used to
describe oceanic particulate organic carbon flux:
Cnpp
CfluxðzÞ ¼ ð1Þ
ð0:0283z þ 0:212Þ

0:858
z
CfluxðzÞ ¼ Cexport ð2Þ
z0
Particulate organic carbon flux (Cflux(z); mg Corg m2 d1) is
described as a function of the production of organic carbon
in surface waters (Cnpp) or the export of organic carbon
(Cexport) from the base of the euphotic zone (z0), scaled to
depth below the sea-surface (z). The Suess [1980] equation
was determined from field-based production and sediment
trap flux measurements, collected from the subtropical
eastern Pacific and northwestern Atlantic at depths between
50 and 5400 m. The Martin et al. [1987] normalized power
function is a ‘‘best fit’’ based on sediment trap data
collected in the low to midlatitude east Pacific from depths
between 100 and 2000 m. Global carbon models including
marine biology commonly describe flux to depth using the
fixed parameters shown in equations (1) and (2).
4. Methods
[9] Our approach builds on the relationships of Suess
[1980] and Martin et al. [1987] [equations (1) and (2)] by
using the greater amount of recently available data to
constrain more of the variability between production and
flux to depth. In particular, we compare globally distributed
C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Figure 1. Geographic locations of sediment trap particulate organic carbon flux to depth measurements.
Observations include annual estimates (6) and subannual time series (.). Arrows indicate locations of
the meridional transects of net primary production time series shown in Figure 5.

annual and time series sediment trap flux measurements,
and remotely sensed estimates of NPP and SST. Sediment
traps and satellites allow for the characterization of
marine biogeochemical variability on timescales longer
than the data sets collected through traditional ship-based
oceanography.
[10] The global sediment trap data set assembled for this
analysis contains estimates of flux collected during the
past 25 years. Satellite-based estimates of production are
employed because field-based observations of production
are not available at the same locations and durations as the
sediment trap experiments. Annual climatologies are used to
compare the seasonality of these temporally discordant time
series. Interannual variability is not focused upon in this
study.
4.1. Sediment Traps
[11] Moored sediment traps are funnel-shaped devices
attached at varying depths to line that is fixed in location
to the seafloor [Honjo, 1978]. Settling detritus intercepted
by these funnels collects in sample bottles opened and
closed at the funnel base. Each sediment trap measurement
reflects the total mass of flux collected during each bottle
open-close interval. Sampling frequency and interval dura-
tion typically varies within sediment trap experiments.
Experiments often include interruptions produced during
collection interval malfunctions and between trap deploy-
ments. The result of a sediment trap experiment is typically
a discontinuous time series of average flux rates represen-
ting bottle open-close intervals of variable durations.
[12] The following criteria are used in assembling sedi-
ment trap data that best reflect surface production (Table 1
and Figures 1 and 2):
[13] (1) Values are from depths greater than the local
export depth (ze). The depth of export herein describes
maximum of the euphotic zone and mixed layer depths
during flux formation. Sediment traps located above this
depth may not reflect the flux of particulate matter to the

Figure 2. Depth versus latitude of sediment trap particulate organic carbon flux to depth measurements.
Observations include annual estimates (6) and subannual time series (.).

3 of 26
 Table 1. Sediment Trap Particulate Organic Carbon Flux to Depth (Corg) Observations
C10011

Water Trap Collection interval

depth depth Corg
Region Trap ID Lat. Lon. (m) (m) Start End (mg m2 d1) Labela Reference
Pacific Ocean
Central Bering Sea 58 179 3783 3137 18 Jul 1991 12 Jun 1992 5.53 Honjo [1996]b
Bering Sea, Aluetian Basin AB 53.5 177 3788 3198 7 Aug 1990 25 Jul 1995 6.96 1-D Takahashi et al. [2000]c
Central Okhotsk Sea OS 53 149 1170 258 12 Aug 1990 12 Aug 1991 8.58 Honjo [1996]b
Central Okhotsk Sea OS 53 149 1170 1061 12 Aug 1990 12 Aug 1991 4.08 1-I Honjo [1996]b
S of Kamchatka Peninsula GD 51.5 165 4960 4500 Jul 1991 Jun 1992 4.38 2-D Wong et al. [1994]d,e
W Pacific Subarctic Gyre 50N 50 165 5500 1227 1 Dec 1997 18 May 2000 4.6 2-I Honda [2001]; Honda et al. [2002]b,c
W Pacific Subarctic Gyre 50N 50 165 5500 3260 1 Dec 1997 18 May 2000 3.1 3-D Honda [2001]; Honda et al. [2002]b,c
W Pacific Subarctic Gyre 50N 50 165 5500 5090 1 Dec 1997 18 May 2000 2.3 4-D Honda [2001]; Honda et al. [2002]b,c
Subarctic Pacifc OSP 50 145 4240 200 8 May 1989 16 May 1994 18.2 1-S Wong et al. [1999]c,d,e
Subarctic Pacifc OSP 50 145 4240 1000 27 Mar 1983 16 May 1994 7.42 2-S Wong et al. [1999]c,d,e
Subarctic Pacifc OSP 50 145 4240 3800 23 Sep 1982 16 May 1994 3.10 5-D Wong et al. [1999]c,d,e
Subarctic Pacifc SA 49 173.9 5406 4806 9 Aug 1990 2 Aug 1995 3.93 6-D Takahashi et al. [2000]c
Juan de Fuca Ridge JDF 48.0 128.1 na 2200 9 Sep 1984 10 Aug 1985 2.99 Dymond and Lyle [1994]
N Central Pacific NP-B 46.8 162.1 5670 700 Aug 1985 1 Jun 1986 33.7 Tsunogai and Noriki [1991]d
N Central Pacific NP-B 46.8 162.1 5670 5200 Aug 1985 1 Jun 1986 5.1 Tsunogai and Noriki [1991]d
Subarctic Front Site 8 46.1 175.0 5435 1412 15 Jun 1993 16 Apr 1994 8.11 3-I Kawahata [2002]b
E of Kurile Is. GA 45 165 5830 5300 Jul 1991 Jun 1992 3.01 7-D Wong et al. [1994]d,e
S of Aleutian Is. GB 45 177 6100 5600 Jul 1991 Jun 1992 1.37 8-D Wong et al. [1994]d,e
W Pacific Subarctic Gyre KNOT 44 155 5500 924 1 Dec 1997 13 May 2000 9.1 3-S Honda et al. [2002]c,d
W Pacific Subarctic Gyre KNOT 44 155 5500 2960 1 Dec 1997 13 May 2000 6.1 Honda et al. [2002]c
W Pacific Subarctic Gyre KNOT 44 155 5500 4989 1 Dec 1997 5 Mar 2000 4.2 Honda et al. [2002]c
California Current, Midway MW 42.2 127.6 na 2830 22 Sep 1987 16 Sep 1988 6.02 Dymond and Lyle [1994]

4 of 26
California Current, Nearshore NS 42.1 125.8 na 2829 22 Sep 1987 16 Sep 1988 13.4 Dymond and Lyle [1994]
California Current, Gyre G 41.6 132 na 3664 28 Sep 1987 14 Sep 1988 2.46 Dymond and Lyle [1994]
NW Pacific EM 40.9 142.0 5370 5000 1 Sep 1988 1 May 1989 12.8 Tsunogai and Noriki [1991]d
Subarctic boundary 40N 40 165 5500 953 1 Dec 1997 20 Jan 2000 4.9 4-S Honda [2001]; Honda et al. [2002]b,c
Subarctic boundary 40N 40 165 5500 2986 1 Dec 1997 20 Jan 2000 3.9 9-D Honda [2001]; Honda et al. [2002]b,c
Subarctic boundary 40N 40 165 5500 5016 1 Dec 1997 20 Jan 2000 3.4 10-D Honda [2001]; Honda et al. [2002]b,c
E Japan Sea Sta. T 39.7 132.4 3300 2800 19 Jul 1994 18 Jul 1995 8.1 11-D Hong et al. [1996]
California Current MFZ 39.5 127.7 na 4230 9 Sep 1983 1 Sep 1984 3.48 Dymond and Lyle [1994]
Subarctic Front Site 7 37.4 174.9 5105 1482 1 Jun 1993 9 Apr 1994 6.44 4-I Kawahata [2002]b
Subarctic Front Site 7 37.4 174.9 5105 4588 1 Jun 1993 9 Apr 1994 3.06 12-D Kawahata [2002]b
Monterey Bay S1 36.8 122.0 700 450 Aug 1989 1 Nov 1992 39.5 Pilskaln et al. [1996]c
Kuroshio Extension WCT-7-s 36.7 154.9 5578 1191 19 Aug 1999 29 Aug 2000 4.44 5-I Mohiuddin et al. [2004]
LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP

Kuroshio Extension WCT-7-d 36.7 154.9 5578 5034 19 Aug 1999 29 Aug 2000 3.83 13-D Mohiuddin et al. [2004]
Kuroshio Extension WCT-3-s 36.0 147.0 5615 1108 30 Aug 1998 10 Aug 1999 2.50 6-I Mohiuddin et al. [2004]
Kuroshio Extension WCT-3-d 36.0 147.0 5615 5081 30 Aug 1998 10 Aug 1999 4.06 14-D Mohiuddin et al. [2004]
Subtropical Front Site 5 34.4 177.7 3365 1342 15 Jun 1993 16 Apr 1994 2.89 7-I Kawahata [2002]b
Subtropical Front Site 5 34.4 177.7 3365 2848 15 Jun 1993 1 Jun 1994 4.28 15-D Kawahata [2002]b
Santa Barbara Basin 34.2 120.0 590 540 12 Aug 1993 10 Sep 1996 12.3 Thunell [1998a]c
Subtropical Front Site 6 30.0 175.0 5390 3873 15 Jun 1993 1 Jun 1994 2.67 16-D Kawahata [2002]b
Gulf of California Guaymas Basin 27.9 111.7 700 500 8 Jul 1990 5 Jan 1997 18.9 5-S Thunell [1998b]c
Okinawa Trough JAST01 27.2 126.4 1650 1010 19 Jan 1993 10 Aug 1995 6.23 8-I Honda [2001]b,c
Okinawa Trough JAST01 27.2 126.4 1650 1547 19 Jan 2003 30 Dec 2003 4.11 9-I Honda [2001]b
Ryukyu Trench JAST03 25.1 127.4 3771 3157 8 Oct 1994 10 Aug 1995 1.23 17-D Honda [2001]b,c
South China Sea SCS-N 18.5 116 3750 1000 10 Sep 1987 21 Oct 1988 3.92 Wiesner et al. [1996]; Jianfang et al. [1998]
South China Sea SCS-N 18.5 116 3750 3350 10 Sep 1987 21 Oct 1988 2.02 Wiesner et al. [1996]; Jianfang et al. [1998]
C10011
 Table 1. (continued)
Water Trap Collection interval
C10011

depth depth Corg

Region Trap ID Lat. Lon. (m) (m) Start End (mg m2 d1) Labela Reference
South China Sea SCS-C 14.6 115.1 4310 1200 1 Dec 1990 29 May 1995 4.20 Wiesner et al. [1996]; Jianfang et al. [1998]c
South China Sea SCS-C 14.6 115.1 4310 2240 1 Dec 1990 29 May 1995 3.51 Wiesner et al. [1996]; Jianfang et al. [1998]c
South China Sea SCS-C 14.6 115.1 4310 3770 1 Dec 1990 29 May 1995 2.52 Wiesner et al. [1996]; Jianfang et al. [1998]c
N Equatorial Current NEC 12.0 134.3 5300 1200 21 Nov 1988 16 Dec 1989 0.38 10-I Kemp and Knaack [1996]
N Equatorial Current NEC 12.0 134.3 5300 4300 21 Nov 1988 16 Dec 1989 0.43 18-D Kemp and Knaack [1996]
N Equatorial Counter Current MANOP-S 11 140 na 700 29 Dec 1982 14 Feb 1984 3.12 6-S Dymond and Collier [1988]c
N Equatorial Counter Current MANOP-S 11 140 na 1600 29 Dec 1982 14 Feb 1984 2.33 11-I Dymond and Collier [1988]c
N Equatorial Counter Current MANOP-S 11 140 na 3400 29 Dec 1982 14 Feb 1984 1.61 19-D Dymond and Collier [1988]c
N Equatorial Counter Current MANOP-S 11.1 140.1 na 4620 29 Dec 1982 14 Feb 1984 0.82 Dymond and Lyle [1994]
Equatorial Pacific JGOFS-EqPac-9N 9 140 5100 2150 2 Feb 1992 24 Jan 1993 1.51 12-I Honjo et al. [1995]
Equatorial Pacific JGOFS-EqPac-9N 9 140 5100 2250 2 Feb 1992 24 Jan 1993 1.52 13-I Honjo et al. [1995]
Equatorial Pacific JGOFS-EqPac-9N 9 140 5100 4400 2 Feb 1992 4 Dec 1992 1.09 20-D Honjo et al. [1995]
E Tropical Pacific MANOP-M 8.8 104.0 na 3150 12 Sep 1980 23 Oct 1981 3.78 Dymond and Lyle [1985]; Dymond and Lyle [1994]
Equatorial Counter Current Site 4 7.9 175.0 5260 4743 25 Sep 1992 13 Apr 1993 0.78 Kawahata et al. [2000]f
E Tropical Pacific MANOP-H 6.6 92.8 na 3565 20 Sep 1980 17 Oct 1981 2.44 Dymond and Lyle [1985]; Dymond and Lyle [1994]
Panama Basin PB2 5.4 85.6 3860 890 3 Dec 1979 2 Dec 1980 9 7-S Honjo [1982]d
Panama Basin PB2 5.4 85.6 3860 2590 3 Dec 1979 2 Dec 1980 11 21-D Honjo [1982]d
Panama Basin PB2 5.4 85.6 3860 3560 3 Dec 1979 2 Dec 1980 14 22-D Honjo [1982]d
Equatorial Pacific JGOFS-EqPac-5N 5 140 4493 1191 2 Feb 1992 24 Jan 1993 6.02 14-I Honjo et al. [1995]
Equatorial Pacific JGOFS-EqPac-5N 5 140 4493 2091 2 Feb 1992 24 Jan 1993 4.50 15-I Honjo et al. [1995]
Equatorial Pacific JGOFS-EqPac-5N 5 140 4493 3793 2 Feb 1992 7 Jan 1993 3.69 23-D Honjo et al. [1995]
Equatorial Counter Current ECC 5 138.8 4130 1130 21 Nov 1988 16 Dec 1989 1.78 16-I Kemp and Knaack [1996]
Equatorial Counter Current ECC 5 138.8 4130 3130 21 Nov 1988 16 Dec 1989 0.67 24-D Kemp and Knaack [1996]

5 of 26
Equatorial Counter Current Site 2 4.1 136.3 4888 1769 4 Jun 1991 15 Apr 1992 6.72 17-I Kawahata et al. [2000]; Kawahata et al. [2002]f
Equatorial Counter Current Site 2 4.1 136.3 4888 4574 4 Jun 1991 15 Apr 1992 6.06 25-D Kawahata et al. [2000]f
Equatorial Counter Current Site 1 3.0 135.0 4402 1592 4 Jun 1991 27 Apr 1992 9.33 18-I Kawahata et al. [1998]; Kawahata et al. [2002]f
Equatorial Counter Current Site 1 3.0 135.0 4402 3902 4 Jun 1991 27 Apr 1992 7.83 26-D Kawahata et al. [1998]f
Equatorial Pacific JGOFS-EqPAC-2N 2 140 4397 2203 2 Feb 1992 24 Jan 1993 4.02 19-I Honjo et al. [1995]
S Equatorial Current Site 10 1.22 160.6 3181 1164 1 Oct 1994 16 Apr 1995 1.94 20-I Kawahata et al. [2000]
Equatorial Pacific C 1.04 138.9 na 4445 23 Dec 1982 3 May 1985 3.56 Dymond and Lyle [1994]c
S Equatorial Current MANOP-C 1 139 na 1089 12 Dec 1982 1 May 1985 4.17 21-I Dymond and Collier [1988]c
S Equatorial Current MANOP-C 1 139 na 1889 12 Dec 1982 1 May 1985 5.52 22-I Dymond and Collier [1988]c
S Equatorial Current MANOP-C 1 139 na 2908 12 Dec 1982 25 Feb 1984 5.18 27-D Dymond and Collier [1988]
S Equatorial Current MANOP-C 1 139 na 3495 25 Feb 1984 1 May 1985 3.26 28-D Dymond and Collier [1988]
Equatorial Pacific JGOFS-EqPac-Eq 0.0 140 4358 880 2 Feb 1992 24 Jan 1993 4.65 8-S Honjo et al. [1995]
LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP

Equatorial Pacific JGOFS-EqPac-Eq 0.0 140 4358 2284 2 Feb 1992 24 Jan 1993 4.49 23-I Honjo et al. [1995]
Equatorial Pacific JGOFS-EqPac-Eq 0.0 140 4358 3618 2 Feb 1992 24 Jan 1993 4.37 29-D Honjo et al. [1995]
S Equatorial Current Site 3 0.0 175.2 4880 1357 1 Jun 1992 16 Apr 1993 2.44 24-I Gupta and Kawahata [2000]; Kawahata et al. [2000]f
S Equatorial Current Site 3 0.0 175.2 4880 4363 1 Jun 1992 16 Apr 1993 1.50 30-D Gupta and Kawahata [2000]; Kawahata et al. [2000]f
Equatorial Pacific JGOFS-EqPac-2S 2 140 4293 3593 2 Feb 1992 24 Jan 1993 3.61 31-D Honjo et al. [1995]
Equatorial Pacific JGOFS-EqPac-5S 5 140 4198 2099 2 Feb 1992 24 Jan 1993 2.73 25-I Honjo et al. [1995]
Equatorial Pacific JGOFS-EqPac-5S 5 140 4198 2209 2 Feb 1992 24 Jan 1993 2.72 26-I Honjo et al. [1995]
Equatorial Pacific JGOFS-EqPac-5S 5 140 4198 2316 2 Feb 1992 24 Jan 1993 2.79 27-I Honjo et al. [1995]
Equatorial Pacific JGOFS-EqPac-12S 12 135 4294 1292 2 Feb 1992 24 Jan 1993 1.52 28-I Honjo et al. [1995]
Equatorial Pacific JGOFS-EqPac-12S 12 135 4294 3594 2 Feb 1992 24 Jan 1993 0.71 32-D Honjo et al. [1995]
Tropical Converg., Coral Sea Site 11 13.0 156.0 1832 1315 16 May 1995 1 Apr 1996 1.50 29-I Kawahata and Ohta [2000]f
Tropical Converg., Coral Sea Site 12 17.8 154.8 2821 2304 16 May 1995 16 Mar 1996 0.56 30-I Kawahata and Ohta [2000]f
Peru-Chile current CH3, CH4 29.5 73.2 4360 2323 21 Jul 1993 23 Sep 1994 7.69 31-I Hebbeln et al. [2000]c
Peru-Chile current CH1, CH3 29.5 73.2 4360 3687 2 Nov 1992 23 Jan 1994 7.56 33-D Hebbeln et al. [2000]c
C10011
 Table 1. (continued)
Water Trap Collection interval
C10011

depth depth Corg

Region Trap ID Lat. Lon. (m) (m) Start End (mg m2 d1) Labela Reference
Tasman Front Site 13 35.5 161 3174 1161 1 Jun 1995 1 Mar 1996 2.50 32-I Kawahata and Ohta [2000]f
Subtrop. Front, N Chatham Rise NCR 42.7 178.6 1500 300 9 Jun 1996 15 May 1997 10.1 Nodder and Northcote [2001]
Subtrop. Front, NChatham Rise NCR 42.7 178.6 1500 1000 9 Jun 1996 15 May 1997 20.6 Nodder and Northcote [2001]
Subtrop. Front, S Chatham Rise SCR 44.6 178.6 1500 300 9 Jun 1996 15 May 1997 4.11 9-S Nodder and Northcote [2001]
Subtrop. Front, S Chatham Rise SCR 44.6 178.6 1500 1000 9 Jun 1996 15 May 1997 4.93 10-S Nodder and Northcote [2001]
Subantarctic Zone JGOFS-AESOPS-MS1 53.0 174.7 5441 986 28 Nov 1996 24 Dec 1997 1.25 11-S Honjo et al. [2000]b
Polar Frontal Zone JGOFS-AESOPS-MS2 56.9 170.2 4924 982 28 Nov 1996 27 Jan 1998 4.92 12-S Honjo et al. [2000]b
Polar Frontal Zone JGOFS-AESOPS-MS2 56.9 170.2 4924 4224 28 Nov 1996 27 Jan 1998 1.71 34-D Honjo et al. [2000]b
Antarctic Circumpolar Current JGOFS-AESOPS-MS3 60.3 170.1 3958 1003 28 Nov 1996 27 Jan 1998 6.40 33-I Honjo et al. [2000]b
Antarctic Circumpolar Current JGOFS-AESOPS-MS4 63.1 169.9 2886 1031 28 Nov 1996 27 Jan 1998 6.03 34-I Honjo et al. [2000]b
Antartic Zone JGOFS-AESOPS-MS5 66.2 168.7 3016 1842 28 Nov 1996 3 Nov 1997 2.82 35-I Honjo et al. [2000]b
Antartic Zone JGOFS-AESOPS-MS5 66.2 168.7 3016 937 28 Nov 1996 27 Jan 1998 5.31 13-S Honjo et al. [2000]b
Ross Sea polynya C top 72.5 172.5 493 230 22 Jan 1990 22 Feb 1992 10.8 Dunbar et al. [1998]c
Ross Sea polynya C bot 72.5 172.5 493 443 22 Jan 1990 22 Feb 1992 2.78 Dunbar et al. [1998]c
Ross Sea polynya JGOFS-AESOPS-MS6 73.5 176.9 565 200 28 Nov 1996 27 Jan 1998 5.23 14-S Collier et al. [2000]
Ross Sea polynya JGOFS-AESOPS-MS7b 76.5 178.0 581 206 28 Nov 1996 27 Jan 1998 13.6 15-S Collier et al. [2000]g
Ross Sea polynya JGOFS-AESOPS-MS7a 76.5 178.0 581 465 28 Nov 1996 27 Jan 1998 28.9 16-S Collier et al. [2000]g
Ross Sea polynya JGOFS-AESOPS-MS7b 76.5 178.0 581 481 28 Nov 1996 27 Jan 1998 33.4 17-S Collier et al. [2000]g,h
Ross Sea polynya A top 76.5 167.5 719 230 14 Jan 1990 24 Apr 1991 13.7 Dunbar et al. [1998]
Ross Sea polynya A bot 76.5 167.5 719 669 13 Jan 1990 7 Feb 1992 11.1 18-S Dunbar et al. [1998]c
Ross Sea polynya B top 76.5 175.0 519 230 17 Jan 1990 1 Jan 1992 19.2 19-S Dunbar et al. [1998]c,g,i
Ross Sea polynya B bot 76.5 175.0 519 469 17 Jan 1990 9 Feb 1992 11.2 20-S Dunbar et al. [1998]c,g,i

6 of 26
Atlantic Ocean
Central Fram Strait FS-1 78.9 1.4 2823 2442 20 Aug 1984 15 Aug 1985 0.65 36-I Honjo et al. [1987]
E Fram Strait SP-2, SP-3 78.9 6.7 1669 1118 1 Jul 1988 5 Jul 1990 19.7 37-I Hebbeln [2000]c
N Water polynya, Baffin Bay S5A 76 78 365 258 Aug 1997 Jun 1999 26.9 Hargrave et al. [2002]c
N Water polynya, Baffin Bay S2B 76 73 561 511 Sep 1997 Jul 1999 30 Hargrave et al. [2002]c
N Norwegian Sea BI-1 75.9 11.5 2123 1700 12 Aug 1984 10 Aug 1985 4.60 38-I Honjo et al. [1987]
Greenland Basin GB-23 75.6 6.7 3445 2823 4 Aug 1985 20 Jul 1986 0.88 35-D Honjo et al. [1987]
E Greenland Sea OG7 75N 75.0 10.6 3073 500 23 Jul 1994 15 Aug 1995 10.7 Ramseier et al. [1999]
Greenland Sea OG 72.5 7.7 2700 500 Sep 1988 Jul 1991 7.83 21-S Bodungen et al. [1995]c,d
Greenland Sea OG 72.5 7.7 2700 1000 Sep 1988 Jul 1991 3.16 Bodungen et al. [1995]c
Greenland Sea OG 72.5 7.7 2700 2200 Sep 1988 Jul 1991 0.95 Bodungen et al. [1995]c
Norwegian Basin NB 70 0.4 3350 500 19 Feb 1992 19 Feb 1993 9.81 Bodungen et al. [1995]
LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP

Norwegian Basin NB 70 0.4 3350 1000 19 Feb 1992 19 Feb 1993 6.03 Bodungen et al. [1995]
E Lofoten Basin LB-1 69.5 10 3161 2760 15 Aug 1983 1 Aug 1984 2.21 36-D Honjo et al. [1987]
Voering Plateau VP 67.8 5.5 1300 525 Jun 1986 Oct 1987 6.66 22-S Bathmann et al. [1990]d
Aegir Ridge NA-1 65.5 1 3058 2630 21 Aug 1985 16 Jun 1986 1.62 37-D Honjo et al. [1987]
E Gotland Sea 57.3 20 na 140 1 Sep 1996 30 Jul 1997 16.8 23-S Schneider et al. [2000]d
NE Atlantic L3 54.6 21.2 3027 2200 10 Jun 1992 24 May 1994 2.15 Kuss and Kremling [1999]c
NE Atlantic L3 54.5 21.1 2979 2880 10 Jun 1992 12 May 1993 2.03 Kuss and Kremling [1999]
Mid-European cont. mar. OMEX-2 49.2 12.8 1450 600 1 Jul 1993 3 Sep 1994 5.75 Antia et al. [1999]
Mid-European cont. mar. OMEX-2 49.2 12.8 1450 1050 1 Jul 1993 3 Sep 1994 6.30 Antia et al. [1999]
Mid-European cont. mar. OMEX-3 49.1 13.4 3660 580 1 Jul 1993 12 May 1994 6.03 Antia et al. [1999]
Mid-European cont. mar. OMEX-3 49.1 13.4 3660 1450 1 Jul 1993 3 Sep 1994 10.1 Antia et al. [1999]
Mid-European cont. mar. OMEX-3 49.1 13.4 3660 3260 1 Jul 1993 3 Sep 1994 5.75 Antia et al. [1999]
Madeira Abyssal Plain PAP 48.8 16.5 4850 1000 12 Oct 1995 8 Mar 1998 2.60 24-S Lampitt et al. [2001]c
Madeira Abyssal Plain PAP 48.8 16.5 4850 3000 18 Apr 1989 26 Sep 1999 3.32 38-D Lampitt et al. [2001]c
C10011
 Table 1. (continued)
Water Trap Collection interval
C10011

depth depth Corg

Region Trap ID Lat. Lon. (m) (m) Start End (mg m2 d1) Labela Reference
Madeira Abyssal Plain PAP 48.8 16.5 4850 4700 18 Apr 1989 29 Aug 1999 3.18 39-D Lampitt et al. [2001]c
NE Atlantic L2 47.8 19.7 4553 500 27 Mar 1992 12 Jun 1994 2.96 Scholten et al. [2001]
NE Atlantic L2 47.8 19.8 4551 1033 4 Apr 1993 28 Jun 1995 3.56 Kuss and Kremling [1999]; Scholten et al. [2001]c
NE Atlantic L2 47.8 19.8 4551 2017 10 Jun 1992 28 Jun 1995 5.11 Kuss and Kremling [1999]; Scholten et al. [2001]c
NE Atlantic L2 47.8 19.8 4553 3515 10 Jun 1992 28 Jun 1995 2.35 Kuss and Kremling [1999]; Scholten et al. [2001]c
North Atlantic Drift JGOFS-NABE-48N 47.7 20.9 4435 1110 3 Apr 1989 16 Apr 1990 4.05 39-I Honjo and Manganini [1993]c
North Atlantic Drift JGOFS-NABE-48N 47.7 20.9 4435 2109 3 Apr 1989 16 Apr 1990 3.78 40-I Honjo and Manganini [1993]c
North Atlantic Drift JGOFS-NABE-48N 47.7 20.9 4435 3734 3 Apr 1989 16 Apr 1990 2.74 Honjo and Manganini [1993]
North Atlantic Drift BOFS-48N 47.3 19.5 4555 3100 18 Apr 1989 16 Sep 1990 5.19 Newton et al. [1994]; Jickells et al. [1996]
NE Atlantic POMME-NE 43.5 17.3 3760 400 14 Feb 2001 25 Jun 2002 3.29 Guieu et al. [2005]
NE Atlantic POMME-NE 43.5 17.3 3760 1000 14 Feb 2001 25 Jun 2002 4.93 Guieu et al. [2005]
NE Atlantic POMME-SE 39.5 17.3 4940 400 14 Feb 2001 25 Jun 2002 6.30 Guieu et al. [2005]
NE Atlantic POMME-SE 39.5 17.3 4940 1000 14 Feb 2001 25 Jun 2002 3.29 Guieu et al. [2005]
E Alboan Gyre ALB-4-S 36.3 1.5 2240 645 1 Jul 1997 22 May 1998 26.4 Sanchez-Vidal et al. [2004]
E Alboan Gyre ALB-4-I 36.3 1.5 2240 1170 1 Jul 1997 22 May 1998 16.6 Sanchez-Vidal et al. [2004]
W Alboan Gyre ALB-1-S 36.2 4.26 1004 471 7 Jan 1997 22 May 1998 26.9 Fabres et al. [2002]
W Alboan Gyre ALB-2-S 36.0 4.29 1337 396 7 Jan 1997 22 May 1998 46.6 Fabres et al. [2002]
E Subtropical Gyre JGOFS-NABE-34N 33.8 21.0 5172 1159 3 Apr 1989 16 Apr 1990 2.74 41-I Honjo and Manganini [1993]c
E Subtropical Gyre JGOFS-NABE-34N 33.8 21.0 5172 1981 3 Apr 1989 16 Apr 1990 2.82 42-I Honjo and Manganini [1993]c
E Subtropical Gyre JGOFS-NABE-34N 33.8 21.0 5172 4478 3 Apr 1989 16 Apr 1990 2.03 40-D Honjo and Manganini [1993]c
NE Atlantic L1 33.1 22 5269 2010 20 Sep 1993 25 Sep 1995 1.82 Kuss and Kremling [1999]; Scholten et al. [2001]c
NE Atlantic L1 33.1 22 5269 4075 20 Sep 1993 14 Oct 1995 1.59 Kuss and Kremling [1999]; Scholten et al. [2001]c
Hatteras Abyssal Plain HAP 32.7 70.8 na 5400 7 Jun 1982 28 Apr 1983 2.09 Dymond and Lyle [1994]

7 of 26
W Sargasso Sea OFP 31.8 64.2 4500 500 29 Mar 1984 25 Jun 1998 4.1 25-S Conte et al. [2001]c,j
W Sargasso Sea OFP 31.8 64.2 4500 1500 29 Mar 1984 25 Jun 1998 2.4 43-I Conte et al. [2001]c,j
W Sargasso Sea OFP 31.8 64.2 4500 3200 6 Apr 1978 25 Jun 1998 1.7 41-D Deuser et al. [1981]; Conte et al. [2001]c,j
Madeira Abyssal Plain BOFS-31N 31.6 24.7 5440 4440 10 Dec 1985 27 Oct 1986 1.44 Lampitt [1992]; Jickells et al. [1996]
Canary Current ESTOC-CI 29.1 15.5 3600 900 25 Nov 1991 2 Sep 1994 1.37 26-S Fischer et al. [1996a]; Neuer et al. [1997]c,d
Canary Current ESTOC-CI 29.1 15.5 3600 3077 25 Nov 1991 2 Sep 1994 2.30 42-D Neuer et al. [1997]c,d
Subtropical Gyre E BOFS-28N 28 22.0 4820 3600 7 Oct 1990 28 Jul 1991 1.34 Jickells et al. [1996]
Subtropical Gyre E BOFS-25N 24.6 22.8 4860 3870 14 Oct 1990 27 Sep 1991 1.99 Jickells et al. [1996]
Nares Abyssal Plain NAP 23.2 64.0 na 5847 21 Aug 1983 27 Sep 1984 1.34 Dymond and Lyle [1994]
Cabe Blanc CB3, CB4 21.2 20.7 4100 732 8 Apr 1990 19 Nov 1991 7.1 27-S Fischer et al. [1996b]c
Cabe Blanc CB1 21.2 20.7 3646 2195 22 Mar 1988 8 Mar 1989 3.3 44-I Fischer et al. [1996b]; Fischer et al. [2000]
Cabe Blanc CB2, CB3, CB4 21.2 20.7 4100 3540 15 Mar 1989 19 Nov 1991 4.8 43-D Fischer et al. [1996b]; Fischer et al. [2000]c
LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP

Mauritanian upwelling zone EUMELI-O 21 31 4600 1000 19 Feb 1991 2 Dec 1992 1.8 28-S Bory et al. [2001]
Mauritanian upwelling zone EUMELI-O 21 31 4600 2500 23 Feb 1991 2 Dec 1992 1.5 45-I Bory et al. [2001]
E Atlantic Coastal-Boundary BOFS-19N 19 20.2 3295 2190 21 Oct 1990 2 Jun 1991 21.3 Jickells et al. [1996]
Mauritanian upwelling zone EUMELI-M 18.5 21 3100 1000 12 Feb 1991 2 Dec 1992 20.2 29-S Bory et al. [2001]
Mauritanian upwelling zone EUMELI-M 18.5 21 3100 2500 12 Feb 1991 2 Dec 1992 16.2 46-I Bory et al. [2001]
Mauritanian upwelling zone EUMELI-M 18.5 21 3100 3000 9 Oct 1991 2 Dec 1992 5.3 44-D Bory et al. [2001]
Cabe Verde CV1, CV2 11.5 21 4971 989 5 Oct 1992 5 Apr 1994 4.52 Fischer et al. [2000]c
Cariaco Basin A 10.5 64.7 1400 275 8 Nov 1995 9 May 2005 72.1 30-S Thunell et al. [2000]; Müller-Karger et al. [2004]c,k
Cariaco Basin B 10.5 64.7 1400 440 8 Nov 1995 9 May 2005 53.6 31-S Thunell et al. [2000]; Müller-Karger et al. [2004]c,k
Cariaco Basin C 10.5 64.7 1400 840 8 Nov 1995 9 May 2005 37.3 32-S Thunell et al. [2000]; Müller-Karger et al. [2004]c,k
Cariaco Basin D 10.5 64.7 1400 1255 8 Nov 1995 9 May 2005 30.6 47-I Thunell et al. [2000]; Müller-Karger et al. [2004]c,k
E Equatorial Atlantic GB2, GBN3, GBN6, EA2 1.8 11.2 4314 853 15 Mar 1988 13 Apr 1991 5.97 33-S Fischer et al. [2000]c
Guinea Basin GBN3-l, GBN6-l 1.8 11.1 4502 3921 1 Mar 1989 7 Apr 1991 5.48 45-D Fischer and Wefer [1996]c
W Equatorial Atlantic WA8 0.0 23.5 3744 718 25 Aug 1994 17 Aug 1995 6.82 Fischer et al. [2000]
C10011
 Table 1. (continued)
Water Trap Collection interval
C10011

depth depth Corg

Region Trap ID Lat. Lon. (m) (m) Start End (mg m2 d1) Labela Reference
E Equatorial Atlantic EA3c, EA7, EA9, EA10 0.0 10.8 4385 1138 13 Apr 1991 27 May 1994 4.35 Fischer et al. [2000]c
E Equatorial Atlantic GBS4, GBS5 2.2 9.9 3916 696 1 Mar 1989 30 Mar 1991 5.62 34-S Fischer et al. [2000]c
Guinea Basin GBZ5-l 2.2 9.9 3920 3382 1 Apr 1990 30 Mar 1991 5.75 Fischer and Wefer [1996]
W Equatorial Atlantic WA1, WA4, WA7 4 25.7 5552 771 17 Oct 1992 17 Aug 1995 4.61 Fischer et al. [2000]
E Equatorial Atlantic EA5 4.3 10.3 3490 947 13 Apr 1991 29 Nov 1991 2.16 Fischer et al. [2000]
E Equatorial Atlantic EA8 5.8 9.4 3450 598 15 Dec 1991 6 Oct 1992 6.05 Fischer et al. [2000]
W Equatorial Atlantic WA2, WA3, WA6 7.5 28 5363 602 19 Oct 1992 17 Aug 1995 2.57 Fischer et al. [2000]c
Walvis Ridge WR1, WR2, WR3, WR4-l 20.0 9.2 2221 1663 4 Mar 1988 17 Dec 1991 10.1 Fischer et al. [2000]c
Walvis Ridge WR2-u 20.0 9.2 2196 599 18 Mar 1989 13 Mar 1990 14.0 35-S Wefer and Fischer [1993]
Namibia Upwelling NU2 28.9 14.6 3055 2516 20 Jan 1992 3 Feb 1993 4.41 Fischer et al. [2000]
Polar Front PF3, PF5, PF7, PF8 50.1 5.87 3795 3145 10 Nov 1989 15 Jan 1996 4.93 Fischer et al. [2002]c
Polar Front PF1, PF3, PF5, PF7, PF8 50.1 5.85 3787 658 15 Jan 1987 15 Jan 1996 3.84 Fischer et al. [2002]c
Bovert Island BO1, BO2, BO3, BO4, BO5 54.3 3.34 2728 487 28 Dec 1990 15 Jan 1996 2.19 Fischer et al. [2002]c
Bovert Island BO1, BO2, BO5 54.3 3.34 2729 2209 28 Dec 1990 15 Jan 1996 1.10 Fischer et al. [2002]c
N Weddell Sea Gyre VIII-u 62.1 40.6 3280 2453 1990 1992 0.61 Pudsey and King [1997]
Bransfield St., King George Is. KG1 62.3 57.5 1952 494 31 Dec 1983 25 Nov 1984 21.1 36-S Wefer et al. [1988]; Wefer and Fischer, [1991]
Bransfield St., King George Is. KG1 62.3 57.5 1952 1588 1 Dec 1983 25 Nov 1984 8.20 48-I Wefer et al. [1988]; Wefer and Fischer, [1991]
Bransfield St., King George Is. KG2, KG3 62.4 57.7 1992 687 4 Dec 1984 7 May 1986 3.01 37-S Wefer et al. [1988]; Wefer and Fischer, [1991]c,l
N. Weddell Sea Gyre I-u 63.2 42.7 3798 2971 1990 1992 0.24 Pudsey and King [1997]
Weddell Sea WS3 64.9 2.6 5053 360 16 Jan 1988 4 Feb 1989 6.25 38-S Wefer and Fischer [1991]
Weddell Sea WS2 64.9 2.5 5000 4456 20 Jan 1987 20 Nov 1987 0.47 46-D Wefer et al. [1990]; Wefer and Fischer [1991]

Indian Ocean

8 of 26
Arabian Sea MS-1 17.7 57.9 1447 808 11 Nov 1994 24 Dec 1995 10.5 39-S Honjo et al. [1999]b,c
Arabian Sea MS-1 17.7 57.9 1447 999 11 Nov 1994 24 Dec 1995 10.5 40-S Honjo et al. [1999]b,c
Bay of Bengal North-s 17.4 89.6 2263 809 1 Oct 1987 1 Oct 1988 9.84 Ittekkot et al. [1991]
Bay of Bengal North-d 17.4 89.6 2263 1727 1 Oct 1987 1 Oct 1988 7.26 Ittekkot et al. [1991]
Arabian Sea MS-2 17.4 58.8 1447 839 11 Nov 1994 24 Dec 1995 13.5 41-S Honjo et al. [1999]b,c
Arabian Sea MS-2 17.4 58.8 1447 914 11 Nov 1994 13 Sep 1995 17.2 42-S Honjo et al. [1999]b,c
Arabian Sea MS-2 17.4 58.8 3642 1985 11 Nov 1994 24 Dec 1995 17.4 49-I Honjo et al. [1999]b,c
Arabian Sea MS-2 17.4 58.8 3642 3150 11 Nov 1994 24 Dec 1995 13.2 47-D Honjo et al. [1999]b,c
Arabian Sea MS-3 17.2 59.6 3465 778 11 Nov 1994 24 Dec 1995 13.2 43-S Honjo et al. [1999]b,c
Arabian Sea MS-3 17.2 59.6 3465 873 11 Nov 1994 24 Dec 1995 17.5 44-S Honjo et al. [1999]b,c
Arabian Sea MS-3 17.2 59.6 3465 1870 11 Nov 1994 24 Dec 1995 16.3 50-I Honjo et al. [1999]b,c
Arabian Sea MS-3 17.2 59.6 3465 2979 11 Nov 1994 24 Dec 1995 12.8 48-D Honjo et al. [1999]b,c
LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP

Arabian Sea WAST 16.5 60.5 4016 3027 10 May 1986 15 Oct 1990 8.77 Haake et al. [1993]
Arabian Sea EAST 15.5 68.7 3785 2830 10 May 1986 23 Oct 1990 5.75 Haake et al. [1993]
Arabian Sea MS-4 15.3 61.5 3974 814 19 Nov 1994 24 Dec 1995 8.9 45-S Honjo et al. [1999]b,c
Arabian Sea MS-4 15.3 61.5 3974 2222 11 Nov 1994 27 Aug 1995 11.1 51-I Honjo et al. [1999]b,c
Arabian Sea MS-4 15.3 61.5 3974 3484 11 Nov 1994 7 Dec 1995 8.9 49-D Honjo et al. [1999]b,c
Arabian Sea CAST 14.9 64.1 3904 2954 10 May 1986 24 Feb 1989 5.21 Haake et al. [1993]
Bay of Bengal Central-s 13.2 84.4 3259 906 Oct 1987 Oct 1988 7.23 Ittekkot et al. [1991]
Bay of Bengal Central-d 13.2 84.4 3259 2282 Oct 1987 Oct 1988 7.15 Ittekkot et al. [1991]
Arabian Sea MS-5 10.0 65.0 4411 2363 28 Nov 1994 24 Dec 1995 3.8 52-I Honjo et al. [1999]b
Arabian Sea MS-5 10.0 65.0 4411 3915 28 Nov 1994 24 Dec 1995 3.3 50-D Honjo et al. [1999]b
Bay of Bengal South-s 4.43 87.3 4017 1040 Oct 1987 Oct 1988 6.49 Ittekkot et al. [1991]
Bay of Bengal South-d 4.43 87.3 4017 3006 Oct 1987 Oct 1988 5.59 Ittekkot et al. [1991]
Southern Ocean ANTARES-M2 52 61.5 4600 1300 13 Feb 1994 31 Jan 1995 2.88 53-I Tréguer, unpub.m
Southern Ocean ANTARES-M2 52 61.5 4600 4025 13 Feb 1994 31 Jan 1995 1.56 51-D Tréguer, unpub.m
C10011
C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

deep ocean. On the basis of the geographic and depth

distribution of sediment trap observations, we apply a
first-order approximation of the export zone depth as 100
m at equatorial latitudes (<35°) increasing linearly to 400 m
at high-latitudes (>50°).
[14] (2) Observations are minimally influenced by resus-
pension of benthic surface sediment, typically those from
Reference

depths above the nepheloid layer.

[15] (3) Terrestrial sources of detritus are minimal.
[16] (4) Observations must describe at least one entire
Pilskaln et al. [2004]

year of flux to depth. This includes trap experiments of less

Trull et al. [2001]
Trull et al. [2001]

Tréguer, unpub.m
Tréguer, unpub.m

than a year in duration if the seasonal cycle of flux may

be well approximated. The sediment trap data set assembled
for this study includes 244 annual flux estimates and
153 subannually resolved flux time series used to create
flux climatologies.
[17] Flux climatology construction involves multiple
(mg m2 d1) Labela

52-D
46-S
54-I
55-I

Discrete open-close interval flux to depth data not available in numerical format. Records of flux to depth are digitized from data presented in graphs.

steps depending on the temporal coverage of trap measure-

ments. First, time series are made continuous for the entire
duration of the experiment. Gaps produced during sampling
Excluding KG2 10 Dec. 1985 to 24 Dec 1985 interval of overlap between KG2 and KG3 trap deployments to avoid attenuating seasonality.

bottle failures or between trap deployments are filled with

2.19
1.37
2.47
0.30
0.44
Corg

the linear integral of temporally adjacent observations.

Next, to account for timing inconstancies between trap
experiments, time series are temporally standardized. Tem-
1998
1998
1999
1995
1995

poral standardization involves a method of describing

End

sediment trap measurements that is a combination of the

Collection interval

21 Feb
21 Feb

8 Feb
8 Feb
30 Dec

Data available online (http://www.imars.usf.edu/CAR); F. Müller-Karger, R.Varela, R. Thunell, M. Scranton, and others.

regularly applied techniques.

[18] Authors typically depict sediment trap experiments
Flux corrected for a component potentially associated with pteropod ‘swimmers’ following Collier et al. [2000].

using linear connections between observation midpoints

1997
1997
1998
1994
1994

Climatology open and close dates are estimated as the first days of the month of reported monthly averages.

[Bathmann et al., 1990; Neuer et al., 1997; Honjo et al.,

Data available online (http://usjgofs.whoi.edu/mzweb/data/Honjo/sed_traps.html); S. Honjo and R. Francois.
Start

Data available online (http://www.obs-vlfr.fr/cd_rom_dmtt/ANTARES/A3/a3_parameters.htm); P. Tréguer.

30 Dec
21 Sep
21 Sep

20 Feb
20 Feb

Excluding 10 Feb. 1990 to 8 Feb. 1992 interval of overlap between traps to avoid attenuating seasonality.

1999; Hargrave et al., 2002]. Flux is also frequently

reported in bar-graph format as the average rate during
the open-close intervals of each bottle [Newton et al., 1994;
depth depth

1580
1400
1300
3445
Water Trap

830
(m)

Honjo et al., 2000; Lampitt et al., 2001; Honda et al.,

2002]. Our approach, demonstrated in Figure 3, is a
Due to local cloud cover, remote sensing data used are from
2700 m north of location.
2280
2280
4000
4020
4020

smoothing of the linear style held equal in mass collected

(m)

per bottle interval to the bar-graph style. Dashed lines

Organic carbon estimated as (1.8 * OC = OM) following Kawahata et al. [1998].

connecting bottle midpoints (closed circles) and grey

141.8
141.8
Lon.

73.0
71
71

columns indicate the linear and bar-graph data representa-

tion styles. Open circles designate temporal intersections of
53.8
53.8
62.4

the linear style with sample bottle openings (xo) and clos-
63
63
Lat.

ings (xc). The solid thin line l connects these intersections.

The curve D indicates the ‘‘stretching’’ of line l such that the
integral of D equals the area represented by the bar-graph
Data available online (http://www.whoi.edu/OFP); M. Conte.

style for each bottle:

Multiple trap deployment flux estimates are combined.
Trap ID

Zxc
ANTARES-M3
ANTARES-M3

ð DÞdx ¼ Cflux ; ð3Þ

Labels refer to flux time-series in Figure 8.

xo
PFZ54
PFZ54
PZB-1

where Cflux denotes the average flux rate. The stretch

function D is accomplished by multiplying line l by a daily
cubic spline interpolation of normal distribution constrained
so that the endpoints (open circles) remain constant. The
direction line l stretches to become curve D, up, down, or
Table 1. (continued)

not at all, depends on the flux rate measured in each bottle

Polar Frontal Zone
Polar Frontal Zone
Region

relative to the rates of neighboring bottles. Minimum daily

Southern Ocean
Southern Ocean

flux rates estimated by the stretch function D are

Prydz Bay

constrained not to be negative. Finally, sediment trap

measurements including more than 1 year of observations
are averaged into one climatological year.
m
b

g
h

k
a

e
f

i
j

9 of 26
C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP
Figure 3. Demonstration of the stretch function ((D)dx)
curve fit technique developed to create sediment trap
particulate organic carbon flux to depth climatologies. Time
series standardization involves a combination of the
regularly applied description techniques: a smoothing of
the linear midpoint connection style (dashed lines and .)
held equal in mass to the bar-graph format (grey columns).
Open circles (6) designate temporal intersections of the
linear style with sample bottle openings (xo) and closings
(xc). The solid thin line l shows linear connects these
intersections. The curve D indicates ‘‘stretching’’ of line l so
that the integral of D equals the area represented by the bar-
graph style for each bottle. The direction line l stretches to
become curve D, up, down, or not at all, depends on the flux
rate measured in each bottle relative to that of its
neighboring bottles.
4.2. NPP and SST
[19] NPP is estimated following Behrenfeld and Falkowski
[1997a] using 7 years of 8-day satellite images available
between 19 August 1997 and 24 June 2004. Data sets applied
include the NOAA/NASA AVHRR Oceans Pathfinder SST
(http://podaac.jpl.nasa.gov/products/product216.html),
NASA SeaWiFs surface chlorophyll concentrations, and
photosynthetically active radiation (http://daac.gsfc.nasa.
gov/data/dataset/SEAWIFS/). Images applied display global
coverage with an equal-area grid of 9-km resolution. NPP
climatologies are constructed in manner identical to that of
flux climatologies. During climatology construction, missing
production estimates, for example, those obscured by cloud
cover, are substituted with the linear interpolation of adjacent
values.
4.3. Potential Error
[20] Errors associated with methods used to estimate
marine biogeochemical processes are difficult to assess.
Field-based oceanography is far from a controlled well-
calibrated laboratory experiment. The ability of sediment
traps to accurately measure flux has received much attention
in the scientific literature. Possible trap biases include
inadvertent ‘‘swimmer’’ capture [Lee et al., 1988], uncertain
preservation of trapped particulate matter [Lee et al., 1992],
hydrodynamic interactions with traps of various designs
10 of 26
C10011
[Gust et al., 1994; Buesseler et al., 2000], and influences in
brine and poison addition [Lee and Cronin, 1982; Knauer et
al., 1984]. A standard trap design and methodological
protocol is not adopted by the oceanographic community.
The magnitude of these and other trap biases may be highly
variable and as large as a factor of two or more [Gardner,
2000]. Calibration of sediment trap results have been
attempted [Buesseler et al., 2000; Yu et al., 2001; Scholten
et al., 2001]. In defense of sediment trap technology, we
note that sediment trap results: (1) are interannually consis-
tent with respect to timing, variability, and magnitude of
particle fluxes [Deuser, 1986; Conte et al., 2001]; and
(2) reflect euphotic zone biological variability [Deuser
et al., 1981; Honjo, 1982; Deuser et al., 1990]. We use
sediment trap data sets here because they represent the only
available direct measurements of annual subsurface particle
fluxes through the water column.
[21] To address potential error of sediment trap observa-
tions, estimates global flux to depth include the calibration
rationale suggested by radionuclide studies. The validity of
sediment traps to measure flux to the deep ocean (>1.5 km)
is validated by 230Th and 231Pa calibration studies [Scholten
et al., 2001; Yu et al., 2001]. Within the upper ocean
(<1500 km) these radionuclide studies suggest sediment
traps may often underestimate fluxes. With the exception of
the California margin, Yu et al. [2001] found a trapping
efficiency of 40% is a typical minimum value for the
pelagic upper ocean. To account for the potential under-
trapping error, we report global estimates of flux to the
upper ocean with (observed flux divided by 0.4) and
without radiochemical calibration. This trapping efficiency
estimate may be uncertain in part because of the variable
incorporation of radionuclides on particles of different sizes
[Buesseler et al., 1995; Yu et al., 2001].
[22] Satellite-based estimates of NPP also include sig-
nificant uncertainties [Platt and Sathyendranath, 1993;
Behrenfeld et al., 2002a]. These uncertainties largely stem
from errors in relating surface chlorophyll biomass to
phytoplankton carbon biomass [Behrenfeld et al., 2005].
Furthermore, empirical models used to estimate NPP
from ocean color may not correctly simulate relevant
phytoplankton physiological variability [Behrenfeld and
Falkowski, 1997b; Behrenfeld et al., 2002b; Banse and
Postel, 2003]. Ocean color is a property of the uppermost
portion of euphotic zone and additional factors are
needed to estimate deeper ocean production. Finally,
field-based radiocarbon measurements of production used
to calibrate satellite-derived algorithms include error
[Sakshaug et al., 1997]. A recent performance analysis
indicates various NPP algorithms yield significantly dis-
similar results [Campbell et al., 2002]. We acknowledge
algorithms describing production using satellite data may
have significant systematic biases.
[23] Specific estimates of error regarding satellite-based
NPP and sediment trap flux are not easily quantified and
such an exercise is generally avoided in the literature.
There is no a priori reason to believe errors associated
with sediment trap observations covary with errors asso-
ciated with satellite-based observations. Thus we infer that
statistical significance in the results described below is
found in spite of, and not because of, error in the data sets
used.
C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP
4.4. Seasonal Variation Index
[24] We use the seasonal variation index (SVI) to describe
temporal variability of the time series. SVI is defined as the
coefficient of variation, the standard derivation (s(X))
normalized to the average (X ), of either the NPP or flux
climatologies:
sðX Þ
SVI ¼ : ð4Þ
X
[25] SVI is dimensionless. This description of variability
is statistically similar to the seasonality index, the number of
months required to accumulate one half of the total annual
primary production [Berger et al., 1989; Berger and Wefer,
1990], and the flux stability index, the minimum time taken
for 50% of the annual flux to be collected [Lampitt and
Antia, 1997].
4.5. Annual and Seasonal Production Ratios
[26] Previous research has compared e ratios, the ratio of
flux to export production, to examine the transfer efficiency
of POC [Laws et al., 2000; Francois et al., 2002]. A recent
study shows transfer efficiency described by flux normal-
ized to either production or export yield results of similar
accuracy [Lutz et al., 2002]. Here following the approach of
Suess [1980], we compare the transfer efficiency between
regions using annual production (p) ratios, defined as the
annual particle flux at depth (z) normalized to annual NPP
in the overlying surface waters:
CfluxðzÞ
p ratioðzÞ ¼ ð5Þ
Cnpp
This study also uses seasonal p ratios to examine subannual
production-to-flux dynamics. Seasonal p ratio creation
involves several steps and is conducted at locations where
an entire year of flux time series is available. First, seasons
of production are delineated by dividing NPP climatologies
into autumn, winter, spring, and bloom intervals. The bloom
production interval describes the average production during
the 30 continuous days of an annual record with the
maximum average production rates. Similarly, the winter
production interval describes the average production during
the 30 continuous days with the minimum average
production rates. Autumn and spring production intervals
describe average productions during the intervening time
periods between bloom and winter seasons. The durations
of autumn and spring production intervals varies depending
on the timing of the bloom and winter seasons, and are
constrained to be of at least one month in duration. By this
constraint, 134 time series of production are included in the
seasonal p ratio analysis.
[27] Next, the timings of corresponding sediment trap
flux seasons are determined by adding a temporal lag to the
timing of the production seasons. The temporal lag is
defined by dividing the trap depth (m) by a sinking rate
(m d1). Here we use a sinking rate of 70 m d1 based on
the 1.5-month lag between surface events observed by
satellite and arrival of the consequences of those events in
sediment traps at 3.2 km shown by Deuser et al. [1990].
Finally, seasonal p ratios are determined by normalizing
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C10011
seasons of flux to corresponding seasons of production. We
acknowledge this technique allows for a first-order descrip-
tion of production and flux dynamics, as sinking rates may
differ between seasons, regions, and depths [Berelson,
2002]. Due to the lack of polar wintertime production,
winter season p ratios are absent at latitudes >60°.
4.6. Flux Algorithm With Labile and Refractory
Components
[28] To quantify relationships between satellite-based
NPP and SST data, and sediment trap flux observations,
annual production ratios are estimated using the following
exponential algorithm:


ze
p ratioðze Þ ¼ prd exp þ prr ð6Þ
rld
[29] This algorithm was previously derived from an
empirical fit between regional production and flux measure-
ments [Lutz et al., 2002] and is applied here to determine if
flux can be estimated using environmental parameters
derived from satellite observations. This function describes
the labile and refractory components of flux to depth below
the export zone depth ze [depth (z) minus export zone
depth]. The prd and rld coefficients measure flux that is
available to decay and sinks more slowly. The rld coefficient
describes the e-folding remineralization length/depth scale
and measures the rate of sinking detritus degradation. The
prr coefficient describes the more refractive and more
rapidly sinking portions of flux. Larger prd and prr values
indicate the export of a greater fraction of NPP. Larger rld
values indicate the labile fraction of export sinks deeper
before regeneration. For simplicity, this equation treats
sinking and remineralization rates as constants, although
we acknowledge these factors vary as particles are trans-
formed during their descent through the ocean [Berelson,
2002]. For further derivation of equation (6) see Banse
[1990] and Lutz et al. [2002].
[30] Annual p ratio estimates are used to determine the
coefficients of equation (6) grouped by either SST or SVI.
Coefficient approximation requires the p ratio data be
divided into groups so that the entire water column is
described for each SVI and SST value evaluated. To best
characterize SVI and SST variability, groups used herein are
of equal spacing on a logarithmic-scale for SVI and a linear-
scale for SST. The prd, rld, and prr coefficients are deter-
mined for each group separately. Within each group the prr
coefficient describes the median of the deepest 25% of
p ratios, the depth of which vary slightly between groups.
Thus for the purpose of this comparison it is assumed that
on an annual basis flux to the deepest traps is refractory
relative to upper ocean traps. The prd coefficient describes
the maximum shallow p ratio minus the prr coefficient. The
rld coefficient is determined by fitting equation (6) to the p
ratio data with the previously determined prd and prr
coefficients. For each coefficient the maximum number of
groups is used that yields a statistically significant relation-
ship to either SVI or SST. Hence the number of groups for
the prd and prr parameters differs depending on the avail-
ability of the shallow and deep trap data within each group.
Similarly the grouping for the rld parameter requires a
sufficient number of observations to characterize the entire
C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Figure 4. The geographic distribution of the seasonal variation index (annual standard deviation
divided by average) of net primary production (NPP). This estimate is derived from NPP climatology
modeled following Behrenfeld and Falkowski [1997a] and constructed from 7 years of satellite-based
estimates of sea surface temperature and chlorophyll. Arrows indicate locations of the meridional
transects of NPP time series shown in Figure 5. Missing data (dark grey) indicates landmasses and
permanent ice cover.

water column. Due to the infrequency of sediment trap
observations near the local export zone depth, prd values are
deemed minimal approximations.
5. Results
5.1. Patterns of Remotely Sensed Parameters,
NPP, and SST
[31] The results of our NPP climatology generally agree
with those described by Behrenfeld and Falkowski [1997b].
Here we briefly describe the first-order characteristics of
production temporal variability limited to those relating to
patterns shown by our flux to depth climatology.
[32] The NPP climatology, as described by the SVI
(Figure 4), displays regional- and basin-scale geographic
patterns. Temporal trends of the NPP climatology (Figure 5)
are similar to those found in the literature [Yoder et al.,
1993; Longhurst, 1995] and include the well-known open
ocean equatorial near-constant low productivity, the multi-
ple blooms of temperate and monsoonal regions, and the
intense summer bloom of polar regions. A primary compo-
nent of global distribution of NPP SVI is the increase of
values poleward of roughly 45°S and N, reflecting the
seasonal availability of photosynthetically available radia-
tion and distribution of sea ice.
[33] The heterogeneous distribution of SVI values at
lower-latitudes indicates provinces where interactions of
annual climatic phenomenon with the density structure of
upper ocean waters permit seasonal upwelling. In open
ocean waters, diminished SVI values characterize subtropi-
cal regions of year-round high surface atmospheric pressure
and the seasonal limits of the intertropical convergence
zone. Reduced SVI values characterize the oligotrophic
subtropical ocean gyres and equatorial western Pacific and
Atlantic Oceans, where production is relatively constant
year-round. Narrow longitudinal bands of moderate SVI
values resulting from seasonal water mass divergence
characterize the equatorial upwelling regions of the Pacific
and Atlantic Oceans. Elevated SVI values approximate the
influence of the circumpolar westerlies. Monsoonally influ-
enced regions of the western Indian Ocean exhibit enhanced
SVI values. Larger SVI values typically characterize the
centers of eastern boundary seasonal coastal upwelling and
the associated offshore areas where upwelled nutrients are
advected. Additionally, SVI values reflect the seasonal input
of riverine and aeolian nutrients, as well as limitations to
production, such as mixing of surface waters beneath the
photic zone, phytoplankton self-shading, and herbivore
activity [Parsons et al., 1977; Broecker and Peng, 1982;
Chester, 1990; Duce and Tindale, 1991].

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C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Figure 5. Climatologies of net primary production (NPP; g Corg m2 yr1) versus latitude. Shown are
time series of NPP located along meridional transects, indicated in Figures 1 and 4, within the (a) central
Pacific (134°W), (b) Atlantic (29°W), and (c) Indian (65°E) Oceans. This estimate uses NPP modeled
following Behrenfeld and Falkowski [1997a] and constructed from 7 years of satellite-based estimates of
sea surface temperature and chlorophyll. Missing data (dark grey) indicates landmasses and permanent
ice cover.

[34] The Southern Hemisphere of the Pacific Ocean
indicated by transect A of Figures 4 and 5 epitomizes the
transition from low-amplitude seasonality and diminished
production of equatorial regions to high-amplitude season-
ality and strong summer blooms of polar regions. Heading
south from the equator, between 5° and 15°S, SVI values
decrease as the strength of equatorial upwelling diminishes.
Continuing south, a latitudinal ribbon of elevated SVI
values, between 25° and 35°S, indicates where mixing of
subsurface waters increases surface nutrient levels sufficient
to generate a summer bloom. Adjacently poleward, a
narrow latitudinal band of minimum SVI values, between
35° and 40°S, indicates where upper water column mixing
sustains elevated production year-round, without distinct
spring and fall blooms. Farther poleward SVI values in-
crease as bloom intensity amplifies. The latitude-dependent
SVI fluctuations and the northeast trending ‘‘sustained-
bloom’’ band of diminished SVI values distinguish the
influence of the westerlies, and are less distinctly repeated
at similar latitudes in the western and eastern portions of the
Northern and Southern Hemispheres, respectively.
[35] For much of the global ocean the SVI of produc-
tion and SST show similar trends (Figures 6 and 7).
Poleward of 35° latitude, where waters are cooler than
approximately 18°C, SVI, and SST generally covary. At
lower-latitudes the distribution of SVI and SST varies
depending on regional oceanographic circumstances and
differs significantly between ocean basins. Globally,
neither variability of production nor SST correlates sig-
nificantly with rates of NPP.
5.2. Patterns of Sediment Trap Flux
[36] The results of the flux to depth climatology are shown
in Figure 8. Here we focus on regional- and basin-scale
patterns of flux rather than restate findings of original
sources. Global sediment trap sampling is heterogeneous
in depth and geographic distribution. Often, the water
column is not entirely measured, leaving either shallow,
intermediate, or deep waters uncharacterized. Sediment trap
observations are heavily weighted, by 70%, toward the
Northern Hemisphere. Major portions of the Southern
Hemisphere are uncharacterized, including the deep Antarc-

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C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Figure 6. Latitude versus (a) the Seasonal Variation Index (annual standard deviation divided by
average) of net primary production and (b) sea surface temperature (SST) for the Pacific, Atlantic, and
Indian Oceans. Circles represent data at 1.5° latitude and longitude intervals.

tic circumpolar waters of Atlantic and Indian Oceans. The

Indian Ocean has received particularly little attention, with
less than an eighth of all observations. Large segments of
continental shelf regions are unknown, such as surrounding
South America and much of Antarctica, and bordering the
Indian Ocean. Meagerly characterized open ocean regions
include the equatorial upwelling of the Atlantic and Indian
Oceans, and the moderately productive Southern Hemi-
sphere subtropical convergence. Regions of mesotrophic
productivity have received the majority of attention. The
most productive centers of upwelling regions are not well
characterized. The modestly productive oligotrophic central
ocean gyres are similarly not frequently sampled. Hence
regions characterizing minimum and maximum limits of
global productivity rates largely await description.
[37] Recognition of basin-scale seasonal cycles of flux to
depth is limited by the geographic heterogeneity of sam-
pling and intermittent high-frequency temporal variability
of measurements. Nevertheless, the flux climatology compi-
lation includes five major patterns of seasonality (Figure 8)
similar to those of NPP: polar, equatorial and coastal
upwelling, monsoonal, and subtropical-subpolar. Cycles of
enhanced summertime flux and diminished wintertime flux Figure 7. The seasonal variation index (annual standard
characterize the poles [e.g., Honjo et al., 1987; Bathmann et deviation divided by average) of net primary production
al., 1990; Wefer and Fischer, 1991; Bodungen et al, 1995; versus seas surface temperature (SST) for the Pacific,
Dunbar et al., 1998; Honjo et al., 2000; Schneider et al., Atlantic, and Indian Oceans. Circles represent data at
2000; Takahashi et al., 2000; Wong et al., 1999; Honda 1.5° latitude and longitude intervals.

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C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Figure 8. Climatologies of particulate organic carbon flux to depth (mg Corg m2 d1) derived using
sediment traps versus latitude. Horizontal contours indicate each sediment trap time series of flux to
various depth ranges (shallow 1 km; intermediate >1 and 2.5 km; deep >2.5 km) within the Atlantic,
Pacific, and Indian Oceans. Circles represent the climatological year-day of each sediment trap bottle
observation. Sediment trap experiments are identified in Table 1 by labels located on the right of each
time series.

et al., 2002; Collier et al., 2000; Pilskaln et al., 2004; and production hiatus and summer blooms, respectively. In
additional references in Table 1 and Figure 8]. Polar general, summertime fluxes to shallow, intermediate, and
seasonality is greater than of other regions, with fluxes deep-water depths are 20, 10, and 5 times wintertime fluxes.
ranging from <0.5 to >100 mg Corg m2 d1 during winter Atypical wintertime flux peaks of some polar observations

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C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Figure 9. (a) Seasonal production ratios describing the particulate organic carbon fraction of production
that sinks beneath surface waters associated with each season of production. (b) Seasonal production
ratios normalized to the annual production ratio at each location. Values to the left and right of the dashed
vertical line indicate the factor to which the seasonal p ratios are less or greater than, respectively, the
annual p ratio.

(15 and 19 s) may be due to sediment resuspension [Dunbar
et al., 1998; Collier et al., 2000].
[38] Equatorial seasonality is low and varies little with
depth [e.g., Honjo et al., 1995; Dymond and Collier, 1988;
Kemp and Knaack, 1996; Kawahata, 2002]. Seasons of
maximum flux are generally double the rate of seasons of
minimum flux. Monsoonal seasonality is moderate and
characterized by the multiple flux maxima of the southwest
and northeast monsoons [Honjo et al., 1999]. The range of
rates between seasons of maximum and minimum flux is
typically a factor of four, with minor attenuation of seaso-
nality with increasing depth. Regions influenced by coastal
upwelling show relatively enhanced seasonality [e.g., Neuer
et al., 1997; Fischer and Wefer, 1996; Hebbeln et al., 2000;
Bory et al., 2001]. Maximum fluxes to shallow, interme-
diate, and deep-water depths are typically 13, 9, and 4 times
minimum fluxes.
[39] Flux seasonality of subtropical-subpolar open ocean
waters is characterized by a latitude trending pattern,
whereby maximum fluxes occur later in the year at
higher-latitudes. This pattern is coherent across multiple
sediment trap time series, recognizable in the Atlantic
Ocean in intermediate [e.g., Figure 8: 40-i, 41-i, and 42-i,
Honjo and Manganini, 1993] and deep waters [e.g., Figure 8:
36-d, Honjo et al., 1987; 38-d and 39-d, Lampitt et al.,
2001; 40-d, Honjo and Manganini, 1993; 41-d, Deuser
et al., 1981; Conte et al., 2001; 42-d, Neuer et al., 1997].
This pattern is also apparent in deep waters of the Pacific
Ocean [e.g., Figure 8: 9-d and 10-d, Honda et al., 2002; 12-d,
15-d, and 16-d, Kawahata et al., 2002; 13-d and 14-d,
Mohiuddin et al., 2004]. Overall, flux peaks are delayed by
approximately five days per degree latitude increase. Maxi-
mum flux timings are generally synchronous with the timing
of temperate spring blooms of lower latitudes and summer-
time polar blooms of higher latitudes, with a production-to-
flux lag typically between 40 and 80 days. The range of flux
rates between season’s maximum and minimum flux is
roughly a factor of six.
6. Discussion
6.1. Limitations Using Seasonal Production Ratios
[40] Sediment trap measurements of flux to depth reflect
variability of surface water production whereby periods of
enhanced production generally correspond to periods of
enhanced flux to depth [Deuser et al., 1981; Honjo, 1982;
Deuser et al., 1990]. We use seasonal production ratios
(section 4.5) to characterize global-scale subannual variabi-
lity of particle transport efficiency. Inferences using seasonal
production ratios are limited due to methodological and
natural factors. The seasonal interval technique does not
completely describe subannual variability of production
and flux to depth. For example, dual production blooms

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C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Figure 10. (a) Statistical distribution of seasonal production ratios grouped by depth. Horizontal black
lines designate median values and shaded boxes designate the distribution range 25 and 75% quartiles.
(b) Statistical distribution of seasonal production ratios normalized to the annual production ratio at each
location. Values above and below the dashed horizontal lines indicate the factor to which the seasonal
p ratios are greater or less than, respectively, the annual p ratio. Seasonal p ratio estimates shown are
grouped into the following depth ranges: 1 km wide groups between 0 and 4 km, and >4 km. Quartile
distributions are derived using data shown in Figure 9.

and flux events of monsoonal regions [Honjo et al., 1999] are
not completely characterized. Furthermore, the technique is
limited by interannual differences between the timing of
production and flux to depth time series used to compile
the climatologies. For example, where production and flux
are influenced by long-term climate phenomenon, such as
ENSO [Kawahata and Gupta, 2004], some bloom produc-
tion and flux intervals may be mismatched. Differences in
particulate matter sinking rates between seasons and depths
may further obscure interpretations. Furthermore, the poten-
tial inaccuracy of shallow sediment traps may limit the
interpretation of shallow p ratio estimates. This analysis
represents an initial step toward characterizing subannual
production-to-flux variability.
6.2. The Seasonal Sinking Fraction of NPP
[41] Our results indicate the sinking fraction of produc-
tion is not seasonally constant. The global range of seasonal

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C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Figure 11. Latitude versus the seasonal variation index (annual standard deviation divided by average)
of particulate organic carbon flux to various depth ranges [1 km (6), >1 and 2.5 km (+), and >2.5 km
(4)] and the seasonal variation index of net primary production (.) at sediment trap locations.

production ratios (Figures 9a and 10a) spans four orders
of magnitude, from 0.0003 to 0.93, with much overlap
between seasons. This seasonal range is almost two orders
of magnitude greater than the range of annual p ratios
between different ocean regions (from about 0.001 to 0.1)
[Lutz et al., 2002]. A trend toward lower p ratios during the
bloom seasonal interval is indicated; however, an overlap
between seasonal estimates makes differentiation between
seasons difficult. Much of the global variability in seasonal
p ratios reflects differences between regions that exhibit
different ranges of NPP and different efficiencies of the
biological pump [Lutz et al., 2002; Neuer et al., 2002]. In
order to reduce the influence of variability between loca-
tions and changes between depths, seasonal p ratios are
normalized to local annual p ratios (Figures 9b and 10b).
Normalized p ratios during bloom intervals are on average
half of those during the rest of the year. The greatest range
of normalized p ratios and the bulk of the lowest normalized
p ratios occur during the bloom season at <1 km.
[42] The production ratio results indicate a global-scale
synchronicity in the seasonal functioning of the biological
pump. This pattern may reflect a seasonal change in the
biodegradability of sinking particulate matter. Diminished
bloom p ratios are consistent with a greater proportion of
particulate matter remineralized during enhanced produc-
tion. Increases in flux lability in response to increased
production is suggested by previous flux studies involving
sediment traps [Lee and Cronin, 1984; Lohrenz et al., 1992;
Haake et al., 1993; Newton et al., 1994; Lampitt and Antia,
1997]. Changes of biodegradability may be due to the
seasonal manufacture of skeletal material by phytoplankton.
For example, growth forms of many Antarctic diatoms
progress seasonally from long, lightly silicified chains
(more labile) in the austral spring, to heavily silicified
valves (more dense and refractory) in the autumn and winter
[El-Sayed and Fryxell, 1993].
[43] The pattern of seasonal production ratio may addi-
tionally reflect particulate matter retention or the delay of
sinking particulate matter to reach deeper waters. Dimi-
nished p ratios during bloom production relative to other
seasons is consistent with a portion of bloom-derived
particulate matter being retained to be recycled or fluxed
during latter seasons. Multiseasonal retention and recycling
of detritus within the deep ocean is suggested to explain
seasonal patterns of suspended particulate matter concen-
trations in the northeast Pacific [Bishop et al., 1999].
6.3. Seasonality of NPP and Flux to Depth
[44] The balance between seasonality of production and
seasonality of flux reverses with latitude (Figure 11). At
higher-latitudes seasonality of production is generally greater
than seasonality of flux. At lower-latitudes seasonality of
production is generally less than seasonality of flux. To
account for this latitudinal difference we suggest that
processes influence flux seasonality discernable at lower-
latitudes, where variability of production is diminished, are
masked by the larger-amplitude production seasonality
signal of higher latitudes. Processes that may enhance
low-latitude flux seasonality relative to production include
phytoplankton mass sedimentation events [Kemp et al.,
2000] and transient meteorological forcing of pulsed export
[Conte et al., 2003]. Processes that may attenuate season-
ality between production and flux at high-latitudes include
the regeneration of detritus retained within surface waters,
delayed herbivore growth, and seasonal mixed-layer deep-
ening associated with polar winter onset. Overall, the
production-to-flux seasonality signal may be influenced
by horizontal water mass advection [Siegel and Deuser,
1997], which may covary with rates of production [Lampitt
and Antia, 1997].
6.4. Parameterization of the Annual Sinking Fraction
of NPP
[45] Our analysis of SST- and SVI-associated hypotheses
includes determining relationships between the remotely
sensed parameters and production ratio data, and comparing

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C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Figure 12. Coefficients used to forecast the annual average particulate organic carbon flux to depth
normalized to overlying production [p ratio(ze)] as a function of satellite-derived parameters, the seasonal
variation index of production (SVI; annual standard deviation divided by average) and sea-surface
temperature (SST; °C). Coefficients indicate the components of flux using equation (6): the labile fraction
of export (prd; a and b), remineralization length scale (rld; c and d), and more refractory and rapidly
sinking fraction of export (prr; e and f). Curve fit coefficient algorithms are reported in Table 2.

the ability of algorithms derived to predict flux. Flux
predictions are based on algorithms that describe the coef-
ficients of equation (6) as a function of the remotely sensed
parameters, as outlined in section 4.6. Coefficient parame-
terization involves testing different equation functional
forms (polynomial and exponential), various orders of
equations, and different numbers of data groups to find
the most accurate predictions. Algorithm curve fits were
constrained to not allow negative coefficient parameter-
izations. Figure 12 and Table 2 show the data groupings
and coefficient algorithms that produced the most accurate
flux predictions. Curve fits shown do not imply complex
relationships, but rather show the simplest and most accu-
rate coefficient algorithms attained.
[46] Comparison of SST and p ratio data groups shown in
Figure 12 indicates little significant variation in p ratios for
much of the range of SST. Dissimilar coefficient behavior is
generally confined to minimal SST values. This discontin-
uous distribution may imply that SST influences reminer-
alization in a stepwise manner with little influence until a
certain low threshold temperature is reached, where flux is
more labile as indicated by the prd and rld coefficients.
Alternately, this behavior may reflect SST and SVI covari-
ance, characteristic of lower temperatures (Figure 7). SVI
coefficients and p ratio data groups show somewhat more
continuous distributions and include a larger range of rld
and prr coefficient values. SVI coefficient distributions are
consistent with the suggestion that where production is
more variable, sinking PM is more labile and decays more
rapidly.
[47] Flux to depth forecast performance abilities of
the SST- and SVI-associated parameterizations and the
relationship presented by Suess [1980] are compared in
Figure 13. The most accurate forecast performance is
found using the SVI-related algorithm (Figure 13). All
equations overestimate flux to depth and p ratios in the
upper ocean (1500 m), although to degrees varying
depending on latitude range evaluated. Overestimation of

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C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP
Table 2. Curve Fit Algorithms Describing Coefficients Used to
Estimate Annual Particulate Organic Carbon Flux to Depth
Normalized to Overlying Production (p ratio(ze)) as a Function
of Satellite-derived Parameters, the Seasonal Variation Index of
Production (SVI; Annual Standard Deviation Divided by Average)
and Sea-surface Temperature (SST; °C)
Parameter (x) Coefficient algorithmb
SVI prd = (31 x2 + 49 x + 7.8) 103
rld = 1400 exp(0.54 x)
prr = (2.6 x2  4.2 x + 4.8) 103
SST prd = (0.0060 x4  0.42 x3 +
10 x2  100 x + 340) 103
rld = 2.0 x2 + 60 x + 680
prr = (0.010 x2  0.34 x + 6.0) 103
Coefficients describe flux using equation (6)a: the labile fraction of export
(prd; Figure 12, A and B), remineralization length scale (rld; Figure 12, C
and D), and more refractory and rapidly sinking fraction of export (prr;
Figure 12, E and F).
a z
Equation (6): p ratio(ze) = prd exp( rl e ) + prr.
b d
The functional forms of coefficient algorithms selected are either
polynomial or exponential fits of lowest order constrained to not yield
negative values and produce the most significant curve fits.
c
The number of data groups used are selected to produce the most
significant curve fits.
flux and p ratios is largest using the equation of Suess
[1980], especially at shallow depths. The SVI- and
SST-algorithms perform similarly in the deep ocean
( 1500 m). A portion of the improved accuracy derived
using equation (6) may be due to our incorporation of a
larger range flux and production data available to Suess
[1980]. In the upper ocean the SST algorithm over-
estimates high-latitude flux and p ratios at all latitudes
more than the SVI algorithm. This depth dependant
discrepancy suggests the exponential form of equation
(6) and the depth scaling of the equation of Suess [1980]
do not always account for the most rapid degradation of
detritus in the upper water column.
6.5. Predictions of Annual Flux to Depth
[48] Coupling between surface and subsurface biogeo-
chemical process has been proposed by comparing satellite-
derived estimates of production and sediment trap-derived
flux to depth [Lampitt and Antia, 1997; Fischer et al., 2000;
Antia et al., 2001; Müller-Karger et al., 2005]. We build on
this insight by using parameters in addition to the rate of
NPP to further constrain flux to depth. Algorithms deve-
loped using the remotely sensed parameters, the SVI of
production and SST, and equation (6) allow for predictions
of flux and p ratios and the assessment of forecast accuracy
relative to the equation of Suess [1980].
[49] The accuracy of SVI-associated annual flux and p
ratio predictions allows for prediction of global particulate
organic carbon flux using satellite-derived NPP (Figure 14
and Tables 3 and 4). For much of the global ocean, the
geographic pattern of flux is similar at different depths.
Enhanced export and flux characterize regions where rates
of production and production seasonality are enhanced.
However, in the central northern Atlantic and Pacific
Oceans and in the Southern Ocean where export is
enhanced, flux to the seafloor is diminished. Flux to the
seafloor is greatest on continental shelves and within centers
of coastal upwelling. At depths greater than the continental
shelves the geographic distribution of flux to the seafloor is
C10011
similar to that of flux within the water column. While
absolute flux rates differ, the geographic patterns of flux
and export predicted by the SVI algorithm are generally
similar to other satellite-derived global estimates [Falkowski
et al., 1998; Laws et al., 2000; Müller-Karger et al., 2005],
with proportionally larger fluxes in regions of enhanced
seasonality (for example, higher latitudes and regions of
Nc R2
seasonal upwelling).
10 0.92
10 0.68 [50] Sediment trap-derived estimates of global export are
8 0.96 significantly less than those developed using other methods.
7 1.0 Multiple causes may influence this discrepancy. Accuracy
of sediment trap-derived estimates of export is limited by
8 0.39
7 0.62 the lack of measurements characterizing the upper mesope-
lagic where greatest rates of subsurface recycling occur. As
noted in section 4.3, underestimation of upper ocean fluxes
by sediment traps is suspected for a variety of reasons.
While radiogenic calibration narrows the discrepancy be-
tween estimates, the difference remains significant. Vari-
ability associated with the radiogenic technique may be
responsible [Yu et al., 2001]. Finally, a portion of this
discrepancy may be due to export of dissolved organic
carbon [Carlson et al., 1994] not measurable using sedi-
ment traps.
[51] Sediment trap estimates of flux to the seafloor,
although not significantly dissimilar from one another,
are significantly greater than flux estimated using apparent
oxygen utilization (AOU) in surface sediments [Jahnke,
1996]. This discrepancy may be due to errors associated
with sediment trap and AOU-associated flux methods.
The accuracy of traps within the deep ocean may be
influenced by some of the hydrodynamic limitations
associated with traps in shallow waters. Resuspension of
benthic detritus into deep-water traps may be greater than
anticipated. Multiple factors may limit the accuracy of the
AOU-associated flux estimations. The flux and subsequent
accumulation of settled detritus on the seafloor may be
geographically heterogeneous (for example, favoring to-
pographic low points) and thus not well characterized by
spatial distribution of coring techniques typically used to
collect benthic surface sediments. Benthic biological ac-
tivity and bioturbation may further enhance the geographic
heterogeneity of benthic remineralization [Tedesco and
Wanless, 1991; Meadows and Meadows, 1994]. Finally,
the remineralization of flux arriving on the seafloor may
occur on timescales not assessed by the methods reported in
the work of Jahnke [1996].
7. Conclusions
[52] Theoretical connections have been proposed between
variability of upper ocean dynamics and pelagic biogeo-
graphy [Longhurst, 1995], and between biogeography and
biogeochemical cycling within the ocean [Longhurst and
Harrison, 1989; Lampitt and Antia, 1997]. In particular,
Lampitt and Antia [1997] suggest biogeography, as des-
cribed by the plankton climate categories of Longhurst
[1995], influences marine biogeochemical cycling. Results
presented in this study further establish these findings. Our
analysis suggests variability of production, as characterized
by the seasonal variation index, reflects ecosystem-scale
biogeochemical processes. This connection may be because,
20 of 26
C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Figure 13. Residuals describing the accuracy of algorithms used to forecast annual average particulate
organic carbon flux to depth relative to sediment trap observations grouped by latitude. Residuals indicate
(a) predicted minus observed flux rates (mg Corg m2 d1) and (b) the ratio of predicted to observed p
ratios (flux normalized to production). Flux is estimated as a function of satellite-derived data using the
seasonal variation index (annual standard deviation divided by average) of production- (SVI; 6) and
SST-associated (~) using equation (6), and the equation of Suess [1980] (&).

Table 3. Annual Average Particulate Organic Carbon Export, Flux to Depth, and Flux to the Seafloor in the Global Ocean
Depth Flux (Pg Corg yr1) Methods Reference
Export 1.8; 4.6a SVI-algorithm using sediment trap flux and remotely sensed production this study
1 km 0.88; 2.2a SVI-algorithm using sediment trap flux and remotely sensed production this study
2.5 km 0.31 SVI-algorithm using sediment trap flux and remotely sensed production this study
Seafloor 0.76; 1.6a SVI-algorithm using sediment trap flux and remotely sensed production this study
Export 16 f ratio algorithmb using remotely sensed production Falkowski et al. [1998]
Export 10 Global ocean circulation/biogeochemical inverse model using hydrographic, Schlitzer [2000]
oxygen, nutrient, and carbon data
Export 11 – 13 Pelagic food web models using remotely sensed production Laws et al. [2000]
Seafloor 0.886 ‘Mineral ballast’ sediment trap derived model Klaas and Archer [2002]
Seafloor 0.93 Sediment trap derived flux algorithmc and remotely sensed production Müller-Karger et al. [2005]
Seafloor 0.40 Apparent oxygen utilization of surface sediments Jahnke [1996]
a
Radiogenic calibration.
b
Eppley and Peterson [1979].
c
Pace et al. [1987].

21 of 26
C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP C10011

Table 4. Annual Average Particulate Organic Carbon Export, Flux to Depth, and Flux to the Seafloor (Pg Corg yr1) Divided Into Ocean
Basins
Regiona Area (%) Export Flux to 1 km Flux to 2.5 km Flux to seafloor
Pacific Ocean 43 0.60, 1.5b 0.30, 0.76b 0.12 0.27, 0.55b
Atlantic Ocean 21 0.52, 1.3b 0.24, 0.60b 0.078 0.27, 0.60b
Indian Ocean 15 0.25, 0.62b 0.12, 0.29b 0.044 0.085, 0.16b
Arctic waters 1 0.026, 0.065b 0.0082, 0.020b 0.00081 0.045, 0.11b
Southern Ocean 21 0.42, 1.0b 0.20, 0.51b 0.061 0.079, 0.15b
Estimates are derived as a function of a satellite-derived net primary production (NPP) and the Index of Seasonal Variation (annual standard deviation
divided by average) of NPP using equation (6).
a
Ocean basins are divided such that: the Southern Ocean is delineated south of 40°S; Arctic waters are delineated north of 70°N; the Indian Ocean is
delineated east of the Cape of Good Hope (20°E) and west of Sumatra and Australia from Cape Londonderry (127°E) to Melbourne (147°E); the Atlantic
Ocean includes the Mediterranean Sea, which has minor a contribution to global flux.
b
Radiogenic calibration at depths <1.5 km.

by measuring environmental change, SVI of production
reflects pelagic ecosystem structure [Longhurst, 1995].
[53] The following conclusions are based on our study of
the biological pump: The NPP climatology displays sea-
sonal patterns coherent over large geographic provinces,
indicating the relative dominance of solar, climatic, and
oceanographic controls on the annual variability of NPP. In
general, seasonal patterns of flux reflect those of production.
Prominent patterns of flux include polar, equatorial upwelling,
coastal upwelling, monsoonal, and within subtropical-

Figure 14. Global ocean forecasts of annual average particulate organic carbon (a) export from surface
waters, (b) flux to the base of the mesopelagic zone (1 km), (c) flux to the center of the bathypelagic zone
(2.5 km), and (d) flux to the seafloor (g Corg m2 yr1). Flux is estimated as a function of a satellite-
derived net primary production (NPP) and the seasonal variation index (annual standard deviation
divided by average) of NPP using equation (6). Flux to the seafloor employs the TerrainBase 5-min
global bathymetry available from the National Geophysical Data Center.

22 of 26
C10011 LUTZ ET AL.: SEASONALITY OF THE BIOLOGICAL PUMP
subpolar regions. Notably, within subtropical-subpolar open
ocean regions the timing of maximum flux is delayed by
approximately 5 days per degree latitude increase. Coher-
ence of flux patterns between multiple widely dispersed
locations demonstrates the ability of sediment traps to
characterize sinking particulate matter. Seasonal produc-
tion-to-flux analyses indicate POC vertical transfer efficien-
cy is significantly seasonally variable. In particular, the ratio
of flux to production during bloom production is typically
half that of the remaining year. Comparison of production
and flux variability shows a latitudinal dependant relation-
ship. At lower-latitudes seasonality of flux is typically
greater than that of production, while at higher latitudes,
seasonality of production is typically greater than that of
flux. This reversal of variability may describe a biogeo-
graphic distinction in the controls of production-to-flux
relationships.
[54] By analyzing a globally distributed data set of NPP
and flux to depth, we show the accuracy of algorithms
describing flux is improved by incorporating SVI- and SST-
related controls and describing labile and refractory sinking
fractions of production. The use of the Behrenfeld and
Falkowski [1997a] global NPP model with equation (6),
parameterized as a function of the SVI of production and
SST, yields annual satellite-based estimates of deep-sea
particulate fluxes with greater skill than the commonly
applied equation of Suess [1980]. Global-scale coherence
between seasonal patterns of production and flux to depth
demonstrate the influence of annual climatic variability on
the marine carbon cycle. Results suggest atmospheric CO2
variability is influenced by changes in ecosystem structure
as well as the rate of production.
[55] Differentiation between SVI- and SST-associated
controls is limited because of their covariance. Correla-
tions found do not prove causality. Furthermore, the
potential for systematic error in either the NPP or
sediment trap flux data may influence the accuracy of
predictions. Greater confidence in flux to depth forecasts
may require consideration of additional NPP model esti-
mates [Campbell et al., 2002], flux to depth techniques
[Buesseler et al., 2000], or other marine carbon cycle
methodologies [e.g., Aydin et al., 2004; Bishop et al.,
2004]. This study is an initial step toward characterizing
the efficiency of the biological pump.
[56] Evaluation of additional flux mechanisms may help
refine remotely sensed flux relationships and further improve
simulation of the marine biogenic carbon cycle. For example,
microbial heterotrophic activity responds to the rate of NPP
[Lucas et al., 1986] and thus may influence the SVI-derived
relationship. Differences in the mineral ballast of phytoplank-
ton may contribute to seasonal variability of particulate
organic carbon flux and remineralizaiton [Armstrong et al.,
2002; Klaas and Archer, 2002]. Additional factors that may
influence the efficiency of the biological pump include
plankton community structure variability [Boyd and Newton,
1995; Arrigo et al., 1999], phytoplankton taxa-specific
particulate matter biodegradability [Dunbar et al., 2003],
the vertical migration of zooplankton [Bishop et al., 1986;
Bishop, 1989], physical forcings of surface waters [Conte et
al., 2001; Fischer et al., 1996b], multiseasonal recycling and
retention of subsurface particulate matter [Bishop et al.,
1999], and mass sedimentation events [Kemp et al., 2000].
23 of 26
C10011
[57] Acknowledgments. We thank the following researchers for their
inspiration and advice: James Bishop (Laurence Berkeley National Labo-
ratory), Kevin Arrigo, Gert van Dijken (for advice on satellite image
processing), Pamela Matson, Alexandria Boehm, Alessandro Tagliabue,
Rochelle Labiosa, and Tasha Reddy (Stanford University). This research
was supported by a number of sources, including the NSF ROAVERRS
program, Lawrence Livermore National Laboratory DOE Center for
Research on Ocean Carbon Sequestration, Stanford University McGee
and A. W. Mellon Foundations, and International JGOFS Program (Ocean
Biogeochemical Modeling Course, Bangalore, India). Finally, we thank the
J. Geophys. Res. reviewers for their recommendations.
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M. J. Behrenfeld, Department of Botany and Plant Pathology, Cordley
Hall 2082, Oregon State University, Corvallis, OR 97331-2902, USA.
K. Caldeira, Department of Global Ecology, Carnegie Institution of
Washington, 260 Panama St., Stanford, CA 94305, USA.
R. B. Dunbar and M. J. Lutz, Department of Geological and
Environmental Sciences, Stanford University, Stanford, CA 94305-2115,
USA. (michael.jlutz@gmail.com)