Journal of Marine Systems 17 Ž1998. 275–288
Estimates of Southern Ocean primary production—constraints
from predator carbon demand and nutrient drawdown
J. Priddle ) , I.L. Boyd, M.J. Whitehouse, E.J. Murphy, J.P. Croxall
British Antarctic SurÕey, Natural EnÕironment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK
Received 15 October 1995; accepted 15 July 1996
Abstract
In view of the wide range of estimates for the total primary production for the Southern Ocean south of the Subantarctic
Front—current estimates range from 1.2 to 3.5 Gtonne C yeary1 —we have examined two indirect methods for assessing
primary production. First, we have estimated the primary production needed to sustain the carbon requirements of the
endotherm top predators in the ecosystem. Estimation of the carbon requirements for crabeater seals of about 7 Mtonne C
yeary1 is extrapolated to a value for all endotherm predators of 15–30 Mtonne C yeary1. Current data indicate that 70–80%
of the diet of this suite of predators is zooplankton Žpredominantly the euphausiid krill., making for highly efficient transfer
from primary production to top predators. Our best estimate of Southern Ocean primary production by this method is of the
order of 1.7 Gtonne C yeary1, or an averaged areal primary production of about 30–40 g C my2 yeary1. Our second
approach is to estimate primary production from the drawdown of inorganic nutrients, based on the limited suite of studies
from which an annual nutrient deficit can be calculated. Again, this indicates annual primary production of the order of 1.5
Gtonne. Although both methods have inherent uncertainties, taken together they provide a relatively robust constraint on
annual primary production. For both methods to underestimate primary production by the 1–1.5 Gtonne C implied by the
higher current estimates, carbon export from the Southern Ocean pelagic ecosystem would need to be much higher than is
normally found in other oceans.
Resume
´
´
Au regard
a` la vaste gamme des estimations de la production primaire totale pour l’Ocean
´
´ Austral au sud du Front
Subantarctique—les estimations actuelles varient de 1.2 a` 3.5 Gt C yy1 —nous avons examine´ deux methodes
indirectes
´
pour evaluer
la production primaire. Nous avons en premier lieu estime´ la production primaire necessaire
pour subvenir aux
´
´
besoins en carbone des predateurs
superieurs
endothermes dans l’ecosysteme.
Une estimation d’environ 7 Mt C yy1 pour les
´
´
´
´
besoins de la population de phoques crabiers est extrapolee
´ a` une valuer de 15–30 Mt C yy1 pour l’ensemble des predateurs
´
endothermes. Les donnes
sont constitues
´ actuelles indiquent que 70–80% de la ressource alimentaire de ces predeteurs
´
´ de
zooplancton Žprincipalement du krill., ce qui permet un transfert efficace de la production primaire vers les predateurs
´
superieurs.
Notre meilleure estimation de la production primaire de l’Ocean
est de’ordre de 1.7 Gt
´
´ Austral par cette methode
´
C yy1, soit une moyenne pour la zone d’environ 30–40 g C my2 yy1. Notre second approche est d’estimer la production à
partir de la consommation d’elements
nutritifs mineraux,
en nous basant sur l’ensemble restreint d’etudes
pour lesquels un
´
´
´
deficit
annuel de sels nutritifs peut etre
donne egalement
une production primaire annuelle de l’ordre
´
ˆ calcule.
´ Cette methode
´
´
)
Corresponding author. Tel.: q44-1223-221-597; Fax: q44-1223-221-254; E-mail: [email protected]
0924-7963r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved.
PII: S 0 9 2 4 - 7 9 6 3 Ž 9 8 . 0 0 0 4 3 - 8
276
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
de 1.5 Gt. Bien que les deux methodes
presentent
des incertirtudes propres, elle encadrent, prises ensemble, la production
´
´
primaire annuelle de maniere
exactes, les deux methodes
´ assez robuste. Si les plus fortes estimations actuelles etaient
´
´
devraient sous-estimer de 1 a` 1.5 Gt C la production primaire annuelle, ce qui impliquerrait une exportation de carbone par
l’ecosysteme
tres
a` ce qu’elle est normalement dans les autre oceans.
q 1998 Elsevier Science B.V. All
´
´ pelagique
´
´ superieure
´
´
rights reserved.
Keywords: Predator; Carbon requirement; Nutrient
1. Introduction
Current estimates of the primary production of the
Southern Ocean south of the Subantarctic Front Žreferred to here as the Antarctic Southern Ocean,
ASO., range from 1.2 to 3.5 Gtonne C yeary1
ŽHuntley et al., 1991; Smith, 1991.. A recent estimate based on ocean colour measurements puts total
ocean primary production of 45–50 Gtonne C yeary1
ŽLonghurst et al., 1995.. Their biogeochemical
provinces do not match the delineation of the ASO
used here, but their most southerly zones APLR and
ANTR had an estimated combined primary production of 2.24 Gtonne C yeary1 , but this excludes the
Polar Frontal Zone which forms the southern part of
their larger SANT province Žtotal production 3.63
Gtonne C yeary1 .. It seems likely that Longhurst et
al. Ž1995. would predict a primary production of
3.5–4 Gtonne C yeary1 for the ASO as defined here
and by other studies. In most estimates, the ASO has
a primary production lower than that implied by its
area Žabout 35 = 10 6 km2 or around 10% of the
world’s ocean area., which suggests that it should
have an annual primary production of around 4
Gtonne C yeary1 . The ASO is also the largest area
of the world’s ocean where nutrients are not utilized
fully by phytoplankton production during the growth
season—the so-called ‘High Nutrient–Low Chlorophyll’ ŽHNLC. phenomenon Žsee Chisholm and
Morel, 1991.. Consequently there is a need to understand the dynamics of carbon cycling within the
Southern Ocean in the context of the global carbon
cycle, because such areas can be identified as the
only locations where nutrient concentrations do not
limit annual primary production and thus increases in
biological carbon drawdown are at least possible
ŽPriddle et al., 1992..
The uncertainty in our current understanding of
the total primary production in the Southern Ocean is
a drawback when considering global oceanic carbon
fluxes. The database for ‘conventional’ measurements of primary production is patchy in space and
time ŽPriddle et al., 1992; Longhurst et al., 1995.,
and such ‘point estimates’ may, in any case, provide
poor integrations of annual productivity ŽWiggert et
al., 1994.. The use of ocean colour remote sensing
estimates provides a coverage which is closer to
synoptic, but for the Southern Ocean poor coverage
with the Coastal Zone Colour Scanner ŽCZCS—the
only satellite dataset. is compounded by bio-optical
problems which may compromise phytoplankton
biomass retrieval algorithms ŽMitchell and HolmHansen, 1991; Fenton et al., 1994; Sagan et al.,
1995.. The calculation of primary production data
from chlorophyll biomass is again dependent on
scarce measurements of photosynthetic parameters
Žcf. Longhurst et al., 1995..
Here we examine Southern Ocean primary production from two contrasting standpoints. First, we
have combined estimates of the carbon flux to top
predators with a simple model of trophic efficiency
to predict a likely range for the primary production
needed to sustain the pelagic foodweb. Second, we
compile the relatively restricted dataset on annual
drawdown of inorganic nutrients and interpret these
in terms of primary production. This again suggests a
relatively narrow range for Southern Ocean annual
primary production, and we compare the two approaches and their likely sources of error. We emphasise that we are putting neither approach forward
as proxy measurements per se, but at the same time
they provide a valuable constraint on regional estimates which are otherwise poorly controlled.
2. Carbon demand by top predators
A special feature of interest in the context of
oceanic carbon cycling is the unusual combination of
features of the ASO food-web. Classically, this contains relatively short pathways between relatively
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
large organisms—diatoms, large euphausiid crustaceans, and mammalian and avian predators. Although such a picture understates the complexity of
the ASO pelagic food web, it also highlights features
important in the context of carbon cycling. The high
proportion of endotherm top predators in the ASO
has been implicated as a means whereby autotrophically-fixed carbon may be returned rapidly to the
atmosphere ŽHuntley et al., 1991. although the magnitude of this ‘leak’ has been questioned ŽMoloney,
1992; van Franneker et al., 1994, van Franneker et
al., 1997; Banse, 1995.. This paper is not concerned
directly with that particular argument, but we return
to the magnitude of CO 2 flux from air-breathing
predators at the end. However, the apparent dominance by birds and mammals of the top predator
level in the Southern Ocean pelagic system provides
a means of describing the underlying primary production. Because some of these predators are accessible on land for part of the year, they have been the
subject of physiological studies which are not carried
out so easily with aquatic predators Žfish and pelagic
cephalopods.. On the basis of these measurements,
and using biomass and demographic data, we argue
that overall carbon demand by Southern Ocean endotherm predators can be estimated with a moderate
level of accuracy. We then combine this information
with a range of scenarios of food-web efficiency to
‘back predict’ a most plausible range of primary
production.
2.1. The estimation of carbon demand by all warmblooded top predators
We started our calculation of carbon flux to endotherm predators by considering the single species
for which we have the best data, and fortunately one
which is of considerable importance in the Southern
Ocean ecosystem. The crabeater seal Ž Lobodon carcinophagus. is very abundant ŽErickson and Hanson,
1990., is predominantly a krill predator ŽLaws, 1984.,
and has a body size which falls around the midpoint
of the suite to avian and mammalian predators for
which we eventually wish to estimate carbon demand. Our calculation of the flux of carbon to
crabeater seals in the Southern Ocean is set out in
detail in Appendix A. Net of losses during assimilation, demand was in the range of 3.9–9.3 Mtonne C
yeary1 with a most probable value of 6.0 Mtonne C
yeary1 ŽTable 1.. The assimilation efficiency of
crabeater seals feeding on krill is 83.8 " 2.2%
ŽNordøy et al., 1994.. This implies that the total flux
of carbon to crabeater seals is 7.2 Mtonne yeary1
Žrange 2.8–11.1 Mtonne yeary1 ..
The mass of carbon sequestered within body tissues was 0.27 Mtonne Žrange 0.01–0.03 Mtonne.
and the ratio of carbon flux to sequestered carbon
was 8.4:1 Žrange 7.3:1–9.0:1.. Thus growth efficiency, expressed in terms of carbon sequestered as a
percentage of carbon assimilated, was 3.7%. This is
within the range estimated for mammals ŽHumphries,
1979..
This analysis only considered crabeater seals. We
do not have similar data to calculate carbon budgets
for other major endotherm predator species, and
therefore need to apply our estimates for crabeater
seals to other predators. Based on the rough calculations presented in Table 2, crabeater seals are likely
to constitute about one-third of the total metabolic
biomass of endotherm predators in the Southern
Ocean, the remainder being composed of whales
Žmainly 0.75 million minke whales, Balaenoptera
Table 1
Estimate of carbon flux to crabeater seals including maximum and minimum values
Source
Carbon flux
ŽMt yry1 .
Minimum carbon flux
ŽMt yry1 .
Maximum carbon flux
ŽMt yry1 .
Y Metabolism
Y Growth
Y Reproduction
? Metabolism
? Growth
Total
2.973
0.013
0.136
2.879
0.014
6.028
1.126
0.005
0.057
1.091
0.004
2.283
4.570
0.016
0.225
4.429
0.017
9.257
See Appendix A for details of calculations.
277
278
Table 2
Calculation of the approximate metabolic biomass for the main species and groups of top predators in the Southern Ocean
Mean body
mass
Žkg.
Population
size
Žmillions.
Metabolic
biomassa
Žmillion tonnes.
Source
Major
proportion
of diet b
Crabeater seal
180
12
2.65
zooplankton
Weddell seal
Southern elephant seal
Antarctic fur seal
Minke whale
Penguins
Odontocete whales
Total
200
250
35
5000
4.5
; 3500
2
1
3
0.75
50 c
1
0.49
0.30
0.16
3.09
0.87
0.29 d
7.85
Erickson and Hanson Ž1990.; Laws Ž1984.;
BAS unpublished data
Erickson and Hanson Ž1990.
SCAR Ž1991.; Boyd et al. Ž1994.
Boyd Ž1993.; Payne Ž1979.
International Whaling Commission; Folklow and Blix Ž1992.
Croxall Ž1984.
Kasamatsu and Joyce Ž1995.
fish
fish and squid
zooplankton
zooplankton
zooplankton
fish and squid
The numbers given are approximate and are for illustrative purposes only. According to these figures, crabeater seals metabolic biomass accounts for 34% of the total endotherm
predator metabolic biomass. Species not included in the calculations are assumed not to have a significant overall effect on the proportion of carbon flux due to crabeater seals
Žespecially when rounded to be one-third of the total flux due to endotherm predators. due either to their small size andror their low numbers.
a
Metabolic biomass was calculated as the product of the approximate population size and the mean mass 0.88 in the case of the mammals and the mean mass 0.75 in the case of the
penguins ŽNagy, 1987..
b
The major proportion of the diet is indicated for each species or group, but this is not exclusive. In particular, some penguin species are fish or squid feeders, and part of the diet
of Antarctic fur seals comprises fish.
c
The figure for the number of penguins is an estimate with a large potential error. However, errors in this value will have a relatively small impact on the estimate of total
metabolic biomass.
d
The biomass for odontocete whales is calculated based on data presented by Kasamatsu and Joyce Ž1995. ŽTable IX. further adjusted for metabolic body mass and for the
proportion of time these animals spend in the Southern Ocean Žestimated by Kasamatsu and Joyce to be 90 days..
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
Species
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
acutorostrata., other seals Ž; 6 million individuals.
and seabirds, the greatest biomass of which will be
penguins. Crabeater seal body mass falls at around
the midpoint of the range for this suite of predators,
and as a crude ‘rule of thumb’ we suggest that
allometric differences across the size range will balance out, allowing us to extrapolate across the range
of predators. On this basis, total carbon flux to
endotherm predators is likely to be in the region of
15 to 30 Mtonne C yeary1 . Based on efficiency of
3.7% Žcalculated for crabeater seals feeding on krill.,
this is equivalent to an overall top predator production of 0.55–1.11 Mtonne C yeary1 . In the following
calculations, we will use the upper bound value only.
2.2. Food-web efficiency
In order to use the carbon flux to top predators to
estimate the primary production needed to sustain
the entire pelagic ecosystem, we must estimate the
efficiencies of the various intervening transfers. In
order to do this, we have used a very simple food
web model, coupled with plausible values of transfer
efficiencies.
279
The model ŽFig. 1a. contains five compartments,
and is structured in two layers. Carbon flux in the
bottom layer may either be directly from phytoplankton to zooplankton, or through an intermediate trophic
level which is dominated by the microbial web but
may also contain smaller mesozooplankton—the taxonomic composition of all compartments in the lower
layer is defined only loosely. In a similar way,
carbon flux in the upper layer may be directly from
zooplankton to top predators Ži.e., endotherms., or
via an intermediate trophic level containing aquatic
predators such as fish and cephalopods. We have
used different transfer efficiencies ŽTE. Žproportion
of production in a lower trophic level which appears
as production in the next level up. for the different
links in the food-web. The TE for the grazers in the
microbial web is taken as 40%, the midpoint of the
range 30–50% quoted by Fenchel Ž1987., although
we are aware that very much higher efficiencies have
been quoted for some microheterotrophs. The TE of
12% used for transfers to zooplankton is a slightly
pessimistic version of the range of 15–20% quoted
by Banse Ž1995. for euphausiids. A TE of 10% for
fish and squid is based on an analysis of marine
Fig. 1. Ža. Diagram of the foodweb model used to predict primary production from top predator production. Carbon flux between
phytoplankton and zooplankton, and between zooplankton and top predators can take either a ‘direct’ route, or an ‘indirect’ route via an
intermediate trophic level. Partition of carbon flux between these routes for the top and bottom of the foodweb is independent. The ‘transfer
efficiencies’ indicated on the diagram represent the production at the higher trophic level as a proportion of production in the lower
component—values used are explained in the text. Žb. Contour plot of the values of primary production ŽGtonne C yeary1 . for the ASO
predicted by different partitioning of carbon flux through the food web model. The graticule indicates our most probable estimates of the
proportion of carbon flow through the higher and lower trophic levels, and the corresponding primary production.
280
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
fisheries ŽPauly and Christensen, 1995.. For the consumption of zooplankton by top predators, we have
used a TE of 3.5% based on the calculation of 3.7%
growth efficiency for crabeater seals in this paper.
The value of TE s 2.5% for fish and squid consumption by top predators reflects the fact that part of this
diet will involve an additional step Žseals feeding on
squid feeding on fish feeding on zooplankton, for
example.. The value for TE is arrived at by assuming
that the transfer to the top predators is also 3.5%
efficient, and that the more complex pathway Žwith
overall TE s 0.35%. accounts for about one-third of
the overall flux along this route. Taking the two
extreme behaviours of the model, a three-level transfer—the classical ‘diatom–krill–whale’ pathway—
has the most efficient transfer, with 0.42% of primary production converted into top predator production, whereas carbon flow passing through all five
‘levels’ in the model reduces the transfer efficiency
to 0.012%.
This very simple model is designed specifically
for the purposes of this paper, and is structured to
highlight the effects of different trophic pathways. In
order to separate the effects of trophic complexity in
the top and bottom layers, we have made these
independent. As a consequence, all carbon flux from
phytoplankton to zooplankton enters the same zooplankton compartment, irrespective of the pathway
along which it travels ŽFig. 1a.. The top level has a
similar structure, with a direct and an indirect route
but all flows directed towards a single top predator
compartment. Apart from this property, the model is
very similar to other models describing carbon flow
through the Southern Ocean pelagic ecosystem
ŽHuntley et al., 1991; Banse, 1995.. The model is
also closed in the sense that all carbon sequestered
by primary production enters the food web and is
either respired or ends up in top predator production.
We have not included other loss processes, although
some of the transfer efficiencies in the bottom layer
are deliberately pessimistic Žcompare our 12% transfer efficiency to zooplankton with the 15–20% for
euphausiids used by Banse, 1995., and note also that
we have used the higher end of the range of predator
carbon demand to prime our model. If loss processes
are underestimated, then our estimate of primary
production could be lower than the real value—a
factor discussed later in the paper.
In describing the model, we noted the overall
transfer efficiencies for the two extreme modes of
the model. In order to use the top predator data to
predict primary production, we vary the share of
carbon flux between direct and indirect pathways
independently for the top and bottom layers of the
foodweb. The share is described by the proportion
flowing along the indirect route—this statistic has a
value 100% is when all carbon passes through an
intermediate trophic level between either the phytoplankton and zooplankton, or zooplankton and top
predators.
Taking the upper value of 30 Mtonne C yeary1
from our range of top predator carbon demand
Žequivalent to production of 1.11 Mtonne C yeary1 .,
100% indirect flow in both layers implies the implausibly high primary production of ) 8 Gtonne C
yeary1 ŽFig. 1b.. At the opposite extreme, with zero
indirect flow the foodweb can be sustained by primary production of 0.5 Gtonne C yeary1 . The efficiency of transfer in the top layer has much greater
impact than at the bottom, because of the low efficiency used for top predator production and the high
efficiency ascribed to the microbial web ŽFig. 1b.. In
order to use this approach, we need to narrow our
choice of values of the percent indirect flow, to
reflect plausible trophic behaviour. Croxall et al.
Ž1985. provide the only large-scale attempt to assess
the relative contributions of different types of prey to
the food supply of Southern Ocean endotherm predators. They estimate that overall 70% of the diet of
birds and seals breeding around the Scotia Sea comprises krill, with the remainder dominated by fish
and squid. This figure may underrepresent the importance of krill, which is the major component of the
diet of baleen whales not covered by Croxall et al.
Ž1985., but subsequent evidence that fish and squid
may be the dominant component of diet in winter for
predators which are krill-feeders in summer may
counterbalance this. We also note that the overall
contribution of crabeater seals to the prey uptake by
endotherm predators will not be well-represented by
the Scotia Sea data, and again these are almost
exclusively krill predators. We therefore examine a
scenario for 70–80% krill Ž‘zooplankton’ in our
model. in predator diet, or an ‘indirect’ flow of
20–30%. For the lower layer of the foodweb, we
follow the suggestion of Banse Ž1995. of an indirect
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
flow of about 50% for the Southern Ocean as a
whole, and note our earlier observation that the
output of this simulation is, in any case, less sensitive to the behaviour of this part of the food web.
Taking our most plausible picture of transfer
through the foodweb, and using top predator production of 1.11 Mtonne C yeary1 , we suggest a value
for Southern Ocean annual primary production of the
order of 1.7 Gtonne C yeary1 ŽFig. 1b.. Even with
100% flow through the microbial loop, this would
only just exceed 2 Gtonne C yeary1 for the 20–30%
indirect flow for the top layer, and conversely direct
transfer from phytoplankton to zooplankton lowers
the value to about 0.9 Gtonne C yeary1 ŽFig. 1b.. If
we keep the indirect flow in the lower layer at 50%,
then it is easy to see that increasing importance of
fish and squid in the diet of top predators implies
rapidly increasing primary production—about 3
Gtonne C yeary1 at 50% indirect flow, and 4 Gtonne
C yeary1 at 70%. Increasing the complexity of the
upper part of the food web, and thereby decreasing
its efficiency, has a strong amplifying effect because
it demands greater zooplankton production and thus
greater primary production. To take a simple example, we can run the model for crabeater seal produc-
281
tion alone Žabout 0.26 Mtonne C yeary1 .. If its diet
is 100% krill, then it only requires about 0.1 Gtonne
C yeary1 primary production to maintain crabeater
seal production. However, for an equivalent piscivorous seal the ‘krill–fish–seal’ food chain increases to
this value 1.1 Gtonne C yeary1 , and it would be 11
Gtonne yeary1 for the food chain ‘krill–fish–fish–
seal’. Although the model is clearly sensitive to both
the values of TE and the way carbon is routed
through the food web, we believe that there are
sufficient data to remove much of the uncertainty
from our estimates. In particular, the predominance
of top predators feeding on krill and other zooplankton precludes the higher values of primary production estimated for the ASO. Conversely if all endotherm predators were feeding at the top of the
most complex chain covered here they would require
primary production close to the value estimated by
Longhurst et al. Ž1995. for the entire world ocean.
3. Drawdown of inorganic nutrients
The uptake of dissolved nitrogen, silicon and
phosphorus have been correlated with primary pro-
Table 3
Averaged annual mixed layer nutrient concentration deficitsa for Southern Ocean study areas
SiŽOH.4
PO4
NO 3
Source
Winter-to-summer
South Georgia
Bransfield Strait ŽBIOMASS.
Weddell Sea ice edge
25–30 b
–
17
0.75
; 0.8
0.5
5
; 10
6
Whitehouse et al. Ž1996.
Priddle et al. Ž1994.
Jennings et al. Ž1984.
Residual winter conc.a
Elephant Island ŽAMLR.
Bransfield Strait
Bellingshausen Sea MIZ
Weddell Sea MIZ
Weddell-Scotia MIZ
Ross Sea ice edge
5–21b
13
) 10
- 10
7
20
0.25–0.432 b
0.35
) 0.4
–
0.3
1
1.5–7 b
4.6
)5
;5
2.5
15
Silva et al. Ž1995.
BAS unpublished data
Whitehouse et al. Ž1995.
Bianchi et al. Ž1992.
Nelson et al. Ž1987.
Nelson and Smith Ž1986.
Sediment trap a
Bransfield Strait ŽRACER.
–
; 0.25
; 10
Karl et al. Ž1991.
a
a
Integrated values divided by mixed layer depth, concentration units millimoles per cubic meter. ‘Winter-to-summer’ data are for studies
where the seasonal changes in mixed layer concentrations can be determined directly, whilst ‘Residual winter conc.’ indicates where
calculations are based on differences between mixed layer values and winter concentrations predicted from values at the temperature-minimum layer, or immediately beneath the summer mixed layer. The single sediment trap result is included for comparison with the other
Bransfield Strait data
b
Range of values derived for different water masses.
282
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
duction in a variety of pelagic ecosystems, and may
provide the means to integrate primary production
over the annual cycle Že.g., Jennings et al., 1984..
Although the number of sites in the Southern Ocean
for which suitable data are available is limited, we
consider that it is worthwhile to examine the implications of these measurements for primary production.
In the context of this paper, it is also important to
note that any estimate of primary production based
on nutrient drawdown will be independent of predator carbon demand.
For Southern Ocean studies, there are two approaches to estimating annual nutrient drawdown.
For a very small number of studies, it has been
possible either to construct the entire annual cycle
ŽJennings et al., 1984; Whitehouse et al., 1996. or to
use data for the main growing season Žquasi-annual
data. ŽPriddle et al., 1994.. The remaining estimates
used here depend on the ability to predict winter
mixed layer ŽWML. concentrations on the basis of
the residue of the WML, characterised in Antarctic
Surface Water by a minimum in the vertical temperature profile, below the summer mixed layer. We
have assembled data from nine studies in the Southern Ocean, of which six are based on the residual
WML concentration technique and only three are
annual or quasi-annual studies.
The overall consensus from published data suggests that the average annual changes in concentration of SiŽOH.4 , PO4 and NO 3 are 10–20, 0.5–0.75
and 5–10 mmol my3 yeary1 respectively ŽTable 3..
To convert these data to primary production, we
apply conversion factors based on the stoichiometry
of nutrient uptake. For silicate, we use a C:Si molar
ratio of 4, which appears to be a reasonable compromise value for a range of Southern Ocean phytoplankton communities ŽPriddle et al., 1995, and references therein.. For phosphate, we use the classical
Redfield ratio of C:P s 106. If the averaged deficits
for these two nutrients are scaled up to the entire
Southern Ocean and a mixed layer depth of 50 m,
the resulting estimates of primary production are
1–1.5 Gtonne C yeary1 . For nitrate, the picture is
confused slightly because this only represents a part,
itself poorly constrained, of the nitrogen pool utilised
in primary production ŽSambrotto et al., 1993; Banse,
1994; Priddle et al., 1995.. Conformity with the
Redfield ratio ŽC:N s 6.625. suggests relatively low
primary production, less than 1 Gtonne C yeary1 .
Decreasing the uptake f-ratio Žnitrate as a proportion
of total nitrogen uptake. produces a corresponding
increase in the primary production implied by the
nitrate drawdown. Southern Ocean primary production prediction which corresponds to the values obtained for silicate and phosphate drawdown corresponds to an f-ratio of between 0.5 ŽC:NO 3-N f 13.
and 0.75 ŽC:NO 3-N f 9..
4. Assessment and comparison of the two approaches
At the present level of knowledge, neither method
employed here can be sustained as a proxy for
primary production. However, both are useful as
yardsticks against which to measure the fairly wide
range of estimates of Southern Ocean primary production in the current literature. We need to look at
the likely errors embodied in each technique, before
comparing the two approaches. We do this by an
evaluation of the weaknesses of each, and by considering the implications of primary production values
at the extremes of the current range of estimates
Žabout 1.2 to 3.5 Gtonne C yeary1 : Huntley et al.,
1991; Smith, 1991..
4.1. Predator carbon demand and trophic efficiency
Our approach embodies two components—an extrapolation from one Ždominant. top predator species
to the carbon demand for the entire suite of endotherm predators, and the prediction of primary
production from this carbon demand using a range of
food-web scenarios.
We feel that the range of estimates of carbon
demand for crabeater seals is the best possible for
current data, and that this species is a suitable case
study for such an approach to trophic dynamics. It is
the most abundant Antarctic Žand global. pinniped
species, is predominantly a krill predator, and occupies a midposition in the size spectrum of endotherm
predators Žsmall birds to large whales.. Our extrapolation to give a carbon demand for all endotherm
predators is based on the likely share of total biomass
ascribed to crabeater seals. We have implicitly taken
allometric considerations into account in dividing the
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
biomass, and hence carbon flux between the crabeater
seal, a midsized predator, and the remainder of the
size range from penguins to whales.
The translation of predator carbon demand into
primary production is dependent on the structure and
parameters of the food-web model. We have already
noted that the model does not explicitly include loss
processes other than those arising from the processing of carbon within and between trophic levels. This
includes the assumption that migration out of the
Southern Ocean does not represent a significant route
for carbon loss, in addition to the lack of explicit
treatment of vertical particulate flux. However, we
have already noted that we have erred towards caution in the transfer efficiencies specified in the bottom layer of the foodweb, and that top predator
production used for all calculations is our upper
limit, so that the absence of nontrophic carbon flux
should not be viewed as the major omission it might
at first seem.
This leaves the sensitivity of the model to different interpretations of the trophic structure. We have
commented on this already, and noted that the model
is sensitive to properties of the top of the model food
web, whilst changes in the complexity of the bottom
half of the have little effect. Even 90% routing
through the microbial web does not increase the
value of Southern Ocean primary production to ) 2
Gtonne C yeary1 if predators take F 20% ‘non-krill’
prey. For a 50:50 partition of carbon flow at the
Phytoplankton-to-Krill level, a 50:50 partition or
worse at the top level is required to imply a primary
production value significantly greater than 2 Gtonne
yeary1 . If all of the zooplankton carbon reaches the
top predators via fish and squid, and the microbial
loop accounts for 50% of the carbon flux in the
bottom layer, this implies a primary production of
around 5.5 Gtonne C yeary1 . The upper bound of
current primary production estimates implies that
50–60% of the diet of top predators consists of fish
and squid—a scenario which is clearly at variance
with observations of Croxall et al. Ž1985. and which
conflicts with the fact that crabeater seals and minke
whales, both almost exclusively krill predators, together constitute two thirds of the endotherm predator biomass. Therefore, if the food web structure,
partitioning and efficiencies used here are accepted
as realistic, then either the predicted primary produc-
283
tion is also close to the real value, or higher estimates imply considerable loss of photosyntheticallyfixed carbon from the food web.
4.2. Nutrient uptake
The utility of the nutrient drawdown data depends
crucially on two properties. First, the stoichiometry
of nutrient uptake and carbon fixation need to be
defined. As a part of this, we need to satisfy ourselves that primary production is not being underestimated because of nutrient recycling—we have already explored this problem in the case of nitrate.
Second, we need to be in a position to judge how far
our rather limited dataset can be extrapolated to the
Southern Ocean as a whole.
The three nutrient datasets each have unique properties. Silicate is taken up by a large, and very
important, class of phytoplankton Ždiatoms., so that
primary production by phytoplankton which do not
sequester silicon is not registered. On the other hand,
it is likely that most of the biogenically-fixed silicon
is not recycled within the euphotic zone ŽTreguer
et
´
al., 1995.. Phosphate is taken up by all phytoplankton, but recycling may result in nutrient drawdown
underestimating primary production. We have used
these two properties to evaluate the utilisation of
nitrate, where it is clear that nitrate is not the only
source of nitrogen for primary production. As is
shown by the variation in primary production estimates for nitrate uptake, the degree of recycling has
major impact—greater levels of recycling imply increased primary production for a given nutrient
drawdown. From this point of view, our estimates of
primary production may be low, and perhaps closer
to new than to recycled production.
The question of the representativeness of the data
is easier to address. Most of the sites are neritic or
close to islands, or are ice-edge studies. These are
likely to be in the higher band of primary productivity, albeit in areas where export production is more
important than in other areas of the Southern Ocean,
so that recycling is likely to be less significant.
Overall, we would suggest that our nutrient deficit
data will overestimate the overall production in the
Southern Ocean.
Examining the top and bottom of the range of
estimates of Southern Ocean primary production
284
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
suggests extreme values for nutrient drawdown. Thus
for a total annual primary production of 3.5 Gtonne
C yeary1 , drawdown for silicate, phosphate and
nitrate Ž f-ratio s 0.75. would be expected to be 40,
1.5 and 18 mmol my3 respectively—all values which
are significantly higher than observations for sites
where primary production and hence nutrient drawdown would be high. At the bottom end of the range
of primary production estimates Žabout 1.2 Gtonne C
yeary1 ., the corresponding nutrient deficits would be
around 10, 0.4 and 5 mmol my3 —at the lower limit
of the observed data.
4.3. A consensus between the two estimates
We regard the fact that two contrasting and independent methods present similar results supports our
estimated value for ASO primary production. Despite the fact that we have used the higher estimate
of top predator carbon demand to run our trophic
model, the model itself is likely to underestimate
primary production because it contains no explicit
losses other than those in the transfer between trophic
compartments. By contrast, the estimation of primary
production based on nutrient drawdown is likely to
oÕerestimate primary production, because the studies
used are biased towards more productive neritic and
ice-edge systems. Therefore, the two methods are
likely to be biased in opposite directions, but both
indicate similar values which suggests to us that our
best estimate of ASO primary production is correct.
We can ask whether there is a combination of
circumstances which might lead to both methods
underestimating ASO primary production. The higher
values Ž) 2.5 Gtonne C yeary1 . in the current range
of estimates imply food web dynamics and nutrient
drawdown which appear to differ strongly from observations. For our value of primary production based
on top predator carbon demand to underestimate
primary production, either the food web has to be
very much less efficient than we suggest, or the
percentage of photosynthetically-fixed carbon which
‘escapes’ from the food web must be high. The
proportion of annual primary production which is
exported Žcrudely but not technically equivalent to
that which does not pass through the food web. is
normally considered to be no more that 10%, so that
we appear to be correct in assuming that such losses
can be accommodated within errors in our values for
transfer efficiencies. For carbon export to represent
an addition to estimated primary production to effectively add 1 Gtonne C yeary1 to ASO primary
production, export needs to rise to about 40% in our
model. At the same time, the documented nutrient
drawdown must ‘hide’ a large part of the primary
production. This can only come about if this is being
fuelled by nutrients which are not included in our
calculations. It would certainly imply a high, but
perhaps not improbable proportion of primary production carried out by nonsiliceous phytoplankton. It
would suggest that 40% of the phosphorus is recycled, and that uptake f-ratio for nitrogen should
average 0.45 for the Southern Ocean as a whole. We
do not have firm data to refute any part of this
scenario, but the possibility of 40% carbon export
appears to merit urgent attention! On this basis, we
would suggest that the primary production in the
Southern Ocean south of the Subantarctic Front approximates to our estimate of 1.7 Gtonne C yeary1 ,
or an averaged areal primary production rate of
around 30–40 g C my2 yeary1 .
Finally, we indicated earlier that we were not
approaching this problem from the specific point of
view of how much primary production is respired by
air-breathing, endotherm predators Žcf. Huntley et
al., 1991; Banse, 1995.. However, our estimate of
carbon demand for the entire suite of such predators
in the Southern Ocean does allow us to provide a
limit for the amount of carbon respired. The maximum value would be 96.5% Žbased on transfer efficiency and diet. of the upper bound of carbon demand, or 28.95 Mtonne C yeary1 . This is slightly
under 2% of our best estimate for total annual primary production in the Southern Ocean, or 0.8% of
the primary production value used by Huntley et al.
Ž1991., and agrees with the broad conclusion reached
by Banse Ž1995., although van Franneker et al.
Ž1997. suggest that the value might be even lower at
0.3–0.6%. Our value is very much less than the CO 2
efflux of up to 860 Mtonne C yeary1 , which is
implied by the most extreme case presented by Huntley et al. Ž1991., where 20–25% of primary production of 3.5 Gtonne C yeary1 was respired by endotherm predators. We consider that examination of
the partition of carbon in the Southern Ocean food
web is a key activity for understanding the biogeo-
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
chemical carbon cycle, but that the specific problem
of the role of endotherm predators as a conduit from
aquatic primary production to atmospheric CO 2 is
best addressed by quantifying carbon demand at the
top of the food web.
Acknowledgements
We are grateful to several of our colleagues for
discussion of aspects of this paper, especially Ray
Leakey, Paul Rodhouse and Martin White. The comments by the two referees were most helpful, and
suggested several improvements to the original which
we hope we have implemented to their satisfaction.
Appendix A. A carbon budget for crabeater seals
The crabeater seal Ž Lobodon carcinophagus. is
the most abundant pinniped species in the world and
is a dominant member of the top predator community of the Southern Ocean. It is endemic to the
Southern Ocean, and its diet consists mainly of krill.
The carbon budget for crabeater seals has been assembled as follows.
A.1. Population size
The most recent estimate of crabeater seal population size was given by Erickson and Hanson Ž1990..
Using information from surveys carried out between
1968 and 1983, they concluded that the size of the
crabeater seal population was most likely to be 11–12
million with a minimum of 7 million, which is lower
than previous estimates of somewhere between 15
and 30 million ŽLaws, 1984.. Since the size of the
crabeater seal population is critical to estimates of
carbon flux, estimates are made for minimum Ž7
million., median Ž12 million. and maximum Ž15
million. population sizes.
A.2. Age-specific biomass
The age-specific biomass Žtotal biomass for each
year class. has been estimated from the product of
age-specific individual mass and the number of individuals in each one-year age class. Age-specific
mass was estimated from growth curves fitted to
285
mass-at-age data from crabeater seals shot for dog
food between 1967 and 1977 in the area of Marguerite Bay, Antarctica Peninsula ŽBritish Antarctic
Survey unpublished data.. The von Bertalanffy
growth curve Žvon Bertalanffy, 1938. was used to
smooth and summarise these data. Information about
population age structure was obtained from Siler
survivorship functions fitted to crabeater age structures by Boveng Ž1993.. This gave the proportion of
individuals in each age class and the product of these
proportions with the total population size gave the
age-specific biomass.
A.3. Carbon sequestered in seal biomass
The proportion of fat and protein in crabeater
seals of each age-specific mass was calculated from
the relationships in the carcasses of grey seals
Ž Halichoerus grypus: Reilly and Fedak, 1990. and
ringed seals Ž Phoca hispida: Stirling and McEwan,
1975.. Water content was assumed to be 0.52 body
fresh mass, based on data from female southern
elephant seals under a wide range of feeding conditions and body fat content ŽBoyd et al., 1993.. Green
et al. Ž1993. found slightly higher water contents in
preweaning crabeater seal pups but their measurement projected to the time of weaning supports the
view that adult water contents are likely to lie between 0.50 and 0.55, and these values were also used
in the calculations.
Estimation of the mass of carbon sequestered in
seal biomass was made from the product of the
carcass composition by mass and the proportion by
mass of carbon in protein Ž0.529. and fat Ž0.776.
ŽGnaiger and Bitterlich, 1984.. The annual requirement for carbon in the growth of seal tissue was
estimated from the sum of the annual growth increments between years. Since pups are dependent upon
maternal resources up to weaning, growth in advance
of weaning was included as part of the net flux based
upon a mass of pups at weaning of 77 to 130 kg with
a mean of 97.6 kg ŽGreen et al., 1993..
Apart from the biomass increase due to pregnancy, seasonal changes in biomass were not included in this analysis because these were assumed
to be time lags between the assimilation and oxidation of food which were smoothed out within years.
The costs of storage were also assumed to be insignificant.
286
J. Priddle et al.r Journal of Marine Systems 17 (1998) 275–288
A.4. Carbon flux due to metabolism
Metabolic rate has not been determined for
crabeater seals but studies of metabolic rate in other
pinnipeds have shown sufficient consistency across
species to suggest that they may also be applicable to
crabeater seals after controlling for differences in
body mass. BMR was assumed to vary with mass
Ž M . according to the equation where metabolic rate
s 293Ž M . 0.75 ŽKleiber, 1961.. Although this equation strictly only applies to interspecific comparisons, it may be accepted as a conservative view of
the degree to which body mass affects metabolic rate
within a single species ŽLindstedt and Boyce, 1985..
Most studies have found metabolic rates for pinnipeds when ashore of 2 to 3.3 times the BMR
predicted from mass ŽKleiber, 1961.. Based on these
measurements, an average metabolic rate of crabeater
seals while hauled out was set at 2.8 times BMR
with a minimum of 2.0 and a maximum of 3.3.
When at sea, measurements of metabolic rate vary
from 4.4 to 6.9 times BMR, although it is believed
that lower metabolic rates may be possible for phocid pinnipeds Že.g., Ponganis et al., 1993.. An average at-sea metabolic rate of 4 times BMR was used
in our calculations, with 2.5 and 5 times BMR as the
upper and lower extremes. The average metabolic
rate chosen here also corresponds well with that
predicted for animals the size of crabeater seals for
the allometric relationship between mass and field
metabolic rate given by Nagy Ž1987..
The proportion of time spent in and out of the
water was calculated from the frequency of haulout
in each hour of the day given by Bengtson and
Stewart Ž1992. and supported by Nordøy et al.
Ž1995.. Since crabeater seals are known to feed
almost exclusively on krill Ž Euphausia superba.
ŽLaws, 1984. the ratio of lipid and protein in krill
was used to estimate the composition of the metabolic
substrate. Clarke Ž1980. showed that, on average,
krill contain 4% lipid and 10.5% protein, and using
energy densities of lipid of 39.34 kJ gy1 and protein
of 18.0 kJ gy1 , the percentage of energy from lipid
was:
El s Ž 39.34 = 4 . r Ž 39.34 = 4 . q Ž 18.0 = 10.5 .
s 45.4%
and it follows that metabolic energy derived from
protein was 53.6% of the total budget. The carbon
contents of lipid and protein were used to estimate
the carbon flux due to metabolism Žsee above;
Gnaiger and Bitterlich, 1984..
A.5. Carbon flux due to reproduction
The calculation of the carbon flux due to reproduction assumed that only animals greater than age-3
years breed and that there was an annual pregnancy
rate of 0.87 ŽBengtson and Siniff, 1981; Laws, 1984..
It also assumed that materials transferred from mothers to pups and which were assimilated into pup
growth were accounted for in the growth of the
0 q age class. This analysis concentrated upon the
metabolic costs of lactation, which has been estimated as 14.6 and 18.1 MJ dayy1 for grey and
northern elephant seals Ž Mirounga angustirostris.
respectively ŽAnderson and Fedak, 1987; Costa et
al., 1986.. Given that this is likely to vary with body
size and that crabeater seals have a lactation duration
midway between that of grey and elephant seals
ŽGreen et al., 1993., then a lactation energy expenditure of 17 MJ dayy1 was used for crabeater seals,
with lower and upper extremes of 15 and 19 MJ
dayy1 .
Carbon flux due to reproduction in males was
assumed not to be significantly greater than normal
as suggested by studies of metabolic rate in male
pinnipeds during the breeding season ŽBoyd and
Duck, 1991..
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