C HA PT ER 9

Respiration and its measurement

in surface marine waters
Carol Robinson1 and Peter J. le B. Williams2
1
2

Plymouth Marine Laboratory, UK

School of Ocean Sciences, University of Wales, Bangor, UK

Outline
This chapter reviews the current state of knowledge of the process and measurement of microplankton
respiration in marine surface waters. The principal approaches are outlined and their potentials and limitations discussed. A global database, containing 1662 observations has been compiled and analyzed for
the spatial and temporal distribution of surface water respiration. The database is tiny compared to that
of photosynthesis and biased with respect to season, latitude, community structure, and depth. Measurements and models show that the major portions of respiration lies in that attributable to bacteria (1259%)
and to algae (870%). The mean of the volumetric rates of respiration in the upper 10 m of the open ocean is
3.30.15 mmol O2 m3 d1 and that of depth-integrated open-ocean respiration 1168.5 mmol O2 m2 d1 .
A global estimate of 13.5 Pmol O2 a1 is derived from the mean depth-integrated rate, which signicantly
exceeds contemporary estimates of ocean plankton production (2.34.3 Pmol O2 a1 ). This difference is at
variance with the results of mass-balance calculations, which suggest a small difference (ca. 0.18) between
oceanic production and respiration. The reasons for this are discussed.

9.1

Introduction

This chapter reviews our present understanding

of the process of marine planktonic respiration,
and the methodologies used for its determination. We collate the global database of measured
respiration and use it to assess how far we can determine seasonal, regional, and latitudinal patterns of
distribution. Measurements of respiration are not
yet routine within national and international marine
biogeochemical programs. A signicant relationship
between respiration and more routinely measured
parameters would substantially progress our ability to determine its spatial and temporal variability.
We investigate whether such a relationship exists.
Linked to this is the importance of an appreciation
of the distribution of respiration within the microbial food web, and so improved food web model

parameterization and verication. When considered

on comparable time and space scales, the balance
between plankton respiration and photosynthesis
indicates the potential amount of photosynthetically
xed carbon available for export from the upper
mixed layer. We assume that the epipelagic zone of
the open oceans approaches this ideal, and analyze
the distributions of respiration and photosynthesis in order to assess the global balance between
photosynthesis and respiration.

9.2 Available approaches and their

constraints
Rates of planktonic respiration can be derived in
a number of ways: (i) from the measurement of
the rate of production/consumption of a product
147

chap09 2004/11/8 page 147 #1

148

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

or reactant, (ii) the assay of an appropriate respiratory enzyme or enzyme system, (iii) predictions
from biomass, and (iv) from inverse models of the
community composition and activity.

9.2.1

Flux of products and reactants

Principle of the approach

This approach is based on the measurement of the
change of a reactant (e.g. oxygen) or product (e.g.
carbon dioxide) of respiration over a period of time
(characteristically 12 or 24 h) in the dark. The basic
requirement is the ability to analyze the sample,
a replicate or a representative body of water at
point(s) during the incubation period. The most
common method is the in vitro dark bottle incubation, which was originally developed as a means
of accounting for respiration during the determination of photosynthesis within the light/dark
bottle protocol. For reasons of sensitivity, oxygen is
the usual determinant and comprises most (>90%)
of the global database. Carbon dioxide (either pCO2
or total dissolved inorganic carbon, DIC) has also
been used (Johnson et al. 1983, 1987; Robinson and
Williams 1999; Robinson et al. 1999). Dark incubations are necessary for the measurement of respiration via oxygen or carbon dioxide ux to eliminate
concurrent counter uxes of the same compounds
by photosynthesis. The dark bottles are incubated
at in situ temperature, either deployed on an in
situ rig (usually alongside samples incubated for
determination of primary production), or held in
temperature controlled incubators. In order to measure respiration occurring in both the light and the
dark, an extension of the oxygen ux method has
been developed. This entails subtracting measurements of net community production (derived from
the oxygen ux during a light bottle incubation)
from concurrent measurements of gross photosynthesis (derived from 18 O2 production from a light
bottle incubation of a sample spiked with 18 Olabeled water, Bender et al. 1987; Grande et al.,
1989a,b).
The in vitro nature of the incubation potentially can give rise to errors, which has prompted
attempts to determine respiration by measuring
oxygen and carbon dioxide changes in situ. This

relies on the ability to sample consistently within

the same water mass and to account for nonrespiratory processes which would alter the concentration of the chosen reactant. Depending on
the timescale, these latter processes could include
airsea exchange, evaporation and precipitation,
and production/dissolution of calcium carbonate.
The use of sulfur hexauoride (Upstill-Goddard
et al. 1991) signicantly increases the ability to track
a particular water mass over several days, thereby
allowing consecutive estimates of community respiration to be made. However, in order to obtain a
satisfactory signal to noise ratio the spatial variability of the reactant within the labeled area needs to
be small in comparison with the time-dependent
change in the dark period due to respiration. Low
latitude, low energy gyre systems with long welldened dark periods offer the most favorable physical circumstances, however respiration rates in such
systems are characteristically low (see Williams and
Purdie 1991). High latitude, high energy systems
with short and poorly delineated dark periods and
high spatial variability offer the least promising
circumstances.
Limit of detection
The limit of detection of the in vitro approach is
determined by a combination of (i) the precision of
the analytical technique, (ii) the number of replicates, (iii) the ambient concentration, and (iv) the
incubation time. The analytical methods for oxygen
and carbon dioxide work near the practical limits of
volumetry (estimated to be 0.02%, Robinson and
Williams 1991), so the ambient concentration is the
main determinant of the sensitivity of the analytical method. In Table 9.1 the theoretical limits of
oxygen and carbon dioxide derived rate measurements have been estimated. As oxygen solubility is
strongly temperature dependant in the oceans, the
calculation of this gas has been made for a range
of temperatures. These are estimates of best performance; the precision of the analyses falls away in
areas of high particulate load (see Hopkinson and
Smith, Chapter 8) and under eldwork conditions.
The nal determinant is the time of incubation. In the
euphotic zone, where there is a diel cycle of oxygen
and carbon dioxide ux, then 12 or 24 h incubations

chap09 2004/11/8 page 148 #2

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

149

Table 9.1 Calculation of the precision limits for the measurement of changes in oxygen and total inorganic carbon concentrations
Determinant
CO2
O2
O2
O2

Water temperature
( C)

Ambient concentrationa
(mmol m3 )

Coefcient of variation
of the methodb (%)

Limit of analytical
detectionc (mmol m3 )

0
15
25

2100
350
250
200

0.02
0.02
0.02
0.02

0.6
0.1
0.07
0.06

a Rounded off value, calculated from the specied temperature and a salinity of 35.

b From Robinson and Williams (1991).

c Calculated, assuming four replicates, as 2 (2 ambient concentration coefcient of variation/(100 4)).

have a logic. In deeper water, the diel cycle has little or no relevance, and the important consideration
here is the continued linearity of the rates.
Random and systematic errors
The measurement of respiration will be subject
to a number of random and potential systematic
errors. Random errors derive from two sources:
(i) the analytical method for the measurement of
the reactant and (ii) a form of time-dependent randomness between the incubated replicates. The former can be determined from the precision of the
zero time measurements, the latter by the difference between the precision of the zero time replicates and that of the incubated replicates. These
errors need to be reported, as they set the precision and therefore the signicance of the observations. Typical median coefcient of variation of
the zero time dissolved oxygen replicates during
eldwork conditions fall in the region of 0.015
0.07% while that of dark incubated dissolved oxygen
replicates are 0.080.15% (Robinson et al. 2002a,b).
Typical means of the standard errors of respiration measurements derived from dissolved oxygen ux range from 0.06 to 0.5 mmol O2 m3 d1
(Williams and Purdie 1991; Robinson and Williams
1999; Robinson et al. 2002a,b; Williams et al. 2004).
The median standard error of the oxygen ux
derived rates of respiration collated for this review
is 0.2 mmol O2 m3 d1 (n = 1012). The determination of respiration from the coulometric analysis of dissolved inorganic carbon ux is less
precise and the analytical method requires frequent calibration to maintain its accuracy. Reported
means of the standard errors of the combined

respiration and net community production determinations derived from DIC ux during eldwork are
11.5 mmol C m3 d1 (n = 19), and of respiration
measurements alone, 0.8 mmol C m3 d1 (n = 11)
(Robinson and Williams 1999; Robinson et al. 1999,
2002a).
Errors of accuracy (systematic errors) are always
difcult to assess, particularly when no reference
is available. We have categorized these nonrandom
errors under three headings: procedural errors,
errors of containment, and errors of interpretation.
The separation is not perfect but sufces for the
purpose of discussion.
Procedural errors
The necessity to derive respiration measurements
from oxygen and similar parameter changes in the
dark gives rise to two forms of error: (i) omission in
the determined rate of light-associated respiration
and (ii) a time-dependent run down of respiration due to a decrease in the concentration of the
substrates that fuel respiration.
There are two forms of respiration that
occur exclusively or predominantly in the
lightnotably the Mehler and the RUBISCO
oxidase/photorespiration reactions. These, and
their implications for the measurement of respiration, have been discussed by Raven and
Beardall (Chapter 3) and Williams and del Giorgio
(Chapter 1). They cannot be measured by the
conventional dark bottle approach. Whether this is
a problem, or a blessing, depends upon the purpose
of the measurements. The argument is made in
Chapter 1 that these reactions have little to do
with organic metabolismparticularly the Mehler

chap09 2004/11/8 page 149 #3

150

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

reactionand that for much ecological work its

omission from the respiration measurement is more
likely a gain rather than a loss. This would not
be the case for fundamental physiological work
directed to photon capture and quantum yield
when these two processes would need to be taken
into account. The circumstances surrounding the
RUBISCO oxidase/photorespiration reactions are
less straightforward in this respect.
The run down of respiration due to the exhaustion
of substrates has received the attention of a number
of workers. Of 34 published time courses (Williams
and Grey 1970; Williams 1981; Harrison 1986;
Hopkinson et al. 1989; Kruse 1993; Biddanda et al.
1994; Pomeroy et al. 1994; Sampou and Kemp 1994;
Blight et al. 1995; Arstegui et al. 1996; Carlson et al.
1999; Robinson et al. 1999; Robinson 2000; Robinson
et al. 2002b), more than 80% show a linear rate of
decrease in oxygen concentration (i.e. no observable
change in respiration rate) for at least the rst 6 days
of incubation. In only two inshore studies (Williams
1981; Pomeroy et al. 1994), where respiration rates
were high (from 5 to 11 mmol O2 m3 d1 ) were
monotonic decreases or increases in oxygen concentration seen during incubations of less than 1 day.
Where nonlinearities have been encountered it is
possible to calculate the error that would have been
incurred by using the simple two time point 24 h
incubation and this varies from 2 to 20%; the very
high proportion of linear time courses suggests that
the lower estimate is the more representative one.
Long dark incubations give rise to more subtle
problems in that they may disrupt any inherent
diel cycle. Recent studies have highlighted the diel
synchrony of growth of photosynthetic prokaryotes
in both culture and open-ocean situations (Zubkov
et al. 2000; Jacquet et al. 2001). A 24 h dark incubation of a picophytoplankton dominated community
would therefore disrupt this light : dark cell cycle.
The consequences and importance of such an effect
are unknown.
Errors of containment
All in vitro approaches (be they in 50 cm3 bottles
or 10 m3 mesocosms) involve containment. Containment may cause two categories of error; (i) the
sample size will involve omission of part of the

heterotrophic community, (ii) the container itself

may impact the enclosed population giving rise to
so-called bottle effects.
The omission of organisms will have two consequences: (i) there will be loss of a component of
respiration, (ii) the absence of a predator will remove
grazing pressure and so control on the abundance
of the prey will be lost. Larger organisms occur
at sufciently low abundances that they are poorly
sampled by in vitro procedures, and so community
respiration is in this respect underestimated. It is
possible to quantify the effect in order to establish its
signicance. Distributions of individual abundances
and cumulative respiration rates can be derived
from observed or theoretical proles of biomass.
Figure 9.1 (based on Platt and Denman 1977) shows
the theoretical distribution of both abundance and
cumulative respiration with size. The intersection of
the two straight lines shows the individual size (ca.
50 m) above which the organisms are poorly represented (less than 10 dm3 ) in samples taken for
in vitro studies. However, by this size, in excess of
99% of calculated respiration is accounted for by the
smaller size fractions (see circles in the gure). An
extensive analysis is summarized in Fig. 9.15, and
suggests a gure of 3% of respiration associated with
organisms greater than 100 m. Hernandez-Leon
and Ikeda (Chapter 5), on the other hand, suggest
a larger contribution of zooplankton to total respiration, in the order of 6 to 10% of the total water column
respiration. Thus, although the omission of large
organisms does not introduce a substantial error to
estimates of community respiration, the larger size
classes cannot be ignored.
Omission of a predator will have a potential
secondary effect on respiration deriving from the
increase of biomass of the prey and its associated respiration. Pomeroy et al. (1994) showed the
increase in bacterial numbers and substrate assimilation rates which can occur during bottle incubations,
which they concluded was due to the disruption of
the grazer/prey link within the food web. These
effects may be expected to be greater in size fractionation studies in which the size fraction greater
than for example, 1 m is removed. Sherr et al.
(1999) found a 2 to 8 fold increase in bacterial
activity of a 1 m ltrate incubated for 23 days.

chap09 2004/11/8 page 150 #4

Individuals dm3

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

151

Number of individuals dm3

10 individuals dm3
Integrated respirationModel A
95% of cumulative respiration
99% of cumulative respiration

Size (m)
Figure 9.1 Calculated size distribution of numbers of individuals and cumulative respiration. The circles are the points of 99% and 95%
cumulative respiration. Details are given in Fig. 9.14.

Where concomitant measurements have been made

of changes in bacterial abundance and respiration
rate, it has been found that whereas the former may
increase, this surprisingly is not accompanied with
an increase in community respiration rate (Pomeroy
et al. 1994; Blight et al. 1995).
Aside from purported bottle-induced increases in
bacterial numbers, there are well-dened instances
of contamination effects, notably from heavy metals.
This was one of the foci of the Planktonic Rate Processes in the Oligotrophic Oceans (PRPOOS) study
and it was found (Marra and Heinemann 1984) that
with careful attention to detail and cleanliness these
effects could be overcome.
Errors of interpretation
The oxygen technique determines the decrease of
oxygen in the dark and makes the assumption that
this can be attributed to the physiological process
of respiration. This assumption has been challenged
by Pamatmat (1997), who argued that the decomposition of hydrogen peroxide, which gives rise to
the production of oxygen, could aliaise the respiration measurements, depending upon the technique
used to measure oxygen. Polarographic oxygen sensors and mass spectrometers will accurately record
the changes in oxygen concentration; as a consequence the decomposition of hydrogen peroxide

would be recorded, quite properly, as the production of oxygen in the dark and therefore give rise
to an underestimation of respiration. This would
not occur if the Winkler reaction were used, as the
reagents will react with hydrogen peroxide and so
would be falsely but fortuitously recorded as the
equivalent amount of oxygenhence recording no
net change due to the decomposition of hydrogen
peroxide.
Pamatmat further discussed a cycle of hydrogen
peroxide, which he claimed would give rise to the
net production of 1/2 mole of oxygen per cycle.
Pamatmats proposed hydrogen peroxide/oxygen
cycle can only give rise to net oxygen production at
the expense of reduced structures. Whereas such a
supply of organic proton and electron donors may
exist in the types of environment he studied (tide
pools, saline ponds), they would not accumulate
in signicant quantities in either shelf or offshore
waters.
Signicantly, where hydrogen peroxide concentrations are reported for coastal and offshore
areas they are characteristically in the range of
250 nmol dm3 (Herut et al. 1998; Hanson et al.
2001; Yuan and Shiller, 2001). The ux rates are in the
range, 8230 nmol dm3 d1 (Moffett and Zariou
1993; Yocis et al. 2000; Yuan and Shiller 2001). Both
concentrations and uxes of hydrogen peroxide are

chap09 2004/11/8 page 151 #5

152

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

low in relation to their oxygen counterparts, and

close to, or more often below, the sensitivity of the
methods used to measure in vitro oxygen uxes.
In polluted waters, hydrogen peroxide concentrations are higher (8100 nmol dm3 ; Herut et al.
1998), but even here they are near to or beyond
the limit of the Winkler oxygen technique and so
are a minor source of error in relation to the high
respiratory oxygen uxes observed in such waters.
Thus, present understanding of hydrogen peroxide cycling implies that the rates would be beyond
the sensitivity of the Winkler incubation technique in
open-ocean environments. Thus, Pamatmats concerns over the use of the oxygen technique for
both respiration and production would appear to
be unfounded.
Anomalous observations and reconciliation with other
measures of plankton activity and in situ derived
respiration rates
One virtue of the in vitro oxygen ux technique is
the ability to detect anomalous results; for example,
apparent negative respiration rates or oxygen production in the dark. Williams (2000) analyzed a
dataset of 293 observations after ltering the data for
occasions where the gross production or respiration
rate was less than twice its standard error or where
impossible values of negative gross production or
respiration occurred. This ltering process reduced
the dataset by 510%, but the frequency of the negative respiration rates was not differentiated within
this. We have access to the original titration data
of 859 of the in vitro dark oxygen ux data collected for this review. Within this dataset, on only
nine occasions did the nal concentration of oxygen
exceed the initial concentration, and so produce an
anomalous negative respiration rate.
A different anomaly reported in the literature
(Robinson and Williams 1999) is the determination of higher than expected respiratory quotients
(CO2 /O2 ) derived from the concurrent measurement of oxygen consumption and dissolved
inorganic carbon production during a dark incubation. The authors were unable to account for these
measurements without invoking the occurrence of
metabolic processes such as methanogenesis in the
aerobic euphotic zone of the Arabian Sea.

Several studies have addressed the question of

whether in vitro estimates of plankton activity are
representative of in situ rates. With regard to primary
production, differences of 25% between in vitro
and in situ derived rates have been found (Williams
and Purdie 1991; Daneri 1992; Chipman et al. 1993;
Rees et al. 2001). Bearing in mind the difculty
of recreating an appropriate light eld for in vitro
estimates of primary production and the practical
limitations to in situ work, it seems reasonable to
suggest that the difference between in vitro and in
situ derived rates of plankton respiration would be
of a comparable or lesser magnitude.

9.2.2

Electron transport system (ETS) assay

The use of enzymatic indicators to estimate potential respiration is gaining acceptance due to their
sensitivity (<0.1 mmol O2 m3 d1 ), especially for
mesopelagic waters (del Giorgio 1992; Harrison
et al. 2001; Arstegui and Harrison 2002; Arstegui
et al. 2002; and see Hernndez-Len and Ikeda,
Chapter 5). These methods are not yet routinely
used in biogeochemical studies. ETS activity measurements have to be converted to in situ respiration rates by empirically determined relationships
between ETS activity and respiration derived from
dissolved oxygen ux. Such data interpretation
faces problems, but no more so than those of other
commonly used rate process techniques (14 C and
3 H-thymidine; del Giorgio 1992) or extrapolations
of remotely sensed ocean color data to sea surface chlorophyll and primary production estimates
(Sullivan et al. 1993).
The ETS method estimates the maximum activity of the enzymes associated with the respiratory ETSs in both eukaryotic and prokaryotic
organisms. The rate of reduction of a tetrazolium salt (2-(p-iodophenyl)-3-(p-nitrophenyl)-5phenyl tetrazolium chloride (INT)) is used as an
indicator of electron transport activity, and so oxygen consumption or carbon dioxide production
(Packard 1971; Kenner and Ahmed 1975; Arstegui
and Montero 1995). The enzymatic rates are corrected to in situ temperature using the Arrhenius
equation. Activation energies of between 46 and
67 kJ mol1 have been measured (Arstegui and

chap09 2004/11/8 page 152 #6

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

Montero 1995; Arstegui et al. 2002). The ETS technique measures the maximum capacity of the terminal oxidation system in vitro (in the physiological
sense). In vivo rates are controlled by the rates of
oxidative phosphorylation and so the maximum rate
is not thought to be achieved in the whole cell.
The suppression is not constant, varying with taxonomic group and physiological state (Packard 1985),
and so needs to be established empirically. Typical algorithms used are log R(mg O2 m3 d1 ) =
0.357 + 0.750 log ETS (r 2 = 0.75; n = 197; Arstegui
and Montero 1995) for oceanic surface waters or
R = ETS 0.086 (Christensen et al. 1980) for 200
1000 m depths. The error associated with such conversions is estimated to be 30% (Arstegui and
Montero 1995, and see Hernndez-Len and Ikeda,
Chapter 5).

9.2.3

Derivation from biomass

Given measurements or estimates of biomass

within the planktonic community and appropriate
biomass-specic rates of metabolism, a rate of respiration may be calculated. Methods are available to
determine or estimate the biomass of most components of the planktonic community, although they
are often very demanding of time and skill. An
alternative to determining the biomass of individual
organisms or groups is to use generalized derivations of biomass, either from observations (Sheldon
et al. 1972) or theory (Platt and Denman 1978), within
the size spectrum found in marine plankton. These
can be coupled with allometric equations for respiration versus weight or size of the organism (Blanco
et al. 1998). There is some consensus over the rate
versus size relationship for respiration for larger
plankton (see Fenchel, Chapter 4, and HernndezLen and Ikeda, Chapter 5), but as size decreases
the basic assumption that one can specify metabolic
rates becomes less secure: bacteria for instance probably exhibit the greatest metabolic range of all freeliving organisms. Despite its obvious limitations
the approach offers a valuable constraint to eld
observations of the distribution of respiration within
the planktonic size spectrum (Robinson et al. 1999,
2002b).

153

9.2.4 Derivation from activity and growth

efciencies
Rates of primary production, bacterial production,
and to a lesser extent microzooplankton herbivory
and bacterivory are much more frequently determined than rates of plankton community respiration. Therefore, if the growth efciency of each
of these plankton groups can be sufciently constrained, the respiration rate of each group can
be calculated and the community respiration rate
derived by summation. Unfortunately growth efciencies, particularly those of the bacterial fraction,
are not well constrained. While this approach has
been used with some successthe summed estimated respiration of each trophic group falling
within 50% of the measured community respiration (Robinson and Williams 1999; Robinson et al.
1999, 2002b)the reliance upon an estimate of the
growth efciencies is the greatest limitation to this
technique.

9.2.5

Inverse analysis

A different approach to the determination of community respiration or the respiration of a particular

size class or group of the plankton, is to use inverse
analysis (e.g. Vezina and Platt 1988). The procedure incorporates observations of rates or states and
searches for the best t of the unknown metabolic
rate to the eld data. It is potentially a very powerful approach as it is substantially, but not wholly,
objective. However, the analysis is only as good
as the data incorporated, and with many datasets,
several parameters will not be known, requiring
subjective interpretation. Fasham et al. (1999) used
a size structured ecosystem model forced by measured water column integrated primary production
and heterotrophic bacterial production to derive the
size distribution of community respiration during a
diatom bloom in the north east Atlantic. Ducklow
et al. (2000) used equations of carbon ow through
phytoplankton, zooplankton, and bacteria, along
with the constraint of measured community respiration to estimate bacterial respiration, and Anderson
and Ducklow (2001) used a simple steady-state
model of the microbial loop to examine the reliability

chap09 2004/11/8 page 153 #7

154

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

of measured bacterial production, growth efciency,

and hence respiration. As more datasets are collected which encompass concurrent rate and state
measurements of most of the plankton groups, this
procedure will become more commonplace.

analysis of oxygen isotopes. However these latter

problems are likely to diminish with time.

9.3
9.3.1

9.2.6

Future analytical methods

The importance of plankton respiration measurements to an understanding of carbon ow through

the microbial food web, and the relatively few observations currently available from traditional methods, lead us to continually seek new approaches
which could improve our understanding of the
spatial and temporal variability of community respiration as well as that of components of the plankton
community.
The activity of the enzyme isocitrate dehydrogenase (IDH) has been investigated in batch cultures
of marine bacteria in relation to carbon dioxide production and oxygen consumption (Packard et al.
1996). Rates of carbon dioxide production were predicted from models of second-order enzyme kinetics
throughout the different phases of the cultures with
an r 2 greater than 0.84 (Packard et al. 1996; Roy and
Packard 2001). The potential to use this enzyme as
an index of bacterial respiratory production of carbon dioxide in the ocean awaits further investigation
and improvement.
Luz and Barkan (2000) have recently introduced a
method to estimate time-integrated rates of respiration and photosynthesis from the difference between
the triple isotope (16 O, 17 O, and 18 O) composition
of atmospheric and dissolved oxygen and the rate
of airsea oxygen exchange. Their estimates of gross
oxygen production agreed well with rates determined by bottle incubations in the Sea of Galilee
and with seasonal cycles of production determined
in upper ocean waters near Bermuda (Bender 2000).
The advantage of the method is that it integrates over
week to month periods, something that is impossible
to achieve with bottle incubations. The disadvantages are the reliance on knowledge of gas exchange
rates, (an associated error of about 30%) and of the
fractionation by photosynthesis and respiration, and
the cost and skill required for mass spectrometric

Community respiration rates

Overview of the data

Previous collations of community respiration data

have gathered a few hundred measurements
worldwide. Williams (2000) analyzed a dataset of
293 observations and assessed the interconnections
between plankton community respiration, net community production, and gross production. Rivkin
and Legendre (2001) compiled community respiration data from 12 studies (n = 100) in order
to test the predictive capability of their equation
relating bacterial growth efciency to temperature
and their assertion that the major part of community respiration is attributable to bacteria. Robinson
et al. (2002a) collated data from six oligotrophic
studies and four upwelling studies in order to
calculate a mean respiration rate for oligotrophic
regions of 2.4 mmol O2 m3 d1 (<0.712.7; n = 51)
and a mean respiration rate in upwelling areas of
6.5 mmol O2 m3 d1 (033.4; n = 132).
In the present study, we have combined these
datasets and augmented them with recently published data, unpublished data of our own, and
unpublished and published data kindly supplied by colleagues (Arstegui, J., Gonzalez,
N., Lefevre, D., and Morris, P., personal
communication). The data can be accessed at
www.pml.ac.uk/amt/data/Respiration.xls. This
database will continue to be developed and maintained. We anticipate that we have acquired ca.
80% of the existing surface water respiration data.
Data have not been used in the present analysis
when the rate is less than twice the standard error
(95% condence limits). The combined dataset
consists of 1662 respiration data (693 separate stations), collected between 1980 and 2002, from open
ocean, coastal upwelling and shelf sea environments (Robinson and Williams 1993, 1999; Kiddon
et al. 1995; Pomeroy et al. 1995; Cota et al. 1996;
Lefevre et al. 1997; Eissler and Quinones 1999;
Robinson et al. 1999, 2002a,b; Sherry et al., 1999;
Daneri et al. 2000; Hitchcock et al. 2000; Moncoiffe

chap09 2004/11/8 page 154 #8

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

155

Figure 9.2 Global database of respiration measurements positioned on map of SeaWiFs ocean color.

et al. 2000; Dickson and Orchardo, 2001; Dickson

et al. 2001; Gonzalez et al. 2001, 2002). Where
possible the respiration data are supported by
concurrent measurements of in situ temperature,
chlorophyll a concentration, bacterial abundance,
particulate organic carbon, light attenuation, and
gross production. Of the observations, 91% of the
data are derived from Winkler oxygen titrations,
3% from oxygen consumption measured by oxygen
electrode, 4% are daily respiration rates derived
from 18 O2 (i.e. incorporating both light and
dark respiration; Bender et al. 1999), and <2% of
the data are derived from ETS activity. Open-ocean
observations account for 71% of the measurements;
the remainder have been collected on the shelf
(<200 m). Figure 9.2 highlights just how spatially
restricted and depauperate the global database is.
The mean respiration rate of this complete volumetric dataset is 3.5 0.13 mmol O2 m3 d1 (mean
standard error, the standard deviation is 5.3;
range of the mean is 0.0275 mmol O2 m3 d1 ),
and of surface water (<10 m) alone, is
4.9 0.23 mmol O2 m3 d1 . The mean surface
water (<10 m) respiration rate measured in coastal
areas is 7.4 0.54 mmol O2 m3 d1 (n = 323; range
0.175 mmol O2 m3 d1 ), and the mean of surface

water measurements made in open-ocean areas

is 3.3 0.15 mmol O2 m3 d1 (n = 502; range
0.0233.8 mmol O2 m2 d1 ). Where respiration
was measured at three or more depths we have
calculated depth-integrated rates, to the depth of
the deepest sample using a conventional trapezoid
procedure. The integration depth varies from 10 to
150 m with a mean of 53 m and a median of 40 m.
Since respiration measurements have historically
been made in support of gross production measurements, the deepest depth sampled in most cases
is the 1% light depth rather than the mixed layer
depth. The means for the whole depth integrated
dataset (n = 229), the open-ocean dataset (n = 186),
and the coastal/shelf seas dataset (n = 43) are
114 5.1, 116 8.5, and 107 11 mmol O2 m2 d1
(mean standard error;
standard deviation
100 mmol O2 m2 d1 ), respectively.
The respiration data have been assessed with
respect to latitudinal and seasonal distribution and
covariance with more frequently made measures of
plankton biomass and activity. Figure 9.2 indicates
the spatial distribution of the respiration data presented on a satellite image of ocean color. Such a
portrayal of the data emphasizes the urgent need for
more data (Jahnke and Craven 1995; Williams 2000).

chap09 2004/11/8 page 155 #9

156

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

Figure 9.3 Latitudinal distribution of the number of observations of volumetric rates of community respiration. The mean rate for each
latitude band (mmol O2 m3 d1 ) is shown above each histogram.

Figure 9.4 Depth distribution of the number of observations of volumetric rates of community respiration. The mean rate for each depth
range (mmol O2 m3 d1 ) is shown above each histogram.

The frequency histogram of respiration versus latitude (Fig. 9.3) reveals that the greatest number
of samples have been collected within the latitudinal band between 30 N and 50 N where the
mean respiration rate is 4.3 mmol O2 m3 d1 . As
mentioned above, the majority of respiration measurements have been made within the euphotic
zone. Less than 100 measurements of respiration
(5% of the dataset) were collected below 100 m
(Fig. 9.4). Interestingly, of the small number of

measurements made, the mean rate is still relatively

high (>1 mmol O2 m3 d1 ) and easily measurable
with a 24 h oxygen incubation technique. Data are
unevenly distributed throughout the year (Fig. 9.5).
As might be expected, most of the measurements
were collected during the temperate and austral
spring. In the Northern Hemisphere the mean respiration rates for April, May, June and July, were
3.5, 6.2, 5.8, and 8.9 mmol O2 m3 d1 , respectively.
The mean respiration rates for data collected during

chap09 2004/11/8 page 156 #10

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

157

100
8.9

Number of observations

5.8

75

N hemisphere
S hemisphere

3.5
6.2
4.3
7.2

50
5.4

2.6

1.9
2.9
5.4

25

2.1
3.3

0.7

4.4

2.6
4.0

0.3 9.6
2.2

0.9
1.0

0
Jan Feb Mar April May June July Aug Sep Oct Nov Dec

Figure 9.5 Seasonal distribution of the number of observations of volumetric rates of community respiration. The mean rate for each calendar
month (mmol O2 m3 d1 ) is shown above each histogram.

Figure 9.6 Distribution of the number of observations of volumetric rates of respiration with respect to the algal community size structure.
The mean rate for each category (mmol O2 m3 d1 ) is shown above each histogram.

December, January, and February in the Southern

Hemisphere are 2.1, 5.4, and 1.9 mmol O2 m3 d1 ,
respectively. High mean respiration rates measured
in September and November in the Northern Hemisphere are biased by coastal studies undertaken at
this time of the year.
A focus of research in the late 1980s and 1990s
was the study of global carbon cycling and the role
of phytoplankton in drawing down atmospheric
carbon dioxide (JGOFS Science Plan). Hence, one

expected bias in the respiration data is that the

majority of the data were collected during diatom
dominated spring blooms (Williams 1998). We have
therefore analyzed a frequency histogram of respiration against a broad estimate of phytoplankton community structurethe percentage of total
chlorophyll attributable to the smallest cells present
(Fig. 9.6). Note that some authors have measured
the fraction between 0.22 m as their smallest
size band, while others have used <1 m. There

chap09 2004/11/8 page 157 #11

158

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

does seem to be a bias towards data collected during larger cell dominated algal populationswith
a smaller peak at populations, which have a large
proportion (7080%) of smaller cells. This is possibly due to the inclusion of the three datasets from
the Atlantic Meridional Transect program (AMT),
which sample the picoautotroph dominated midocean gyres (Gonzalez et al. 2002; Robinson et al.
2002a). There is no clear pattern between the percentage of chlorophyll attributed to <2 m cells and
the magnitude of respiration.

9.3.2 Analysis of the data

The respiration data are biased with respect to time,
place, community structure, and depth (see Figs 9.2
9.6). The dataset is particularly decient in data from
deeper water and for periods of the year of low photosynthetic activity. As a consequence the dataset
is not comprehensive enough to allow the preparation of maps. In this respect, we are not at the stage
that was reached by the 14 C community in 1968,
when it was possible to produce a realistic map of
oceanic productivity (see discussion in Barber and
Hilting 2002).
Relationships between respiration and chlorophyll,
bacterial abundance, particulate organic carbon,
and attenuation
As community respiration is determined by the
activity of the algal, bacterial, and microzooplankton community present, one may expect that respiration would be correlated with the abundance
or biomass of one or more of the components of
the plankton community. Robinson et al. (2002a)
found signicant (p < 0.001) relationships between
respiration and bacterial abundance, chlorophyll a,
beam attenuation, and particulate organic carbon
(POC) of samples collected along a 12 000 km latitudinal transect of the Eastern Atlantic Ocean.
Robinson et al. (2002b) combined these data with
those collected during a study of a coccolithophore
bloom in the North Sea, and similarly found signicant relationships between respiration, and bacterial
and microzooplankton biomass, POC, and chlorophyll a. Since these latter parameters are less time

and labor intensive in their collection and analysis, these authors drew attention to their value as
predictors of community respiration. Of the variance in respiration, 4050% could be accounted for
by the variation in bacterial biomass or POC. Using
the larger database of respiration measurements collected for the present review we were curious of
the predictive power of one or more of these single variable regression equations. Figure 9.7 shows
weak relationships between respiration, chlorophyll a, POC, bacterial abundance, and attenuation
with their associated major reduced axis regressions. Only 2030% of the variance in respiration
can be accounted for by the variation in one of
these more routinely measured parameters. Unfortunately, the concurrent data are too sparse to probe
this unexpected result. Of the 18 individual studies where respiration and chlorophyll are reported,
in only 50% of cases is the r 2 of the relationship
between respiration and chlorophyll a greater than
0.3. These nine studies tend to be in shelf seas with
large ranges in chlorophyll (0.250 mg m3 ) and
respiration (153 mmol O2 m3 d1 ). The relationship between respiration and chlorophyll a does
not appear to depend on autotrophic community
structure, for example, within the subset of data
where less than 50% of the total chlorophyll is
attributed to cells <2 m in diameter (i.e. communities dominated by larger cells) respiration and total
chlorophyll were not correlated.
Relationships between respiration and photosynthesis
Assuming that the open ocean is essentially a closed
system (and this is debated), then respiration will
be principally fueled by photosynthetic production
of organic material. The coupling between photosynthesis and respiration will be both physiological
(in algae) but also trophic (in heterotrophs). In the
former case, the coupling may be tight and on physiological rather than ecological timescales. The ow
and recycling through the food web introduce time
lags, so that the two processes of community photosynthesis and respiration become out of phase with
one anotherthe latter trailing the former. Temporal
studies in pelagic marine ecosystems on timescales
that allow the examination of the phasing of the
two processes are few (Blight et al. 1995; Serret et al.

chap09 2004/11/8 page 158 #12

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

159

Figure 9.7 Log10 log10 plots of volumetric rates of respiration against chlorophyll a, POC, bacterial abundance, and attenuance. Respiration
rates as mmol O2 m3 d1 , chlorophyll as mg chl a m3 , bacterial abundance as 109 cell dm3 , POC as mmol C m3 , attenuance as m1 . The
tted lines are a Model 2 major reduced axis. Chlorophyll: y = 1.4x + 0.64; r2 = 0.27, n = 628; bacterial abundance: y = 0.89x + 5.4;
r 2 = 0.27, n = 205; POC:y = 0.97x 0.75; r 2 = 0.32, n = 170; and attenuance: y = 1.01x 0.72; r 2 = 0.22, n = 260.

1999; Williams 2000). In open-water situations, such

studies are hindered by advective processes, hence
mesocosms offer a more successful environment for
such work. Figure 9.8 shows the results of studies in a series of replicate 11 000 dm3 mesocosms
undertaken in a Norwegian Fjord. Figure 9.8(a)
shows the simple time series. This illustrates the
timescale of the phasing between photosynthesis and respiration. In this instance respiration
trails photosynthesis by about 4 days. Figure 9.8(b)
and (c) illustrate the swing from autotrophy to
heterotrophy. Figure 9.8(d) shows the instantaneous
relationship between photosynthesis and respiration. Two lines are tted to the dataan ordinary
least squares (OLS) and major reduced axis (MRA)
regression. Both lines have slopes less than unity and
this reects the smaller variance in the respiration
dataset as compared with concurrent measurements
of photosynthesis. This almost certainly arises as a
consequence of time delays stemming from the ow
of organic production through the various trophic
groups, thus dampening the uctuations seen in

primary production (see Aristegu and Harrison

2002). The system being intermittently charged up
by pulses of photosynthesis and discharged by a
continuous leakage of organic material to respiration (Williams 1995). These concepts are useful in
the interpretation of open eld data.
The dataset of respiration, when compared to that
of 14 C-determined photosynthesis is small, about
1% of the photosynthetic observations (Williams and
del Giorgio, Chapter 1). An obvious solution to this
problem is to seek for relationships between respiration and photosynthesis. If such relationships
can be found, then basin wide estimates of respiration could be derived from the massive database
of photosynthesis, and potentially from models of
photosynthesis.
In Fig. 9.9 we compare the frequency distributions of eld observations of photosynthesis and
respiration from our database. In the case of the
volumetric rates, the respiration rates have a narrower distribution than the photosynthetic rates
consistent with the capacitance effect of the food

chap09 2004/11/8 page 159 #13

160

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

Figure 9.8 Analysis of time series of photosynthesis and respiration followed over 8 days in a series of 11 m3 mesocosms. (a) Time-series
plot of photosynthetic rate (open circles) and respiration (lled circles), (b) phase plots of photosynthesis and respiration, (c) time development of
P/R ratio, and (d) log10 log10 plots of photosynthesis and respiration. The dotted line shows an OLS t, the dashed line an MRA t and the solid
is the P = R line.

web on respiration. The frequency distribution of

the depth-integrated rates of respiration is skewed
at the upper enda product of a small number
(56 proles) of very high respiration values. For
this reason we have worked with log-normalized
rates, as most of the line-tting procedures we use
require a normal distribution of values within the
dataset.
The rst attempt to analyze a wide range of
environments for the relationship between photosynthesis and respiration was made by del Giorgio
et al.(1997). They found that respiration was scaled
to photosynthesis with an exponent less than unity.
Duarte and Agusti (1998) using a larger dataset

(280 observations) conrmed the ndings of del

Giorgio et al. They found that community respiration was scaled as the approximate two-thirds
power of photosynthesis, the correlation between
the two parameters was high (r 2 = 0.42). The
slope of the loglog relationship for the open ocean
was somewhat lower (0.5). We have repeated this
analysis (see Fig. 9.10) on the larger database now
available to us (957 paired observations of volumetric rates of oxygen ux derived gross production
and respiration). The correlation is much the same
(r 2 = 0.43), but the slope is reduced to 0.4, this
is most likely due to the addition of datasets from
coastal regions and low latitudes (Holligan et al.

chap09 2004/11/8 page 160 #14

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

1
Photosynthesis
Respiration
0.75

0.5

0.25

46 to 100

22 to 46

10 to 22

4.6 to 10

2.2 to 4.6

1 to 2.2

0.46 to 1

0.22 to 0.46

0.1 to 0.22

0.046 to 0.1

0.022 to 0.046

0.01 to 0.022

0
0.0046 to 0.01

Frequency (normalized to largest occurrence)

(a)

Rate (as mmol m-3 d-1)

(b)
1
Respiration
0.75

0.5

0.25

1000 to 2150

464 to 1000

215 to 464

100 to 215

46 to 100

22 to 46

0
10 to 22

Frequency (normalized to largest occurrence)

Photosynthesis

Rate (as mmol m-2 d-1)

Figure 9.9 Frequency distribution of photosynthetic and respiration rates. The data has been sorted into three bins per decade and
are normalized to the largest sample. Frequency distributions of (a) volumetric rates and (b) depth-integrated rates are shown.

chap09 2004/11/8 page 161 #15

161

162

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

Figure 9.10 Log10 log10 plot of volumetric respiration and photosynthesis. Rates as mmol m3 d1 . The dotted line shows an OLS t
(y = 0.412x + 0.1), the dashed line an MRA t (y = 0.62x + 0.04), and the solid is the P = R line. The R2 of the log-normalized data
was 0.44.

1984; Arstegui et al. 1996; Robinson et al. 1999;

Robinson unpublished data) where low P /R ratios
have been recorded. The variance of photosynthesis (expressed as the standard deviation) is greater
than respiration (0.72 versus 0.42), which is the basis
of the low slope. Both del Giorgio et al. (1997) and
Duarte and Agusti (1998) noted that at low photosynthetic rates, the rates of respiration exceeded
those of photosynthesis. Based on their derived
relationship between photosynthesis and respiration, and the estimated primary production in each
biogeochemical province in the ocean, Duarte and
Agusti (1998) concluded that 80% of the oceans
surface are expected to be heterotrophic. . ., supported by a net autotrophy in the remaining 20% of
the ocean. This was a controversial conclusion. The
two matters of contention were the timescale of the
net heterotrophy (whether permanent or transient)
and the supply mechanism of the carbon required to
support the net heterotrophy.
With volumetric rates one encounters a separation of photosynthesis and respiration, in time (as
illustrated in Fig. 9.8) but also in space (depth).
This complicates the elucidation of the ecological

relationship between photosynthesis and respiration. Williams (1998) suggested that the depthintegrated rates would overcome the second of these
two effects. The penalty is a vefold reduction in
the number of paired photosynthesis and respiration
observations from 957 volumetric rates to about 200
depth-integrated rates. The depth-integrated rates
are analyzed in Fig. 9.11.
There are important differences between the relationships between photosynthesis and respiration in
the volumetric and depth-integrated datasets. The
principal difference is that in the log normalized
plots, most (72%) of the correlation between photosynthesis and respiration seen in the volumetric
rates is lost in the depth-integrated rates. The reason for such a major loss in correlation is not wholly
clear and critical in understanding its signicance.
It could be that the main basis of the relatively high
correlation in the volumetric plots came from internal correlation in individual proleswere this the
case, then the relationships obtained from analyses of volumetric plots would have little capability
to predict regional differences. A further reason
could be sampling bias, either with respect to depth

chap09 2004/11/8 page 162 #16

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

163

Figure 9.11 Log10 log10 plot of depth-integrated respiration and photosynthesis. Rates as mmol m2 d1 . The dotted line shows an OLS t
(y = 0.26x + 1.5), the dashed line an MRA t (R = 1.0x + 0.01), and the solid is the P = R line. The R2 of the log-normalized data
was 0.07.

(Fig. 9.4), or community structure (Fig. 9.6) as proposed by Serret et al. (2001). Due to the different
depth distributions of photosynthesis and respiration, the disparity between the variances in the
photosynthetic and respiration rates, seen in the volumetric plots is lost in the depth-integrated plots
(standard deviation respiration = 0.34; standard
deviation photosynthesis = 0.33). This implies that
most of the nonlinear scaling between volumetric
rates of photosynthesis and respiration comes from
the differences in the depth distribution of these two
properties.
The low correlation (r 2 = 0.13) between depthintegrated photosynthesis and respiration, suggests
that areal photosynthesis is a weak predictor of areal
respiration. In many respects it is a disappointing
result but was the prediction of Williams and Bowers
(1999) and the conclusion of Serret et al. (2001, 2002).
The conclusion does not sit comfortably with the
proposition, at the beginning of the section, that
respiration is principally fueled by autochthonous
photosynthesis. This may be due to a number of
factors: for example, the systems are not closed, or
there are temporal offsets between respiration and
photosynthesis.

The argument has been made (e.g. Duarte and

Agusti 1998; Serret et al. 2002) that there are
differences between the balance of photosynthesis and respiration in different biogeochemical
zones, thus simply working from global averages
is inappropriate. Longhurst (1998) identied 55 biogeochemical zones in the oceans, these would represent the most logical framework into which to bin
the present data, however with only 200 depthintegrated observations this degree of resolution is
presently far too ne. As an alternative, in order to
attempt an analysis, we have grouped the data in
10 of latitude, this gives 17 bins. Even with such
a coarse separation the distribution is exceedingly
patchy and does not in any way match the areas
of ocean within each latitudinal band (Fig. 9.12).
The Pacic and the Indian oceans are particularly
poorly sampled with no measurements south of
10 N and above 30 N. Most of the measurements
lie between 2050 N in the Atlantic. In the Atlantic
the estimates for the latitudes greater than 20 N
show some degree of consistency (see Fig. 9.13), with
photosynthesis around 120 mmol O2 m2 d1 and
respiration close to 95 mmol O2 m2 d1 . When the
variance in the dataset is considered the difference

chap09 2004/11/8 page 163 #17

164

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

Figure 9.12 Comparison of the latitudinal distribution of depth-integrated rates of community respiration in the Atlantic and other oceans.
The data is divided into Atlantic and non-Atlantic Ocean and presented alongside the area (as 1012 m2 ) of each of the latitudinal bands
of ocean.

of +25 mmol O2 m2 d1 between photosynthesis

and respiration is just signicant. The rates reported
for the latitudes between 20 N and 20 S are higher
(photosynthesis 168 mmol O2 m2 d1 ; respiration
230 mmol O2 m2 d1 ), the number of samples is
however low and the variance considerable, leaving
the difference (62 mmol O2 m2 d1 ) of borderline signicance.
Whereas the differences between respiration and
photosynthesis within the current dataset may be on
the edge of signicance, the pattern of negative net
community production on the eastern periphery of
the North Atlantic Gyre is a repeated observation
(Duarte and Agusti 1998; Duarte et al. 2001; Robinson et al. 2002a; Serret et al. 2001, 2002) and in contradiction with geochemical studies of biogenic (O2
and CO2 ) gas exchange (Jenkins and Goldman 1985;
Keeling and Shertz 1992; Emerson et al. 1997, 2002).
Several suggestions have been made to account for
this anomaly, none of which have as yet been fully
proved or refuted. Sampling methodologies could
be underestimating gross production, second the
area could be fueled by a carbon source from distant previously net productive areas, nally local
temporal separation of photosynthesis from respiration could alias the results. The second explanation
was put forward by Harrison et al. (2001) to account

for the net heterotrophic areas in the eastern subtropical Atlantic where they argued that the subsidy
was derived from laments advecting offshore from
productive areas.
There are very few seasonal studies in low
productivity areas where net heterotrophy has
been reportedhence one could be observing a net
heterotrophic phase following an unobserved net
autotrophic one (Serret et al. 1999). This has recently
been remedied with a 13-month study at the HOT
site (station ALOHA at 22 45
N and 158 00
W) in
the subtropical Pacic gyre (Williams et al. 2004). The
annual totals (photosynthesis 22 mol O2 m2 a1 ;
respiration 31 mol O2 m2 a1 ) give a decit of
9 1.6 mol O2 m2 a1 , which is signicant and
begs an explanation. In this case the proposition of
allochthonous carbon sources is not compelling, as
the areas in question are physically isolated. The
gradients of dissolved organic carbon have been
measured and they are in the opposite direction
(Abell et al. 2000). The scale of the difference and
the lack of any period of protracted seasonal accumulation of organic material exclude long term out
of phase relationships between photosynthesis and
respiration. The explanation favored by Williams
et al. (2004) is based on intermittency of photosynthesis; the argument (Karl et al. 2003) being that there

chap09 2004/11/8 page 164 #18

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

165

a) Latitudinal Averages
500

GP Latitudinal Average
Resp Latitudinal Average
NCP Latitudinal Average

Mean rate (as mmol O2 m2 d1)

400
300
200
100
0

100

8090N

7080N

6070N

5060N

4050N

3040N

2030N

010N

1020N

010S

1020S

2030S

3040S

4050S

5060S

6070S

300

7080S

200

b) Latitudinal Totals
5
GP Latitudinal Average
Resp Latitudinal Average
NCP Latitudinal Average

Total rate (as 1015 mol O2 a1)

4
3
2
1
0
1
2

8090N

7080N

6070N

5060N

4050N

3040N

2030N

1020N

010N

010S

1020S

2030S

3040S

4050S

5060S

6070S

7080S

Figure 9.13 Comparison of the latitudinal distribution of depth-integrated rates of community respiration, net community production, and
gross production. (a) the geometric means for 10 latitude bands, the error bars represent the standard error for each band; (b) the total rates
for each latitude band where data exists, calculated from the data in Fig. 9.12(a) and the oceanic area for each latitude band. The production
values are concurrent O2 -derived rates of gross and net community production.

are short intensive bursts of photosynthesis, which

charge up the organic reservoir, which is then slowly
and steadily discharged by respiration. The evidence for this comes from long-term continuous in situ
observations of dissolved oxygen in the euphotic
zone, which show periods of rapid accumulation
of biologically produced oxygen. The explanation

has an interesting and provocative corollary

that because of its better integrating properties,
respiration may be a superior determinant of timeintegrated production than the measurement of
photosynthesis itself. Whereas these explanations
are the best we can currently offer; one inevitably
asks why our sampling protocols have persistently

chap09 2004/11/8 page 165 #19

166

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

missed these pulses and always made measurements during the periods of decit. Without doubt
we have much to learn about these systems and a
great deal more work to do before we can expect an
understanding of how they function.

9.4 Distribution of respiration within

the planktonic community
When we consider the distribution of respiration
within the community, we implicitly address two
quite separate questions. The rst is the distribution of respiration between the autotrophic and
the heterotrophic communities; autotrophic respiration being that part of gross primary production
(photosynthesis) not available to the rest of the community. The second question is the distribution of
respiration within the heterotrophic component of
the planktonthis provides insight into ecosystem
functioning.
As there is no accepted procedure for blocking the
metabolism of different sectors of the plankton with
selective inhibitors, alternative ways of apportioning respiration within the planktonic community
have had to be devised. They fall into ve categories:
1. Calculations of the distribution of respiration
from either observations of biomass or from algorithms of biomass distribution.
2. Measurements of the size distribution of respiration from which the respiration of organism groups
may be inferred.
3. Derivation of respiration rates from measured
or estimated rates of production, and growth
efciencies.
4. Determination of algal respiration as the difference between gross production and 14 C derived net
primary production.
5. Derivation of respiration rates for various trophic
groups from plankton food web models.

9.4.1

Calculations from biomass

Calculations from observations of biomass

Whereas there are a number of datasets for the
biomass of particular plankton groups there are
few comprehensive studiesin part due to the

time and skill required to make a full analysis of

biomass. No study, to our knowledge, contains
estimates for all the major components of the food
web (bacteria, protozoa, algae, and larval and adult
zooplankton), so the apportionment of the relative
contribution to metabolism will be incomplete.
Clearly, if a class is omitted, then the contribution
of the groups reported will be overestimated. The
problem of ascribing rates to groups across the full
size spectrum of the plankton is nontrivial. It is
tempting to search for universal allometric relationships. In the case of the algae it seems possible to
constrain biomass-related respiration reasonably
well (Langdon 1993). Metazoa and protozoa would
appear to have a sufciently stable respiratory
metabolism that a single allometric equation may
be acceptable (see Fenchel, Chapter 4, Section 4.3),
however one runs into major difculties with the
bacteria.
Table 9.2 contains a summary of reported calculations of respiration for various trophic groupings,
expressed as a percentage of the sum of the reported
rates. By far the most comprehensive study was
that of Williams (1982) who used the data from the
CEPEX study. This comprised data on bacteria, 3
categories of protozoa, 9 categories of algae, and
some 44 categories of zooplankton, spanning the
adults and all the larval stages. These observations
were made on a large (1300 m3 ) mesocosm at 2- or
3-day intervals over a 2-month period. The data in
the table show broad agreement between the various estimates of the contribution of different trophic
groups to overall respiration, with bacteria comprising 1258%, the protozoa a further 1136%, the algae
870%, and the larvae and adult zooplankton 39%.
The CEPEX dataset analyzed by Williams was sufciently extensive (it spanned 3 12 orders of magnitude in the size of the organisms studied) that a size
distribution of metabolism could be constructed.
This is shown in Fig. 9.14, along with projections of
respiration made from generalizations of biomass
distribution. In its broad features it accords very
well with observations of size-fractionated respiration and the projections from theoretical biomass
proles, the main discrepancy being in the 13 m
size range. No organisms of that size were logged
in the CEPEX study, probably not because they

chap09 2004/11/8 page 166 #20

chap09 2004/11/8 page 167 #21

35

26

22

51

32

58(18a )

36

11

13

12

18

21

13

36

11

26

16

24

28

35

35

51

15
20

1.4

11

11

12

Not included in estimate

83

Protozoa

Phytoplankton

Zooplankton

22

12

69

7.8

40

6.2

27

28

34

21

12

13

69

7.8

40

Not inlcuded in estimate

4.2

Not include in estimate

Not included in estimate

9.4

Nanoagellates Heterotrophs dinos. Ciliates Total Pico Nano Micro Total Larval Adults Others Total

52

a Two calculation methods for bacterial respiration.

Outcome from plankton models

Fasham et al. (1999) (inverse Northeast
model)
Atlantic
Nagata (2000) (plankton ow Oligotrophic
model)
ocean

Summary statistics
Arithmetic mean of all
observations
Standard deviation of all
observations
Total number of observations

Calculation from biomass determinations

Williams (1981) (n = 3;
Mesocosm
geometric mean)
(Canada)
Holligan et al. (1984)
English
Channel
Robinson et al. (1999)
East Antarctic
(n = 7; geometric mean)
Robinson and Williams (1999) Arabian Sea
(n = 6; geometric mean)
Sondegaard et al. (2000)
Mesocosm
(n = 3; geometric mean)
(Norway)
Robinson et al. (2002b)
North Sea
(n = 6, 8; geometric mean)

Total

Bacteria

Table 9.2 Estimates of the contribution of various groupings to community respiration

168

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

Cumulative respiration and biomass (as %)

Bacteria

Phytoplankton and Protozoa

Mesozooplankton

100

75

50

Integrated respiration - Model A

Integrated metabolism - Model B
Cumulative respiration
Cumulative biomass
Size fractionated respiration

25

0
0

10

100

1,000

Size (in microns)

were absent but that the skills were not available

to recognize and enumerate them.
There is one caution with the data derived from
eld observations generally. As discussed earlier the
sampling in many cases is biased to the productive
part of the plankton cycle, this would put a bias to
the data toward high algal contributions to overall
community respiration.

Calculations from generalized biomass proles

Generalized continuous biomass proles of the
plankton have been derived from eld observations
(Sheldon et al. 1972) and from theory based on an
idealized food chain (Platt and Denman 1978). Both
of these studies were evolved prior to the modern
understanding of the microbial food web however,
it would appear that they give a fair account of the
modern view of the size of microbial biomass and
metabolism.
Sheldon et al. (1972) concluded that the biomass
prole was at within logarithmic size classes. Platt
and Denman (1978) found a decreasing biomass
with increasing size, the slope being 0.22 (the
broad structure of Platt and Denmans derivation
is given in Box 9.1). These biomass/size distributions can be combined with equations of respiration
versus size to produce size distributions of respiration. In general they show the same features, the
size classes below 10 m account for more than
95% of the respiration; the size classes from 30 to
10 000 m accounting for less than 1% of the total.
A similar analysis was made by Platt et al. (1984)

10,000

Figure 9.14 Size distribution of observed biomass and

calculated and observed cumulative respiration. Integrated
metabolism, Model A based on Platt and Denman (1977),
Model B based on Sheldon et al. (1972). See Box 9.1 for basis
of calculation. Cumulative and size-fractionated respiration
and biomass taken from Williams (1982).

who also highlighted the importance of microbial

metabolism.

9.4.2 Experimental determination of the

size distribution of respiration
In lieu of selective inhibitors to block particular
sectors of the plankton, size-fractionation ltration
procedures have been used to progressively remove
components of the plankton size spectrumwith
respiration measurements being made on the various ltrates. This was used initially in studies
of the size distribution of photosynthesis and was
applied subsequently by Williams (1981) to establish the scale of bacterial respiration in relation to
the whole community. The approach has a number of limitations: it cannot, for example, resolve
between different functional groupings occupying
the same size category. They may be inferred with
a degree of certainty in the case of the extreme
end-members, that is, bacteria (<1 m) or the mesozooplankton (>100 m), as they dominate their
class sizes. Intermediate size classes will contain
both heterotrophs (mainly protozoa) and autotrophs
in variable proportions. There are also problems
with attached organisms being included in largersize classes and the increase in prey consequent
upon the removal of its predator. These cautions
must be taken as constraints when interpreting the
data. Time-series studies of size-fractionated samples and comparison of the size-fractionated respiration rates with those of the whole community can
act as indicators of the scale of the constraint. The

chap09 2004/11/8 page 168 #22

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

169

Box 9.1 Theoretical calculation of biomass and respiration size distribution

A general theory of size distribution within the plankton was
derived by Platt and Denman (1977). It divides the size spectrum into a number of logarithmically increasing steps, either
decades or octaves, and seeks to relate the biomass within
a bandwidth to weight of the size class using an equation of
the form:
bw /b0 = (w/w0 )

(1)

where:
bw is the total biomass within a bandwidth;
w is the characteristic weight of the size class;
is an allometric scaling constant; and
b0 and w0 are values for one particular size class, which
is used to x the relationship.
Assuming a unidirectional ow and Fenchels (1974)
empirical equations for the weight dependence of turnover
(w = Aw ) and respiration (Rw = Bw ), where A, B,

88

73
56

75

25
0
<5

<20

<53

w/w0 = (bw /b0 )1/0.22

(3)

w = w0 (bw /b0 )1/0.22

(4)

Equation (4) can then be embedded into an overall allometric cell mass versus respiration equation (Rw = Bw ),
such that:

Rw = B w0 (bw /b0 ) /0.22 ,

(5)

where characteristically has a value in the region of 0.3.

Several studies (Robinson and Williams, 1999;

Robinson et al. 1999, 2002a,b) have apportioned
community respiration to that attributable to
planktonic trophic groups using measured rates
of bacterial production, microzooplankton herbivory, and/or bacterivory and algal photosynthesis
together with an estimate of the respective growth
efciencies.
Bacterial respiration (BR) can be derived from
measured bacterial production (BP) if the bacterial growth efciency (BGE) can be estimated (i.e.
BR = BP(1 BGE)/BGE). If not directly measured,
bacterial growth efciency is either taken from the
range of published values, for example, 540%, or
derived from the equation (BR = 3.7 BP0.41 )
reported by del Giorgio and Cole (1998) or the temperature relationship (BGE = 0.374 0.0104 t C)
of Rivkin and Legendre (2001). Bacterial growth
efciencies estimated by these two latter equations
were found to differ by almost ninefold during a
study of a coccolithophore bloom in the North Sea
in June 1999 (Robinson et al. 2002b, also Table 9.2).
Microzooplankton respiration (ZR) can be derived

54

<2

The value for of 0.22 in equation (2) comes from the

constants A, B, and Fenchels observation that + 1
Equation (2) may be rearranged as:

100

50

<0.8

(2)

9.4.3 Derivation from rates of production

and growth efciencies

83

65

bw /b0 = (w/w0 )0.22

125

Normalized rate (as %)

Respiration: Average in
size fraction
Photosynthesis: Average
in size fraction

and are constants, one arrives at a solution for the size

distribution for biomass equation (1) as:

<200

Size fraction (m)

Figure 9.15 Rates of respiration and photosynthesis in size
fractions. The rates are normalized against that of the
unfractionated sample. Compiled from 62 sets of observations. Error
bars are the standard errors.

size distribution of respiration from several studies

(Harrison 1986; Grifth et al. 1990; Blight et al.
1995; Boyd et al. 1995; Robinson et al. 1999) is
summarized in Fig. 9.15, alongside size-fractionated
photosynthetic rates.

chap09 2004/11/8 page 169 #23

170

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

from an estimate of herbivory, assuming a constant growth efciency of 25% (Straile 1997) and
an egestion + excretion rate of 20% (Robinson et al.
2002b). Algal respiration (AR) can be derived from
the Rmax : Pmax relationship of Langdon (1993) for
the dominant autotroph present, that is, 0.16 0.04
for Prymnesiophyceae and 0.35 0.17 for Dinophyceae, where Pmax is estimated from 14 C primary
production or dissolved oxygen gross production
measurements.
Given that one can estimate the rates for these various groups, overall community respiration should
be equivalent to their sum (BR + ZR + AR). In
the studies where this type of accounting exercise
has been attempted (Robinson and Williams 1999;
Robinson et al. 1999, 2002a,b), the sum of the estimates of respiration attributable to the component
plankton groups lie within 50% of the measured
whole community respiration. This is probably as
good as can be expected bearing in mind the levels of
uncertainty on accepted measures of phyto, microzoo, and bacterioplankton activity, not to mention
the four to tenfold range in measured and estimated
growth efciencies.

9.4.4 Estimates from 14 C determination of

net primary production
Since net primary production (NPP) is equivalent
to gross production (GP) minus algal respiration
(NPP[C] = GP[C] AR[C]), if one can assume that
the 14 C technique measures net primary production,
that gross production may be derived from oxygen
ux (GP[O2 ]) and that it can be reliably converted
to carbon ux GP[C] via a photosynthetic quotient
(PQ), then algal respiration can be determined from
the difference between GP[O2 ]/PQ and 14 C uptake.
Heterotrophic respiration (HR[C]) could then be
determined from the difference between measured
total community respiration in carbon units (R[C])
and this estimated algal respiration (AR[C]). The
approach has not gained much popularity due to
the uncertainty over whether or not, and when, the
14 C measures gross or net production, as well as the
lesser problem of ascribing a value for the photosynthetic quotient however see Marra and Barber
(2004).

9.4.5

Inverse analysis

As described in Section 9.2.5 above, several authors

have used equations and models of carbon ow
through the microbial food web to estimate the respiration attributable to a particular plankton group,
for example, bacteria or size class, for example,
<5 m (Fasham et al. 1999; Ducklow et al. 2000;
Anderson and Ducklow 2001). Fasham et al. 1999
used a size structured ecosystem model forced with
data collected during a 20 day spring bloom study
in the NE Atlantic to conclude that 62% of the community respiration came from organisms <5 m in
size. The data extracted from this model are given
in Table 9.2, along with that from a model of the
food web of an oligotrophic oceanic region derived
by Nagata (2000).

9.4.6

Summary

In Fig. 9.16, we have attempted to collate the results

from these various approaches to the determination
of the size distribution of respiration. Considering
the scope for variation and error, the general pattern is remarkably consistent. All the approaches
attribute a major proportion (70% or more) of respiration to the smaller-size classes: 42 10% to
organisms less than 1 m (the size class where bacterial biomass usually dominates), 32 20% to the
size class 110 m (bacteria, protozoans, and phytoplankton). Much smaller proportions are found for
the two larger-size classes: 6 5% to the class
10100 m (the larger phytoplankton and protozoan
ciliates) and the largest-size class (1001000 m
the larval and adult mesozooplankton) accounting
for 10 8.5%. Of course one should not expect a
xed pattern, as the composition of the plankton
varies in space and with time.

9.5

Synthesis and conclusions

Respiration is one of the two determinants of the

balance of organic material in the euphotic zone and
the potential to export organic material to the deep
ocean. As such it is a major inuence on the scale
of the biological pumpwhich sequesters carbon
dioxide from the atmosphere.

chap09 2004/11/8 page 170 #24

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

Larval & Adult

Zoopl.

Phytoplankton & Protozoa

75

Unresolved
Autotrophs
Heterotrophs

50

25
40

20

9.5.1 Estimation of global rates of respiration

from direct eld observations
The light/dark bottle incubation technique is the
primary method for measuring respiration. It is not
without its errors and limitations, however it is without doubt in our minds as good, if not better, than
other methods of measuring plankton metabolism.
Acquiring appropriate sized datasets is massively
costly in ship and human time. Nonetheless, since
the late 1960s we have had reasonably good maps
of oceanic photosynthesis based on in vitro observations. In the case of photosynthesis the problem
is greatly simplied in that one can use measurements of light, chlorophyll and photosynthetic
irradiance relationships to ll in the gaps. Satellite
derived ocean color has rendered this as a powerful approach. No analogous approach is available
for respiration. The present database of respiration
is woefully inadequatea mere 693 surface measurements covering an area of 320 106 km2 . The
ideal minimum would be seasonal descriptions of
depth-integrated respiration for the 55 biogeochemical zones described by Longhurst (1998). Figure 9.2
makes it clear that we are a long way away from

Geometric mean 100<1000

Biomass Models 100<1000

Food web Models 100<1000

Biomass Calc 100<1000

Size fractionation 100<1000

Geometric mean 10<100

Biomass Models 10<100

Food web Models 10<100

Biomass Calc 10<100

Size fractionation 10<100

Geometric mean 1<10

Biomass Models 1<10

Food web Models 1<10

Biomass Calc 1<10

Size fractionation 1<10

Geometric mean <1

Biomass Models <1

Food web Models <1

Biomass Calc <1

Size fractionation <1

Percentage Contribution of Trophic Group

Bacteria
Bacteria

171

Figure 9.16 Summary of size distribution

observations. The various analyses are grouped into
categories <1 m, 110 m, 10100 m, and
1001 000 m. Where a distinction was made in the
analyses between autotrophs and heterotrophs, this
distinction has been retained, otherwise they are
grouped as unresolved.

achieving this aim; a crude separation by 10 of latitude still leaves a number of the latitude bands with
no or very little data. This is frustrating as it leaves
us uncertain whether or not the trends of respiration
and net community production we see with latitude in Fig 9.13 are real or simply reect inadequate
sampling.
The respiration data are biased with respect to
time, place, community structure, and depth, and
so cannot provide a denitive global estimate of
plankton respiration. However, they can be used
to derive a maximum and minimum gure for
global ocean photic zone respiration, which can then
be compared with estimates derived from massbalance equations. Summing the latitudinal totals
of depth-integrated respiration given in Fig. 9.13(b)
gives a global (oceanic + coastal) respiration rate
of 17.2 Pmol O2 a1 (186 Gt C a1 , using a respiratory quotient of 0.89, see Chapter 14). The mean
depth-integrated respiration rate in oceanic waters
of 116 8.5 mmol O2 m2 d1 equates to a global
oceanic respiration rate of 13.5 1 Pmol O2 a1
(146 12 Gt C a1 ). These are undoubtedly maximum values given the bias in sampling toward
times and places of high productivity. The lowest values recorded in the database occur in the

chap09 2004/11/8 page 171 #25

172

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

Southern Ocean (e.g. Bender et al. 2000) and during the autumn and winter (e.g. Serret et al. 1999)
and give a lower limit to the estimate of oceanic
respiration (35 mmol O2 m2 d1 ; 4.1 Pmol O2 a1 ;
44 Gt C a1 ). It is worth noting that the lowest estimate which could be derived from the dark oxygen
incubation technique is 10 mmol O2 m2 d1 or
1.2 Pmol O2 a1 (13 Gt C a1 ) (based on a rate of
0.2 mmol O2 m3 d1 and a 50 m euphotic zone)
and so this lower dataset value is not simply a consequence of the limit of detection of the method.
The 13-month study at HOTS provides a crucial
seasonally integrated estimate of respiration in an
area representative of the open-ocean gyres. The
HOTS estimate (31 mol O2 m2 a1 ) would extrapolate to a global ocean estimate of 9.9 Pmol O2 a1
(119 Gt C a1 ). Open-ocean primary production
estimates, derived from 14 C measurements lie in
the range 2.34.3 Pmol C a1 (2852 Gt C a1 , del
Giorgio and Duarte 2002). Comparisons between
14 C and gross production derived from dissolved
oxygen ux suggest that 14 C underestimates gross
production by 3565% (Bender et al. 1999; Robinson
and Williams 1999; Laws et al. 2000; Rees et al. 2002).
Correcting the open-ocean production estimates by
a mean of 50% gives a range of 59 Pmol C a1 (see
also Chapter 14). Comparison with the range in respiration estimates (417 Pmol C a1 ) could be seen
as a major imbalance in the functioning of the oceans
but more likely arises from a lack of our understanding in the seasonal and regional variations in
photosynthesis and respiration.

9.5.2 Derivation of global rates from

correlation analysis
Recognizing the limitations in the current database
of respiration, several authors have attempted to
derive simple relationships between respiration and
indicators of plankton biomass (Robinson et al.
2002a,b) or photosynthesis (del Giorgio et al. 1997;
Duarte and Agusti 1998; Serret et al. 2001). The
analysis we have made in the present chapter (Section 8.3.2) on an enlarged database is not encouraging in this respect. Only 2030% of the variance
in respiration can be accounted for by the variation in routinely measured indicators of plankton

biomass. The low correlation between respiration

and photosynthesis precludes the use of this simple
property relationship to make useful global predictions of respirationconsistent with the arguments
of Williams and Bowers (1999) and Serret et al. (2001,
2002). As the major source of carbon for oceanic
respiration comes from oceanic photosynthesis (see
Box 9.2) there has to be some form of relationship,
although clearly it is not a simple one.

9.5.3 Derivation of rates from ocean

organic mass-balance calculations
Simple mass-balance calculations enable us to
derive a fairly precise estimate of the difference
between production and consumption and so in
principle provide a constraint to the global estimates
of respiration derived from direct measurements.
The strength of the mass-balance calculation is that
the assumptions are clear and the implication of differing assumptions easy to explore. Their limitation
is that they cannot give an independent estimate
of both photosynthesis and respiration. The calculation also implicitly assumes steady state over
the medium term (10100 years). This assumption
appears to be justiable as the size of the principal
organic reservoir in the upper water column (about
58 mol DOC m2 ) is about a third or less than that
of the annual biological turnover of carbon. Thus if
there were persistent imbalances in the upper water
column carbon cycle, major changes in the carbon
reservoirs would result. We have reasonably reliable observations of DOC concentrations that span
45 years and can be fairly certain that major changes
in the DOC pool have not occurred. As estimates
of the external organic inputs into the ocean (predominantly river-borne material) exceed those of the
outputs (predominantly sedimentation), the ocean
as a whole must be net heterotrophic, albeit only
very slightly (0.4%, see Box 9.2). This was essentially
the argument of Smith and Mackenzie (1987). The
difference between production and consumption is
small, in relation to the individual processes themselves. Any estimate we obtain for respiration from
mass-balance calculations is primarily dependent
upon the value we take for oceanic primary production, so in a way we cycle back to the problem

chap09 2004/11/8 page 172 #26

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

Box 9.2

173

Mass-balance calculations for respiration in the whole oceanic water column

The basic mass-balance equation assumes that as there is no

accumulation of organic material, the sum of all the inputs
must equal that of all the outputs:
that is, P +




I R + O = 0,

where:
P is the annual rate of photosynthesis;
R

is the annual rate of respiration;

I is the sum of the external inputs;
O is the sum of the external outputs from the oceanic
water column.
The calculation considers annual sums of all the individual
sources and sinks, the units are Tmol C a1 .

of the uncertainties inherent in this latter estimate.

However the one thing we can be certain of from
the mass-balance calculation is that there cannot
be the massive difference between oceanic production and respiration we derive from analysis of eld
observations.
Whereas the mass-balance approach is a useful
technique on the large scale, it quickly runs into
severe limitations when it is attempted for subdivisions of the ocean. In Box 9.3, the calculation
is repeated with the simple division of the oceans
into the coastal- and the open-ocean zones. The
export of organic carbon from the coastal to the
open ocean has been part of a major international
program (LOICZLandOcean Interactions in the
Costal Zone). The overall spread of values for the
total export from the coastal to the open ocean is
large but we seem to be approaching some consensus in the estimates. Liu et al. (2000b) reported
a range from 17 to 390 Tmol C a1 . They regard
70 Tmol C a1 to be a representative value. Ducklow
and McCallister (in press) adopt a higher gure
of 200 Tmol C a1 . These two estimates (70 and
200 Tmol C a1 ) probably bracket the likely range
and have been used in Box 9.3 to calculate maximum and minimum scenarios. In both situations
the open-ocean water column is calculated to be net

The individual inputs (see Williams 2000) are:

IR = river input of organic material = 34 Tmol C a1 ;
IA = atmospheric deposition of organic material =
2 Tmol C a1 .
The individual outputs (see Williams 2000) are:
OS = net sedimentation = 14 Tmol C a1 ;
OA = input of organic material into the atmosphere =
2 Tmol C a1 .
Then, P + 36 (R + 16) = 0, thus R = P + 20.
If we take 5500 Tmol C a1 as an estimate of whole ocean
gross production (see Box 9.3), then R = 5500 + 20 =
5520 Tmol C a1 and P/R = 0.996.
Trophic balance = 0.4% heterotrophic.

heterotrophic, weakly so (1.7%) in the low export

case, more signicantly so (5%) in the high export
case. The higher gure for carbon export to the
open ocean calls for a strongly (13% ) autotrophic
coastal ocean, the lower export gure, a weakly (3%)
autotrophic one.
As the focus of this chapter is the epipelagic zone,
we have made mass-balance calculations for this
zone. It is regarded (Liu et al. 2000a; Ducklow
and McCallister in press) that the export of organic
material from the coastal ocean occurs down the
continental slope and thus enters the mesopelagic,
rather than the epipelagic zone. This leaves the
budget for the epipelagic dominated by a single
import/export term: the transfer of material to the
mesopelagic zone. Recent estimates for the export
to the mesopelagic are 667 Tmol C a1 (Liu et al.
2000b), 782 Tmol C a1 (Ducklow and McCallister,
in press), 1700 Tmol C a1 (Arstegui, Chapter 10)
and 2292 Tmol C a1 (del Giorgio and Duarte 2002).
In Box 9.4 we have calculated a budget for the
epipelagic zone using the two extremes, as well
as an intermediate gure of 1000 Tmol C a1 . The
broad pattern is the sameit requires the epipelagic
ocean to be distinctly (1657%) net autotrophic.
The difference between photosynthesis and respiration in the epipelagic (euphotic) zone is set by the

chap09 2004/11/8 page 173 #27

174

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

Box 9.3

Mass-balance calculations for respiration in the coastal and open ocean

water columns

Separate calculations are made for coastal (area = 0.36 1014 m2 ) and oceanic (area = 3.2 1014 m2 ) zones. The
sedimentation rates for the coastal and open ocean zones are taken as 12 and 2 Tmol C a1 , respectively (see Box 9.2).
The output to atmosphere (OA = 2 Tmol C a1 , see Box 9.2) is divided pro rata by area between the coastal and open
ocean giving, respectively, 0.2 and 1.8 Tmol C a1 . The input from the atmosphere (IA = 2 Tmol C a1 , see Box 9.2) has
been apportioned assuming twice the fallout rate in the coastal zone giving 0.36 and 1.64 Tmol C a1 , respectively for the
coastal and open ocean zones. Neither of these last two estimates is critical in the calculation. Estimates for the productivity
of the coastal ocean vary three to fourfold: Liu et al. (2000b) gives a range of 340750 Tmol C a1 . We adopt Ducklow
and McCallisters (in press) recent estimate of 1200 Tmol C a1 for net primary production and maintain a ratio of coastal
to oceanic production similar to that of Ducklow and McCallister (in press). As we need to base the calculation on gross
production, we scale up net primary production by 25% to give gross production so obtaining a gure of 1500 Tmol C a1
for the coastal ocean and 4000 Tmol C a1 for the open ocean. The nal terms (OO and IC ), the output from the coastal
production to the open ocean and the import of organic matter produced in coastal waters, must be numerically equal. Two
situations have been calculated, a low value (70 Tmol C a1 ) for OO is taken from Liu et al. (2000b) and a high value
(200 Tmol C a1 ) from Ducklow and McCallister (in press). The calculations (see Box 9.2 for notation) are as follows:
Coastal ocean: mass-balance equation
P + IA + IR (R + OS + OA + OR + OO ) = 0

Open ocean: mass-balance equation

P + IA + IR + IC (R + OS + OA ) = 0

Authors vary over whether to separate organic material of planktonic and river origin in their estimates of export from the
coastal zone, it is a detail that is unnecessary in the present account and so these export/import terms have been embedded
as single values (OO and IC ). The above equations then simplify to:
Coastal ocean: mass-balance equation
P + IA + IR (R + OS + OA + OO ) = 0

Open ocean: mass-balance equation

P + IA + IC (R + OS + OA ) = 0

Coastal ocean: high export calculation

P + 0.36 + 34 (R + 12 + 0.2 + 200) = 0
Thus, R = P 178 Tmol C a1 .
Assume, P = 1500 Tmol C a1 .
Then R = 1322 Tmol C a1 , and P/R = 1.13.
Coastal ocean would be 12% autotrophic.

Open ocean: high export calculation

P + 1.6 + 200 (R + 2 + 1.8) = 0
Thus, R = P + 198 Tmol C a1 .
Assume, P = 4000 Tmol C a1 .
Then R = 4198 Tmol C a1 and P/R = 0.95.
Open ocean would be 5% heterotrophic.

Coastal ocean: low export calculation

P + 0.36 + 34 (R + 12 + 0.2 + 70) = 0
Thus, R = P 48 Tmol C a1 .
Then R = 1452 Tmol C a1 and P/R = 1.03.
Coastal ocean would be 3% autotrophic.

Open ocean: low export calculation

P + 1.6 + 70 (R + 2 + 1.8) = 0
Thus, R = P + 68 Tmol C a1 .
Then, R = 4068 Tmol C a1 , and P/R = 0.98.
Open ocean would be 1.7% heterotrophic.

chap09 2004/11/8 page 174 #28

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

Box 9.4

175

Mass-balance calculation for the open ocean epipelagic zone

The prevailing view is that the exported planktonic production from the coastal regions enters the mesopelagic, rather
than the epipelagic zone of the open ocean (see Liu et al.,
2000a; Arstegui et al., Chapter 10). We make calculations
for the epipelagic (0150 m) zone of the ocean, assuming that coastal production is exported to the mesopelagic
zones. We may expect that the material of river origin passes
into both zones, however as will be seen below whatever
assumption we make of its fate is of little consequence in
the overall calculation.
Mass-balance equation,
P + IA + IR + IC (R + OM + OA ) = 0,
where OM is the export from the epipelagic into the
mesopelagic zone.
As OM >> (OA + IA + IR + IC ), the equation simplies
to:
P (R + OM ) = 0.
Recent estimates for the export to the mesopelagic (OM ) are
667 Tmol C a1 (Liu et al. 2000a), 782 Tmol C a1 (Ducklow and McCallister in press), 1700 Tmol C a1 (Arstegui

export term, which is reasonably well constrained;

if anything it may be an underestimate thus requiring even higher levels of net autotrophy. Whereas
the difference between photosynthesis and respiration is determined by a single term, the absolute values are dependent upon the value taken
for oceanic photosynthesis. del Giorgio and Duarte
(2002) in their review adopted a twofold spread of
valuestheir upper gure for the ocean as a whole
(6400 Tmol C a1 ) is somewhat higher than the one
we have used and it would reduce the calculated
relative net autotrophy to a range of 1449%.
Signicantly, the range of epipelagic zone oceanic
respiration rates derived from mass-balance considerations (1.73 Pmol C a1 ) lie below even the
lowest estimate of oceanic respiration derived from
direct measurements, and are two to eightfold
lower than the mid- and highest estimates derived
from direct measurements. This does not derive
from an error in the mass-balance calculation, but

et al., Chapter 10) and 2292 Tmol C a1 (del Giorgio and

Duarte 2002). Here we make the calculation for the extremes
of the estimate of OM (667 and 2292 Tmol C a1 ), and what
would seem be a median value of 1000 Tmol C a1 .
Epipelagic ocean: low export calculation
R = P 667 Tmol C a1 .
Then R = 3333 Tmol C a1 ,
and P/R = 1.2.
Epipelagic ocean: would need to be 16% autotrophic.
Epipelagic ocean: high export calculation
R = P 2292 Tmol C a1 .
Then R = 1708 Tmol C a1 ,
and P/R = 2.3.
Epipelagic ocean would need to be 57% autotrophic.
Epipelagic ocean: intermediate export calculation
R = P 1000 Tmol C a1 .
Then R = 3000 Tmol C a1 ,
and P/R = 1.33.
Epipelagic ocean would need to be 25% autotrophic.

for the need to supply a gure for the rate of

photosynthesisessentially we return to the problem brought to light in the preceding paragraph.
The prediction from mass-balance equations that the
epipelagic zone is 25% or so autotrophic is at odds
with the direct measurements that imply a balanced
or slightly heterotrophic situation. This discrepancy
will in part result from the different time and space
scales considered by the two approaches. However,
they also point to the weaknesses in our understanding of the global balance between organic carbon
production and respiration. Mass-balance equations
and direct observations indicate (del Giorgio and
Duarte 2002; Williams et al. in press) that we may
be underestimating the rate of organic matter production, by a factor of two or more. In the nal
chapter (Chapter 14) del Giorgio and Williams discuss this in more detail and achieve some resolution
of the problem. Combined with the sampling bias of
oceanic respiration measurements, our appreciation

chap09 2004/11/8 page 175 #29

176

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

of regional and global photosynthesis to respiration balances is rudimentary. If we are to predict

the oceanss response to global change, then current
and future national and international oceanographic
programs will need to incorporate the determination
of oceanic respiration and to address the question of
whether the ocean biota act as a net source or sink
of carbon as a priority research objective.

Acknowledgments
Many thanks to the following for making published
and unpublished data available: Javier Arstegui,
Natalia Gonzalez, Dominique Lefvre, Paul Morris,
and Nelson Sherry, and to Alison Fairclough at the
British Oceanographic Data Centre (BODC) for her
meticulous help in accessing the UK BOFS, PRIME,
and Arabesque data. CR was funded on a NERC
Advanced Research Fellowship (GT5/96/8/MS)
and the Plymouth Marine Laboratory Core Strategic Research Programme. Satellite data in Fig. 9.2
were processed by Gareth Mottram and Peter Miller
at the Plymouth Marine Laboratory Remote Sensing Group (www.npm.ac.uk/rsdas/). SeaWiFS data
courtesy of the NASA SeaWiFS project and Orbital
Sciences Corporation.

References
Abell, J., Emerson, S., and Renaud, P. 2000. Distributions of
TOP, TON and TOC in the North Pacic subtropical gyre:
implications for nutrient supply in the surface ocean and
remineralization in the upper thermocline. J. Mar. Res.,
58: 203222.
Anderson, T. R. and Ducklow, H. W. 2001. Microbial loop
carbon cycling in ocean environments studied using
a simple steady-state model. Aquat. Microb. Ecol., 26:
3749.
Arstegui, J. and Harrison, W. G. 2002. Decoupling of
primary production and community respiration in the
ocean: implications for regional carbon studies. Mar.
Ecol. Prog. Ser., 29: 199209.
Arstegui, J. and Montero, M. F. 1995. The relationship
between community respiration and ETS activity in the
ocean. J. Plankton Res., 17: 15631571.
Arstegui, J., Montero, M. F., Ballesteros, S.,
Basterretxea, G., and van Lenning, K. 1996. Planktonic

primary production and microbial respiration measured

by 14 C assimilation and dissolved oxygen changes in
coastal waters of the Antarctic Peninsula during the
austral summer: implications for carbon ux studies.
Mar. Ecol. Prog. Ser., 132: 191201.
Arstegui, J., Denis, M., Almunia, J., and Montero, M. F.
2002. Water-column remineralization in the Indian sector
of the Southern Ocean during early Spring. Deep-Sea Res.
II, 49: 17071720.
Barber, R. T. and Hilting, A. K. 2002. History of the study
of Plankton Productivity. In P. J. le B. Williams, D. N.
Thomas, and C. S. Reynolds (eds) Phytoplankton Productivity: Carbon Assimilation in Marine and Freshwater
Ecosystems. Blackwell Science Ltd, Oxford, UK, p. 386.
Bender, M., Grande, K., Johnson, K., Marra, J., Williams,
P. J. le B., Sieburth, J., Pilson, M., Langdon, C.,
Hitchcock, G., Orchardo, J., Hunt, C., Donaghay, P., and
Heinemann, K. 1987. A comparison of four methods for
determining planktonic community production. Limnol.
Oceanogr., 32: 10851097.
Bender, M., Orchardo, J., Dickson, M-L., Barber, R.,
and Lindley, S. 1999. In vitro O2 uxes compared
with 14 C production and other rate terms during the
JGOFS Equatorial Pacic experiment. Deep-Sea Res. I, 46:
637654.
Bender, M. L. 2000. Tracer from the sky. Science, 288: 1977
1978.
Bender, M. L., Dickson, M-L., and Orchardo, J. 2000. Net
and gross production in the Ross Sea as determined by
incubation experiments and dissolved O2 studies. DeepSea Res. II, 47: 31413158.
Blanco, J. M., Quinones, R. A., Guerrero, F., and
Rodriguez, J. 1998. The use of biomass spectra and
allometric relations to estimate respiration of plankton
communities. J. Plankton Res., 20: 887900.
Blight, S. P., Bentley, T. L., Lefvre, D., Robinson, C.,
Rodrigues, R., Rowlands, J., and Williams P. J. le B. 1995.
The phasing of autotrophic and heterotrophic plankton
metabolism in a temperate coastal ecosystem. Mar. Ecol.
Prog. Ser., 128: 6174.
Biddanda, B., Opsahl, S., and Benner, R. 1994. Plankton
respiration and carbon ux through bacterioplankton on
the Louisiana shelf. Limnol. Oceanogr., 39: 12591275.
Boyd, P., Robinson, C., Savidge, G., and Williams, P. J. le
B. 1995. Water column and sea ice primary production
during austral spring in the Bellingshausen Sea. Deep-Sea
Res. II, 42: 11771200.
Carlson, C. A., Bates, N. R. T., Ducklow, H. W., and Hansell,
D. F. A. 1999. Estimation of bacterial respiration and
growth efciency in the Ross Sea, Antarctica. Aquat.
Microb. Ecol., 19: 229244.

chap09 2004/11/8 page 176 #30

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

Chipman, D. W., Marra, J., and Takahashi, T. 1993. Primary

production at 47 N 20 W in the North Atlantic Ocean: a
comparison between the 14 C incubation method and the
mixed layer carbon budget. Deep-Sea Res. II, 40: 151169.
Christensen, J. P., Owens, T. G., Devol, A. H., and Packard,
T. T. 1980. Respiration and physiological state in marine
bacteria. Mar. Biol., 55: 267276.
Cota, G. F., Pomeroy, L. R., Harrison, W. G., Jones, E. P.,
Peters, F., Sheldon, Jr., W. M., and Weingartner, T. R. 1996.
Nutrients, primary production and microbial heterotrophy in the southeastern Chukchi Sea: Arctic summer
nutrient depletion and heterotrophy Mar. Ecol. Prog. Ser.,
135: 247258.
del Giorgio, P. A. 1992. The relationship between ETS (electron transport system) activity and oxygen consumption
in lake planktona cross system calibration. J. Plankton
Res., 14: 17231741.
del Giorgio, P. A. and Cole, J. J. 1998. Bacterioplankton
growth efciency in natural aquatic systems. Annu. Rev.
Ecol. Syst., 29: 503541.
del Giorgio, P. A. and Duarte, C. M. 2002. Respiration in
the open ocean. Nature, 420: 379384.
del Giorgio, P. A., Cole, J. J., and Cimbleris A. 1997.
Respiration rates in bacteria exceed plankton production in unproductive aquatic systems. Nature, 385:
148151.
Daneri, G. 1992. Comparison between in vitro and in
situ estimates of primary production within two tracked
water bodies. Arch. Hydrobiol. Beih., 37: 101109.
Daneri, G., Dellarossa, V., Quinones, R., Jacob, B.,
Montero, P. and Ulloa, O. 2000. Primary production and
community respiration in the Humboldt current system
off Chile and associated oceanic areas. Mar. Ecol. Prog.
Ser., 197: 4149.
Dickson, M.-L. and Orchardo, J. 2001. Oxygen production
and respiration in the Antarctic Polar Front region during the austral spring and summer. Deep-Sea Res. II, 48:
41014126.
Dickson, M.-L., Orchard, J., Barber, R. T., Marra, J.,
McCarthy, J. J., and Sambrotto, R. N. 2001. Production
and respiration rates in the Arabian Sea during the 1995
Northeast and Southwest Monsoons. Deep-Sea Res. II, 48:
11991230.
Duarte, C. M. and Agusti S. 1998. The CO2 balance of
unproductive aquatic ecosystems. Science. 281: 234236.
Duarte, C. M., Agusti, S., Arstegui, J., Gonzalez, N.,
and Anadon, R. 2001. Evidence for a heterotrophic
subtropical northeast Atlantic. Limnol. Oceanogr., 46:
425428.
Ducklow, H. W. and S. L. McCallister. In press. The biogeochemistry of carbon dioxide in the coastal oceans.

177

Chapter 10 In The Sea. Volume 13 The Global Coastal Ocean:

Multiscale Interdisciplinary Processes. A. R. Robinson, K.
Brink, H. W. Ducklow, R. Jahnke and B. J. Rothschild.
eds. Harvard University Press. Cambridge, MA. pp.
Ducklow, H. W., Dickson, M-L., Kirchman, D. L., Steward,
G., Orchardo, J., Marra, J., and Azam, F. 2000. Constraining bacterial production, conversion efciency and respiration in the Ross Sea, Antarctica, JanuaryFebruary,
1997. Deep-Sea Res. II, 47: 32273247.
Eissler, Y. and Quinones, R. A. 1999. Microplanktonic respiration off northern Chile during El Nino 19971998. J.
Plankton Res. 21: 22632283.
Emerson, S., Quay, P., Karl, D., Winn, C., Tupas, L.,
and Landry, M. 1997. Experimental determination of
the organic carbon ux from open ocean surface waters.
Nature, 389: 951954.
Emerson, S., Stump, C., Johnson, B., and Karl, D. M. 2002.
In situ determination of oxygen and nitrogen dynamics
in the upper ocean. Deep-Sea Res. I, 49: 941952.
Fasham, M. J. R., Boyd, P. W., and Savidge, G. 1999.
Modeling the relative contributions of autotrophs and
heterotrophs to carbon ow at a Lagrangian JGOFS station in the Northeast Atlantic: the importance of DOC.
Limnol. Oceanogr., 44: 8094.
Gonzalez, N., Anadon, R., Mourino, B., Fernandez, E.,
Sinha, B., Escanez, J., and de Armas, D. 2001. The
metabolic balance of the planktonic community in the
north Atlantic subtropical gyre: the role of mesoscale
instabilities. Limnol. Oceanogr., 46: 946952.
Gonzalez, N., Anadon, R., and Maranon, E. 2002.
Large-scale variability of planktonic net community
metabolism in the Atlantic ocean: importance of temporal changes in oligotrophic subtropical waters. Mar.
Ecol. Prog. Ser., 333: 2130.
Grande, K. D., Marra, J., Langdon, C., Heinemann, K.,
and Bender, M. 1989a. Rates of respiration in the light
measured in marine phytoplankton using an 18 O isotope labelling technique. J. Exp. Mar. Biol. Ecol., 129:
95120.
Grande, K. D., Williams, P. J. le B., Marra, J., Purdie,
D. A., Heinemann, K., Eppley, R. W., and Bender,
M. L. 1989b. Primary production in the North Pacic
gyre: a comparison of rates determined by the 14 C, O2
concentration and 18 O methods. Deep-Sea Res. I, 36:
16211634.
Grifth, P. C., Douglas, D. J., and Wainwright, S. C. 1990.
Metabolic activity of size-fractionated microbial plankton in estuarine, near shore, and continental shelf waters
of Georgia. Limnol. Oceanogr., 59: 263270.
Hanson, A. K., Tindale, N. W., and Abdel-Moatia, M. A. R.
2001. An Equatorial Pacic rain event: inuence on the

chap09 2004/11/8 page 177 #31

178

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

distribution of iron and hydrogen peroxide in surface

waters. Mar. Chem., 75: 6988.
Harrison, W. G. 1986. Respiration and its size-dependence
in microplankton populations from surface waters of the
Canadian Arctic. Polar Biol., 6: 145152.
Harrison, W. G., Arstegui, J., Head, E. J. H., Li, W.
K. W., Longhurst, A. R., and Sameoto, D. D. 2001. Basinscale variability in plankton biomass and community
metabolism in the sub-tropical North Atlantic Ocean.
Deep-Sea Res. II, 48: 22412269.
Herut, B., Shoham-Frider, E., Kress, N., Fiedler, U.,
and Angel, D. L. 1998. Hydrogen peroxide production
rates in clean and polluted coastal marine waters of the
Mediterranean, Red and Baltic Seas. Mar. Pollut. Bull. 36:
9941003.
Hitchcock, G. L., Vargo, G. A., and Dickson, M-L. 2000.
Plankton community composition, production and respiration in relation to dissolved inorganic carbon on
the West Florida shelf, April 1996. J. Geophys. Res., 105:
65796589.
Holligan, P M, Williams, P. J. le B., Purdie, D. A., and
Harris, R. P. 1984. Photosynthesis, respiration and nitrogen supply of plankton populations in stratied, frontal
and tidally mixed shelf waters Mar. Ecol. Prog. Ser., 17:
201203.
Hopkinson, C. S., Sherr, B., and Wiebe, W. J. 1989. Size
fractionated metabolism of coastal microplankton. Mar.
Ecol. Prog. Ser., 51: 155166.
Jacquet, S., Partensky, F., Lennon, J. F., and Vaulot, D.
2001. Diel patterns of growth and division in marine
picoplankton in culture J. Phycol., 37: 357369.
Jahnke, R. A. and Craven, D. B. 1995. Quantifying the
role of heterotrophic bacteria in the carbon cycle: a need
for respiration rate measurements. Limnol. Oceanogr., 40:
436441.
Jenkins, W. J. and Goldman, J. C. 1985. Seasonal oxygen
cycling and primary production in the Sargasso Sea.
J. Mar. Res., 43: 465491.
Johnson, K. M., Davis, P. G., and Sieburth, J. Mc N. 1983.
Diel variation of TCO2 in the upper layer of oceanic
waters reects microbial composition, variation and
possibly methane cycling. Mar. Biol., 77: 110.
Johnson, K. M., Sieburth, J. Mc N., Williams, P. J. le B., and
Brandstrom, L. 1987. Coulometric total carbon dioxide
analysis for marine studies: automation and calibration.
Mar. Chem., 21: 117133.
Karl, D. M., Morris P. J., Williams, P. J. le B., and Emerson,
S. 2003. Metabolic balance of the open sea Nature,
426: 32.
Keeling, R. F. and Shertz, S. R. 1992. Seasonal and
interannual variations in atmospheric oxygen and

implications for the global carbon cycle Nature, 358:

723727.
Kenner, R. A. and Ahmed, S. I. 1975. Measurements of Electron transport activities in marine phytoplankton. Mar.
Biol., 33: 119127.
Kiddon, J., Bender, M. L., and Marra, J. 1995. Production and respiration in the 1989 North Atlantic Spring
blooman analysis of irradiance dependent changes
Deep-Sea Res. I, 42: 553576.
Kruse, B. 1993. Measurement of plankton O2 respiration in
gas-tight plastic bags. Mar. Ecol. Prog. Ser., 94: 155163.
Langdon, C. 1993. The signicance of respiration in production measurements based on oxygen. ICES Mar. Sci.
Symp., 197: 6978.
Laws, E. A., Landry, M. R., Barber, R. T., Campbell, L.,
Dickson, M.-L., and Marra, J. 2000. Carbon cycling in primary production incubations: inferences from grazing
experiments and photosynthetic studies using 14 C and
18 O in the Arabian Sea. Deep-Sea Res. II, 47: 13391352.
Lefvre, D., Minas, H. J., Minas, M., Robinson, C.,
Williams, P. J. le B., and Woodward, E. M. S. 1997.
Review of gross community production, primary production, net community production and dark community respiration in the Gulf of Lions Deep-Sea Res. II, 44:
801832.
Liu, K. K. Atkinson, L., Chen, C. T. A., Gao, S., Hall, J.
Macdonald, R. W., McManus, L. T., and Quinones, R.
2000a. Exploring continental margin carbon uxes on a
global scale EOS, 81: 641642.
Liu K.-K., Iseki, K., and Chao, S.-Y. 2000b. Continental
margin carbon uxes. In R. B. Hanson, H. W. Ducklow,
and J. G. Field (eds) The Changing Ocean Carbon Cycle:
A Midterm Synthesis of the Joint Global Ocean Flux Study
IGBP Series 3. Cambridge University, Press, Cambridge,
UK, pp. 187239.
Longhurst, A. 1998. Ecological Geography of the Sea. Academic Press, San Diego, p. 398.
Luz, B. and Barkan, E. 2000. Assessment of oceanic productivity with the triple-isotope composition of dissolved
oxygen. Science, 288: 20282031.
Marra, J. and Barber, R. T. 2004. Phytoplankton and heterotrophic respiration in the surface layer of the ocean.
Geophys. Res. Lett. 31: L09314.
Marra, J. and Heinemann, K. 1984. A comparison between
non contaminating and conventional incubation procedures in primary production measurements. Limnol.
Oceanogr., 29: 389392.
Moffett, J. W. and Zariou, O. C. 1993. The photochemical
decomposition of hydrogen peroxide in surface waters
of the eastern Caribbean and Orinoco River. J. Geophys.
Res. Oceans, 98: 23072313.

chap09 2004/11/8 page 178 #32

M E A S U R E M E N T I N S U R FA C E M A R I N E W AT E R S

Moncoiffe, G., Alvarez-Salgado, X. A., Figueiras, F. G.,

and Savidge, G. 2000. Seasonal and short-time-scale
dynamics of microplankton community production and
respiration in an inshore upwelling system. Mar. Ecol.
Prog. Ser., 196: 111126.
Nagata, T. 2000. Production mechanisms of dissolved
organic matter. In D. L. Kirchman (ed.) Microbial Ecology
of the Oceans. John Wiley and Sons, Inc., New York.
Packard, T. T. 1971. The measurement of respiratory electron transport activity in marine phytoplankton. J. Mar.
Res., 29: 235244.
Packard, T. T. 1985. The measurement of respiratory
electron transport activity in microplankton. In H. W.
Jannasch and P. J. le B. Williams (eds) Advances in
Aquatic Microbiology. Vol. 3 Academic Press, London, pp.
207261.
Packard, T., Berdalet, E., Blasco, D., Roy, S. O., St-Amand,
L., Lagace, B., Lee, K., and Gagne, J.-P. 1996. CO2 production predicted from isocitrate dehydrogenase activity
and bisubstrate enzyme kinetics in the marine bacterium
Pseudomonas nautica. Aquat. Microb. Ecol. 11: 1119.
Pamatmat, M. M. 1997. Non-photosynthetic oxygen production and non-respiratory oxygen uptake in the dark:
a theory of oxygen dynamics in plankton communities.
Mar. Biol., 129: 735746.
Platt, T. and Denman, K. 1978. The structure of pelagic
marine ecosystems. Rapp. P.-V. Reun. Cons. Int. Explor.
Mer., 173: 6065.
Platt, T., Lewis, M., and Geider, R. 1984. Thermodynamics of the pelagic ecosystem: elementary closure
conditions for biological production in the open ocean.
In M. J. R. Fasham (ed.) Flows of Energy and Materials in Marine Ecosystems. Plenum Press, New York,
pp. 4984.
Pomeroy, L. R., Sheldon, J. E., and Sheldon, W. M. 1994.
Changes in bacterial numbers and leucine assimilation
during estimations of microbial respiratory rates in seawater by the precision Winkler method. Appl. Environ.
Microbiol., 60: 328332.
Pomeroy, L. R., Sheldon, J. E., Sheldon Jr., W. M., and
Peters, F. 1995. Limits to growth and respiration of bacterioplankton in the Gulf of Mexico. Mar. Ecol. Prog. Ser.,
117: 259268.
Rees, A. P., Joint, I., Woodward, E. M. S., and Donald, K. M. 2001. Carbon, nitrogen and phosphorus
budgets within a mesoscale eddy: comparison of mass
balance with in vitro determinations. Deep-Sea Res. II, 48:
859872.
Rees, A. P., Woodward, E. M. S., Robinson, C., Cummings,
D. G., Tarran, G. A., and Joint, I. 2002. Size fractionated
nitrogen uptake and carbon xation during a developing

179

coccolithophore bloom in the North Sea during June

1999. Deep-Sea Res. II, 49: 29052927.
Rivkin, R. B. and Legendre, L. 2001. Biogenic carbon
cycling in the upper ocean: effects of microbial respiration. Science, 291: 23982400.
Robinson, C. 2000. Plankton gross production and respiration in the shallow water hydrothermal systems of Milos,
Aegean Sea. J. Plankton Res., 22: 887906.
Robinson, C. and Williams, P. J. le B. 1991. Development
and assessment of an analytical system for the accurate
and continual measurement of total dissolved inorganic
carbon Mar. Chem., 34: 157175.
Robinson, C. and Williams, P. J. le B. 1993. Temperature and
Antarctic plankton community respiration J. Plankton
Res., 15: 10351051.
Robinson, C. and Williams, P. J. le B. 1999. Plankton net
community production and dark respiration in the Arabian Sea during September 1994. Deep-Sea Res. II, 46:
745766.
Robinson, C., Archer, S., and Williams, P. J. le B. 1999.
Microbial dynamics in coastal waters of East Antarctica:
plankton production and respiration. Mar. Ecol. Prog.
Ser., 180: 2336.
Robinson, C., Serret, P., Tilstone, G., Teira, E., Zubkov,
M. V., Rees, A. P., and Woodward, E. M. S. 2002a. Plankton respiration in the Eastern Atlantic Ocean Deep-Sea
Res. I, 49: 787813.
Robinson, C., Widdicombe, C. E., Zubkov, M. V., Tarran,
G. A., Miller, A. E. J., and Rees, A. P. 2002b. Plankton
community respiration during a coccolithophore bloom
Deep-Sea Res. II, 49: 29292950.
Roy, S. O. and Packard, T. T. 2001. CO2 production rate
predicted from isocitrate dehydrogenase activity, intracellular substrate concentrations and kinetic constants
in the marine bacterium Pseudomonas nautical Mar. Biol.
138: 12511258.
Sampou, P. and Kemp, W. M. 1994. Factors regulating
plankton community respiration in Chesapeake Bay
Mar. Ecol. Prog. Ser., 110: 249258.
Serret, P., Fernandez, E., Sostes, J. A., and Anadon, R. 1999.
Seasonal compensation of microbial production and respiration in a temperate sea. Mar. Ecol. Prog. Ser., 187:
4357.
Serret, P., Robinson, C., Fernandez, E., Teira, E., and
Tilstone, G. 2001. Latitudinal variation of the balance between plankton photosynthesis and respiration in the E. Atlantic Ocean. Limnol. Oceanogr., 46:
16421652.
Serret, P., Fernandez, E. and Robinson, C. 2002. Biogeographic differences in the net ecosystem metabolism of
the open ocean. Ecology, 83: 32253234.

chap09 2004/11/8 page 179 #33

180

R E S P I R AT I O N I N A Q U AT I C E C O S YS T E M S

Sheldon, R. W., Prakash, A. and Sutcliffe W. H. 1972.

The size distribution of particles in the Ocean. Limnol.
Oceanogr., 17: 327340.
Sherr, E. B., Sherr, B. F. and Sigmon, C. T. 1999. Activity of
marine bacteria under incubated and in situ conditions.
Aquatic Microbial Ecology, 20: 213223.
Sherry, N. D., Boyd, P. W., Sugimoto, K., and Harrison,
P. J. 1999. Seasonal and spatial patterns of heterotrophic
bacterial production, respiration, and biomass in the
subarctic NE Pacic. Deep-Sea Res., II, 46: 25572578.
Smith S. V. and Mackenzie, F. T. C. 1987. The oceans as a
net heterotrophic system: implications from the carbon
biogeochemical cycle. Glob. Biogeochem. Cyc., 1: 187198.
Sondergaard, M., Williams, P. J. le B., Cauwet, G.,
Rieman, B., Robinson, C., Terzic, S., Woodward, E. M.
S., and Worm, J. 2000. Net accumulation and ux of dissolved organic carbon and dissolved organic nitrogen
in marine plankton communities. Limnol. Oceanogr., 45:
10971111.
Straile, D. 1997. Gross growth efciencies of protozoan and
metazoan zooplankton and their dependence on food
concentration, predator prey weight ratio and taxonomic
group. Limnol. Oceanogr., 42: 13751385.
Sullivan, C. W., Arrigo, K. R., McClain, C. A., Comiso, J. C.,
and Firestone, J. 1993. Distribution of phytoplankton
blooms in the Southern Ocean. Science, 262: 18321837.
Upstill-Goddard, R. C., Watson, A. J., Wood, J., and
Liddicoat, M. I. 1991. Sulfur hexauoride and 3 He as seawater tracersdeployment techniques and continuous
underway analysis for sulfur-hexauoride. Anal. Chim.
Acta, 249: 555562.
Vezina, A. F. and Platt, T. 1988. Food web dynamics in the
ocean. I. Best-estimates of ow networks using inverse
methods. Mar. Ecol. Prog. Ser., 42: 269287.
Williams, P. J. le B. 1981. Microbial contribution to overall
marine plankton metabolism: direct measurements of
respiration. Oceanol. Acta, 4: 359364.
Williams, P. J. le B. 1982. Microbial contribution to overall
plankton community respiration studies in enclosures,
In G. D. Grice and M. R. Reeve (eds) Marine Microcosms.
Springer-Verlag, Berlin, pp. 305321.

Williams, P. J. le B. 1995. Evidence for the seasonal accumulation of carbon-rich dissolved organic material, its scale
in comparison with changes in particulate material and
the consequential effect on net C/N assimilation ratios.
Mar. Chem., 51: 1729.
Williams, P. J. le B. 1998. The balance of plankton respiration and photosynthesis in the open oceans. Nature, 394:
5557.
Williams, P. J. le B. 2000. Net production, gross production
and respiration: what are the interconnections and what
controls what ? In R. B. Hanson, H. W. Ducklow, and J. G.
Field (eds) The Changing Ocean Carbon Cycle: A Midterm
Synthesis of the Joint Global Ocean Flux Study. Cambridge
University Press, Oxford, UK, p. 514.
Williams, P. J. le B. and Bowers, D. G. 1999. Regional carbon
imbalances in the oceans. Science, 284: 1735b.
Williams, P. J. le B. and Gray, R. W. 1970. Heterotrophic utilization of dissolved organic compounds
in the sea. II: observations on the responses of heterotrophic marine populations to abrupt increase in
amino acid concentration J. Mar. Biol. Assoc. UK, 50:
871881.
Williams, P. J. le B. and Purdie, D. A. 1991. In vitro and
in situ derived rates of gross production, net community
production and respiration of oxygen in the oligotrophic
subtropical gyre of the North Pacic Ocean. Deep-Sea Res.
I, 38: 891910.
Williams, P. J. le B., Morris, P. J., and Karl, D. M. 2004.
Net community production and metabolic balance at the
oligotrophic ocean site: Station ALOHA. Deep-Sea Res..
Yocis, B. H., Kieber, D. J., and Mopper, K. 2000. Photochemical production of hydrogen peroxide in Antarctic
waters Deep-Sea Res. I, 47: 10771099.
Yuan, J. C. and Shiller, A. M. 2001. The distribution of
hydrogen peroxide in the southern and central Atlantic
Ocean Deep-Sea Res. II, 48: 29472976.
Zubkov, M. V., Sleigh, M. A., and Burkill, P. H. 2000.
Assaying picoplankton distribution by ow cytometry
of underway samples collected along a meridional transect across the Atlantic Ocean. Aquat. Microb. Ecol., 21:
1320.

chap09 2004/11/8 page 180 #34