Download Plankton trophodynamics at the subtropical convergence, Southern

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Plankton trophodynamics at the
subtropical convergence, Southern
Ocean
NICOLE B. RICHOUX* AND P. WILLIAM FRONEMAN
DEPARTMENT OF ZOOLOGY AND ENTOMOLOGY, RHODES UNIVERSITY, GRAHAMSTOWN
6140, SOUTH AFRICA
*CORRESPONDING AUTHOR: [email protected]
Received March 29, 2009; accepted in principle May 23, 2009; accepted for publication June 10, 2009; published online 3 July, 2009
Corresponding editor: Mark J. Gibbons
Stable isotope signatures (d13C, d15N) in zooplankton tissues and particulate organic matter
(POM) were determined to assess regional differences in the trophodynamics of zooplankton communities between 38 and 438S, where the cool nutrient-rich subantarctic waters of the Southern
Ocean meet the warm nutrient-poor subtropical waters of the southwest Indian Ocean at the subtropical convergence (STC). Significantly enriched values of d15N were noted in populations of all
major zooplankton groups inhabiting the warm and saline water mass north of the STC
(maximum surface temperature 218C), including the euphausiids, salps, amphipods, copepods,
ostracods, pyrosomes, pteropods and chaetognaths, compared with those in the cool, less saline
southern water mass (minimum surface temperature 118C). Similar patterns of d15N in POM
collected throughout the region suggest that the large changes in zooplankton d15N values across
the frontal region are driven by variations in the phytoplankton communities. The differing trophodynamics in communities north and south of the STC provide compelling evidence of distinct
bottom-up effects on planktonic food webs which have important implications in the determination
of trophic positions and motility of plankton and higher consumers using d15N signatures.
Although expected, similar latitudinal variations in d13C signatures were not found.
I N T RO D U C T I O N
The subtropical convergence (STC) is one of the major
oceanic fronts and represents the northern border of
the Southern Ocean (Longhurst, 1998). In this zone,
the cool nutrient-rich subantarctic water mass meets
and mixes with the warm nutrient-poor subtropical
water mass, resulting in strong latitudinal gradients in
the physical parameters (Longhurst, 1998). South of
Africa, the STC is strongly defined and highly dynamic,
its location determined by the position of the retroflection of the Agulhas Current and the Agulhas Return
Current (Longhurst, 1998; Lutjeharms, 2006). Despite
being an area of strong downwelling, this convergence
zone is characterized by elevated biological activity and
is thought to play an important role in atmospheric
carbon sequestration (Llido et al., 2005). Furthermore,
nitrate concentrations form sharp gradients from
,0.1 mM L21 north of the STC to 27 mM L21 in the
south (Lutjeharms et al., 1985; Altabet and Francois,
1994), with low iron availability representing the proximal control on phytoplankton production in the
Southern Ocean (Takeda, 1998). In seeming contrast to
the macronutrient gradients (apart from silicate),
enhanced chlorophyll biomass is routinely observed at
or just north of the STC (Lutjeharms et al., 1985), probably induced by the increased vertical stratification and
stability created by the passage of the colder,
nutrient-rich subantarctic water sliding below the subtropical water (Lutjeharms et al., 1985; Weeks and
Shillington, 1996). The enhanced productivity occurs in
intermittent pulses primarily in spring and summer
(Llido et al., 2005), and the combination of hydrological,
physical and biogeochemical processes occurring within
this region creates a unique biological habitat and
doi:10.1093/plankt/fbp054, available online at www.plankt.oxfordjournals.org
# The Author 2009. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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planktonic community (Barange et al., 1998; Longhurst,
1998). In addition to the enhanced biological production measured north of the STC, phytoplankton are
continuously advected into the region with the converging currents, thus further amplifying the chlorophyll
biomass (Lutjeharms et al., 1985). Although the STC is
considered as a biogeographical boundary to many
organisms (Barange et al., 1998 and references therein;
Longhurst, 1998) and an important contributor to total
annual production in the Southern Ocean (Lutjeharms
et al., 1985), the trophic ecology and energetics of the
resident plankton remain poorly understood (Pakhomov
and Perissinotto, 1997). Regions of the STC not in close
proximity of continents or islands are particularly
undersampled with respect to planktonic food webs.
Trophic relationships are notoriously difficult to decipher in aquatic environments (Jacob et al., 2006).
Organisms of interest are typically very small, remote
and/or behaviorally complex, and planktonic species in
particular can exhibit a high degree of feeding plasticity
in response to spatial and temporal variability in the
nature and availability of food (Mayzaud et al., 2002).
Furthermore, grazing and biochemical studies have provided ample evidence for the importance of omnivory
in planktonic food webs (Pakhomov and Perissinotto,
1997; Stevens et al., 2004), whereas traditional gut
pigment techniques are not capable of resolving the
contribution from non-photosynthetic food sources
(Mayzaud et al., 2002). As a result, the use of techniques
such as stable isotope ratios and fatty acid profiles are
increasingly being utilized in ecological studies
(Petursdottir et al., 2008). These tools provide a timeintegrated perspective of the assimilated feeding history
of an organism or population (Michener and Schell,
1994). The premise of carbon isotope tracers is that
primary producers fractionate their carbon sources of
13
C and 12C to differing degrees ( preferentially fix the
lighter isotope), and the degree of fractionation of this
ratio from producers to consumers is small (,1‰ relative to diet; Fry and Sherr, 1984). As a result, 13C:12C
ratios are used to match consumers with their diet (Fry
and Sherr, 1984; Michener and Schell, 1994), and
primary producers with their nutrient sources or with
specific water masses (Goericke and Fry, 1994).
Similarly, 15N:14N ratios in consumers differ from their
diet by 3 – 4‰, typically from fractionation during
assimilation and protein synthesis in addition to preferential excretion of the lighter endogenous isotope
(Minagawa and Wada, 1984). Therefore, d15N is a
useful indicator for the trophic level of a consumer
population.
Particulate organic matter (POM) in the southern
hemisphere shows latitudinal gradients in d13C and
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d15N, with pronounced changes reported to occur
across the STC (Altabet and Francois, 1994; Goericke
and Fry, 1994). Francois et al. (Francois et al., 1993)
found a distinct gradient in d13CPOM in a transect crossing the STC near 688E, with depleted values associated
with the cold southern and [CO2(aq)]-rich water mass
relative to more enriched values in the warm northern
and low [CO2(aq)] water mass. Gradients or regional
differences in d13C or d15N imply that phytoplankton
growth and nutrient supply are important factors in
structuring isotopic regimes in the marine environment
(Altabet and Francois, 1994; Schell et al., 1998).
Consumers of POM in any given region are ultimately
affected by the d15N of primary producers and their
physiological status (Minagawa and Wada, 1984).
As global climate change has the potential to cause
major shifts in the location, strength and physical and
biological properties of the STC (Bargagli, 2005), it is
important that we determine the potential effects of
such changes on the biological communities of the
region. Any changes in the food quality or availability
for the dominant species or in the trophic relationships
among producers and consumers may have implications
for top consumers such as fish, birds and mammals and
the assessment of their diets using stable isotopes. As
such, the aim of this study was to determine whether
the strong latitudinal variability in physico-chemical
parameters across the convergence zone influences the
isotopic composition in the planktonic component at
the STC southeast of Africa. We hypothesized that communities inhabiting the nutrient-poor but more productive northern water mass in the subtropical zone
would have food webs isotopically enriched in both 13C
and 15N relative to those in the high nutrient/low production southern water mass. Successful characterization of food webs in the STC will provide an excellent
framework for future studies in Southern Ocean trophic
ecology and will facilitate the assessment of trophic
levels and habitat usage of consumers.
METHOD
Sample collection
Biological and physical data were collected from aboard
the S.A. Agulhas during Voyage 135 from Cape Town,
South Africa, to the Prince Edward Islands in April
2007. Six transects across the STC were completed
between 38 and 438S, and 38 and 428E (Fig. 1). Physical
data were collected by a research team from the
University of Cape Town and will be documented in
more detail elsewhere. Briefly, vertical profiles of salinity
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Fig. 1. Survey area in the STC region during Voyage 135 of the
S.A. Agulhas, April 2007, relative to Africa. Enlargement shows the six
transects and 48 biological sampling stations, in the order of
collection, superimposed on sea surface temperature isotherms. The
thickened 148C isotherm represents the surface division of the STC
between northern and southern water masses.
and temperature were sampled to a depth of 1500 m at
48 stations using a Seabird SBE 9/11. Dissolved oxygen
and macronutrient concentrations (nitrate, nitrite, silicate
and phosphate) were determined using titration and
standard colorimetric analyses, respectively, from water
samples collected in Niskin bottles at 10 depths between
25 and 1500 m at all 48 stations.
Total chlorophyll a (Chl a) concentrations were determined from water samples collected in Niskin bottles
between 25 and 150 m at all 48 stations, and sizefractionated Chl a (.20, 2–20 and ,2 mm) concentrations were determined from hand-collected surface
water. All Chl a extractions and concentration measurements were completed onboard the ship using 90%
acetone and a standard fluorometric procedure, respectively (Parsons et al., 1984; Turner 10AU fluorometer).
Aliquots of 2–4.4 L of surface water (for the determination of POM isotopic ratios) were pre-screened through
a 200 mm nitex mesh, filtered onto pre-ignited GF/F
Whatman glass fiber filters (47 mm filters; ,5 bar
vacuum) and immediately frozen. Zooplankton were collected from 200 m (night) or 300 m (day) to surface using
a Bongo net (200 mm mesh) fitted with flow and depth
meters. Zooplankton samples were roughly sorted, transferred to bottles and frozen for the duration of the voyage.
Sample treatment
Upon return to the laboratory, frozen plankton samples
were defrosted, sorted and measured on ice under a dissecting microscope. Several hundreds of the smallest
organisms (e.g. copepods) were pooled per sample to
obtain an adequate signal, whereas larger animals were
processed as individuals. Euphausiids, amphipods and
tunicates were identified to species using taxonomic keys
(Baker et al., 1990; Esnal, 1999; Esnal and Daponte,
1999; Gibbons et al., 1999; Vinogradov, 1999), whereas
most other taxa were placed into broad taxonomic
groupings. One additional category of euphausiid furcilia was created from surplus animals in abundant
samples from the north. Copepods were sorted into two
categories based on size: large (.3 mm length) or small
(,3 mm length). Small zooplankters were vacuum filtered onto GF/C filters. All filters and animal samples
were visually inspected for contaminant material,
placed in pre-ignited foil envelopes, lyophilized for 24 h
and either shredded into small pieces (filters) or homogenized using a mortar and pestle (animals). A portion
of the crustacean (all species), gastropod and water
samples was treated with 1 M L21 HCL to eliminate
carbonates, rinsed with distilled water, dried and
re-homogenized. The only group to show significant
differences in d13C before and after acidification were
the pteropods; therefore, data from acidified pteropod
samples were used for the d13C measurements.
Samples were analyzed at the Stable Light Isotope
Laboratory in the Archaeology Department, University
of Cape Town, on a Thermo Finnigan Delta XP Plus
mass spectrometer interfaced with a Conflo III device
to a Thermo Flash EA 1112 elemental analyzer.
Results for carbon and nitrogen are reported relative to
v-PDB and atmospheric N2, respectively. The raw data
were corrected using standards of known isotopic composition (sucrose, lentil and valine) and then normalized
against the international standards. The analytical precision of the instruments was within +0.2‰ (1 standard deviation). Isotope ratios are expressed in the d
notation: d(‰) ¼ (Rsample/Rstandard 2 1)1000, where
d(‰) is d13C or d15N and Rsample and Rstandard are the
13
C/12C or 15N/14N ratios of the sample and standard,
respectively.
Calculations and statistics
Given that our samples were not subjected to lipid
extraction, we used a model from Post et al. (Post et al.,
2007): d13Cnormalized ¼ d13Cuntreated 2 3.32 þ 0.99 (C:N),
derived from aquatic organisms to normalize d13C
values in all animal samples. These authors found C:N
ratio to be a successful predictor of animal total lipid
content, and lipid content an appropriate predictor of
the difference in d13C between lipid-extracted and
untreated samples. As such, this equation provided
d13C values normalized for variable lipid content
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among individuals, results that would be comparable to
the d13C signatures obtained had lipids been extracted
(Post et al., 2007).
A consumer has a trophic position defined by
the relative proportions of different prey in its diet.
To calculate trophic positions of consumers, we
followed the method outlined in Vander Zanden and
Rasmussen (Vander Zanden and Rasmussen, 1999):
Trophic positionconsumer ¼2 þ ((d15Nconsumer 2 d15Nsalps)
(Dd15N)21), where d15Nconsumer is the d15N value for a
given consumer, d15Nsalps represents the reference baseline value at trophic position 2 within our food web and
Dd15N is the mean trophic fractionation of 3.4‰
between adjacent trophic levels. As d15N of POM did
not represent a pure phytoplankton signature in our
study, salps were used as the baseline of the food web
and assigned a trophic level of 2 ( primary consumer
position). A trophic level for each sample/individual
was derived using this method, allowing for calculations
of mean and standard deviation per sample type.
For the majority of species or sample types, we did not
collect a sufficient number of individuals to include replicate samples from every location on our transect grid. As
a result, similar sample types collected from each region
(north, south and middle) represented replicate samples
from that region, and the precise sample location was not
included in subsequent statistical analyses. Stable isotope
data were statistically analyzed with general linear models
(GLMs) and standard linear regressions using Systat 12
and SigmaPlot 10, respectively. Residual analysis was
completed with each model to ensure that the assumption
of independent error terms was met. Although the terminology “explanatory variable” is used to describe the
variables tested in the models, significant results do not
imply causative relationships.
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south. The sharp transition zone of the STC was
expressed clearly to 200 m depth (Froneman et al.,
2007). Surface oxygen varied between the northern subtropical (5 mL L21) and the southern subantarctic
(.6.8 mL L21) water masses. A companion study
showed that total surface Chl a concentrations ranged
between 0.03 and 0.42 mg L21 and were dominated by
the picophytoplankton (Daly and Froneman, in press).
Chl a values integrated from 0 to 150 m depth ranged
from 12.8 to 40.1 mg m22, although they did not
change significantly with temperature and salinity
(Froneman et al., 2007). Of the four nutrients measured
(nitrite, nitrate, silicate and phosphate), nitrate concentrations in the top 150 m showed distinct increases from
north to south of the STC (Fig. 2A), whereas significant
changes were not observed at depths down to 1500 m
(Fig. 2B).
R E S U LT S
Physical data
Sea surface temperature clearly identified the STC
between 41 and 428S (Fig. 1). Sample sites north of the
STC were defined as those 35.1 psu and 178C,
south of the STC as those 34.4 psu and 128C, and
the “middle” zone of transition was demarcated by the
region of 34.8 psu between 13 and 168C. These three
broad geographic zones of the STC (north, middle and
south) were used in all figures to aid interpretation only,
whereas salinity and temperature data were included
in statistical models as continuous variables so that
changes in these physical variables were used to represent the different physical properties from north to
Fig. 2. Nutrient concentrations (mM L21) from the first transect
of the research cruise; (A) depth-integrated mean + SD of five
measurements taken between 25 and 150 m depth; (B) depthintegrated mean + SD of five measurements taken between 500 and
1500 m depth (nutrient concentrations along the remaining five
transects showed similar patterns and are not shown). Arrows depict
2
the middle site along the transect. Nitrite¼NO2
2 , nitrate¼NO3 ,
32
silicate¼SiO42
,
and
phosphate¼PO
.
4
4
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Particulate organic matter
Effects of several explanatory variables on the response
variables d13CPOM and d15NPOM were tested using
exploratory GLMs: mean seawater nitrate concentration
(25– 150 m), surface salinity, surface temperature, integrated Chl a biomass (surface to 150 m), acid/no acid
treatment, C:N ratio, mean seawater oxygen concentration (surface to 150 m) and d15NPOM or d13CPOM.
All potential explanatory variables showed no significant
influence on the dependent variable d15NPOM (P .
0.05), with the sole exception of nitrate concentration
(F ¼ 10.07,24, R 2 ¼ 0.75, P , 0.05). An exponential
model was fitted to this smaller data set (nitrate concentrations and d15NPOM) to further describe the relationship between the two variables, and the elevated nitrate
concentrations and d15N-depleted signatures associated
with seawater POM south of the STC separated clearly
from the d15N-enriched POM signatures associated
with northern seawater (Fig. 3; outlier at 3.5 mM L21
included in the analysis). All potential explanatory variables showed no significant effect on the dependent
variable d13CPOM (P . 0.05), with the exception of C:N
ratio (F ¼ 10.87,24, R 2 ¼ 0.76, P , 0.001; Fig. 4). No
distinctions of d13CPOM signatures were apparent
between northern and southern regions.
Euphausiids
Fig. 4. POM. Signatures of d13C (‰) relative to C:N ratio (linear
regression).
response variables d13Ceuphausiid and d15Neuphausiid were
tested with exploratory GLMs: surface salinity, surface
temperature, integrated Chl a biomass (surface to
150 m), body length (mm), species, acid/no acid treatment, C:N ratio, d15NPOM, and d15Neuphausiid or
d13Ceuphausiid. The final models used to explain 77 and
54% of the variability in d15N and d13C, respectively, in
euphausiids were:
d15 Neuphausiid ¼ bo þ b1 ðsalinityÞ þ b2 ðlengthÞ
Nine species of euphausiid were analyzed, seven of
them found both north and south of the STC (Table I;
Fig. 5). Effects of several explanatory variables on the
þ b3 ðd13 Ceuphausiid Þ þ b4 ðd13 Ceuphausiid
salinityÞ þ b5 ðd13 Ceuphausiid lengthÞ þ 1
ð1Þ
13
d Ceuphausiid ¼ bo þ b1 ðlengthÞ þ b2 ðd15 Neuphausiid Þ
þ b3 ðsalinity lengthÞ þ 1
Fig. 3. POM. Signatures of d15N (‰) relative to depth-integrated
mean nitrate concentration (mM L21) in seawater from 25 to 150 m
depth. The curve represents the exponential relationship between the
two variables, and transformation using ln(nitrate concentration) did
not produce a linear relationship between the two variables.
ð2Þ
where d15Neuphausiid and d13Ceuphausiid are dependent
variables; bo, the grand mean of population; b1 – b5,
true means due to explanatory variables salinity, body
length, d13Ceuphausiid, d15Neuphausiid and interactions;
and e the error component. All explanatory variables in
both models were significant at P , 0.05 (d15Neuphausiid
F ¼ 45.35,68, R 2 ¼ 0.77; d13Ceuphausiid F ¼ 15.65,68,
R 2 ¼ 0.54), whereas all other potential explanatory
variables were removed as insignificant (P . 0.05).
These results from GLM (1) clearly showed that region
(north versus south, as represented by changes in salinity), body size (as represented by body length) and
d13Ceuphausiid each contribute significantly to the variation in d15Neuphausiid in addition to the two interaction
terms. In contrast, the results from GLM (2) showed
that only body size, d15Neuphausiid and one interaction
term contributed to the variation in d13Ceuphausiid,
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Table I: Zooplankton and POM signatures of d13C and d15N (mean + SD; ‰) in the north, middle
and south of the STC
North
Species or taxonomic
category
POM
Surface seawater
Euphausiacea Euphausia similis
Euphausia similis armata
Euphausia spinifera
Euphausia longirostris
Euphausia recurva
Nematoscelis megalops
Stylocheiron abbreviatum
Thysanoessa longicaudata
Thysanopoda pectinata
Euphausiid furcilia
Amphipoda
Phronima sedentaria
Themisto gaudichaudii
Vibilia armata
Copepoda
Large copepods
Small copepods
Decapoda
Penaeidean shrimps
Sergestoid shrimps
Mysidacea
Siriella thompsoni
Large mysids
Pyrosomatida Pyrosoma atlanticum
Salpida
Salpa thompsoni
Chaetognatha Chaetognaths
Ostracoda
Ostracods
Pteropoda
Pteropods
Cnidaria
Jellyfish
Osteichthyes Myctophid larvae
Middle
South
d 15N–d
Length range
(mm)
d 13C
10 –23
10 –25
24 –25
8 – 27
10 –17
15 –22
7 – 26
10 –15
16 –32
10 –11
14 –28
11 –26
4–9
.3
,3
30 –70
18 –35
10 –11
32 –37
75 –280
25 –40
13 –20
1 –4
2 –10
2 –20
15 –65
223.2 + 0.5 5.5 + 0.8 222.1 + 0.6 4.0 + 1.1 222.5 + 0.8
2.5 + 0.9 3.0
219.6 + 0.4 8.9 + 0.6 219.1
5.2
219.4 + 0.4
4.1 + 0.8 4.8
218.6 + 0.4 9.6 + 1.2 218.8 + 1.1 6.4 + 1.3 218.8 + 0.2
6.1 + 0.3 3.5
217.8
9.8
218.6
10.3
218.7 + 0.3
6.5 + 0.3 3.3
218.9 + 0.5 9.9 + 0.8
–
–
218.7 + 0.2
6.1 + 1.7 3.8
219.6 + 0.8 8.1 + 0.5
–
–
–
–
219.2 + 0.5
5.8 + 0.6 3.5
219.0 + 0.3 9.3 + 0.7 219.0
7.4
219.7 + 0.2 9.8 + 1.7
–
–
219.6
6.6
3.2
219.8 + 0.3 8.4 + 1.0 219.3
5.2
219.5
4.1
4.3
219.6
9.5
–
–
–
–
220.0 + 0.5 7.9 + 1.0
–
–
–
–
219.4 + 1.0 6.5 + 1.8
–
–
–
–
219.4 + 0.4 4.5 + 0.3 218.3
2.6
219.0 + 0.2
3.4 + 0.4 1.1
219.1 + 0.7 6.1 + 0.8 217.8
3.8
218.5 + 1.0
3.7 + 2.0 2.4
219.7 + 0.5 7.6 + 0.7 218.4 + 0.7 5.7 + 1.9 218.5 + 0.2
4.5 + 1.3 3.1
219.6 + 0.3 6.3 + 1.1 219.1 + 0.1 3.0 + 0.0 217.5 + 0.2
0.2 + 0.2 6.1
218.9 + 0.4 8.2 + 1.5
–
–
–
–
219.7 + 0.8 9.1 + 2.0 219.1
9.8
–
–
219.8 + 0.9 7.3 + 0.6
–
–
–
–
218.6
10.2
–
–
218.6 + 0.7
7.8 + 2.1 2.4
219.8 + 0.3 6.8 + 1.5 220.2 + 0.3 3.7 + 1.0 219.7 + 0.2
2.5 + 0.1 4.3
218.7 + 0.2 3.9 + 0.7
–
–
218.1 + 0.2
0.4 + 0.7 3.5
4.4 + 0.1 5.7
219.1 + 0.3 10.1 + 1.2 218.5
10.8
219.6 + 1.1
219.1 + 0.9 6.0 + 0.5 217.8
3.3
220.0
20.3
6.3
220.3 + 0.5 5.6 + 0.2 220.7
4.1
220.6
0.4 + 0.3 5.2
218.3 + 0.5 7.1 + 0.6
–
–
220.5 + 0.4
5.7 + 0.1 1.4
219.5 + 0.3 8.5 + 1.3
–
–
220.2
4.2
4.3
d 15N
d 13C
d 15N
d 13C
d 15N
d15N– d ¼ mean change in d15N (‰) between north and south. d13C values of fauna were normalized for variable lipid contents using C:N ratios. Refer
to Table II for sample sizes.
therefore no regional differences (i.e. north versus south)
were apparent.
The influential explanatory variables from GLMs (1)
and (2) were examined further using graphics and
regressions to explore the nature of the associations. A
clear separation of the euphausiid communities from
north to south was related to changes in salinity,
whereas carbon signatures showed no significant correlations with any physical properties of the seawater
(Figs 4 – 6). Euphausiid d15N and d13C positively and
linearly correlated with each other in the north and the
south, whereas euphausiids from the middle STC were
variable (Fig. 5). Furthermore, body length was positively and linearly correlated with both d15N and d13C
(Fig. 6), the marked differences in d15N from north to
south resulting in similar slopes but different intercepts
in linear regression models (Fig. 6A).
Despite large standard deviations associated with
d13C (Fig. 5), intra-species coefficients of variation (CV)
were much larger in d15N (CV range d15N ¼ 3.8– 27.1;
CV
range
d13C ¼ 1.08– 4.1).
Signatures
of
15
d Neuphausiid north of the STC (mean 8.9 + 1.1‰)
were on average 3.4‰ more enriched than those in the
south (mean 5.5 + 1.4‰), with euphausiids from the
middle region falling somewhere between (mean 6.8 +
1.9‰; Table I, Figs 3, 5 and 6).
Other fauna
In addition to the nine euphausiids, three species of
amphipod and a variety of broad taxon groups were
analysed (Table I). This list of plankton is by no means
a complete account of the taxa found in the STC
region, but represents those organisms selected for the
purposes of stable isotope analysis. The chaetognath
group was composed primarily of Eukrohnia hamata,
Sagitta gazellae and S. zetesios. The large size class of
copepods was comprised primarily of Calanus simillimus
and Pleuromamma abdominalis, and the small size class
composed of Clausocalanus breviceps and Oncaea conifera. In
situ injestion rates (determined using a gut pigment
method) for these copepod species inhabiting the STC
during a companion study indicated similar feeding
habits among species within each size class (Daly and
Froneman, in press). The pteropod group was dominated
by Limacina retroversa but included numerous
larger specimens from the genera Clio and Cavolinia [for a
more complete account of meso- and macrozooplankton
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Fig. 5. Signatures of d13C and d15N (mean + SD; ‰) in euphausiid
species collected in the north (N), middle (M) and south (S) of the
STC. d13C values have been normalized for variable lipid contents
using C:N ratios. Regression lines in the north and south were created
from raw data and do not include middle sites.
species collected during the cruise refer to Sterley
(Sterley, 2008) and Daly and Froneman (Daly and
Froneman, in press)].
All taxa showed significant enrichment in d15N in the
north relative to the south, with samples taken from the
middle region often having intermediate values
(Table I; Fig. 7). Mean differences of d15N from north
to south within each species or taxonomic group ranged
from 1.1‰ in the amphipod Themisto gaudichaudii to
6.3‰ in the ostracods. In contrast, no detectable trend
from north to south was observed in d13C of plankton
(Table I; Fig. 8). Exploratory GLMs were fitted to d13C
and d15N signatures of amphipods and copepods using
the potential explanatory variables listed for the
euphausiids. Significant terms in the d15Namphipod
model included salinity, d13Camphipod, body length and
species [F (for the four terms, respectively) ¼ 38.8, 8.3,
14.0, 7.85,29, R 2 ¼ 0.85, P , 0.01]. Significant terms in
the d13Camphipod model included only salinity and
d13Namphipod (F ¼ 7.52,32, R 2 ¼ 0.57, P , 0.01). Similar
influential explanatory variables were identified in a
d15Ncopepod GLM (salinity, temperature, d13Ccopepod and
body length; F ¼ 51.14,30, R 2 ¼ 0.87, P , 0.01) and a
d13Ccopepod GLM (salinity, d15Ncopepod and temperature;
F ¼ 18.53,31, R 2 ¼ 0.64, P , 0.01).
Fig. 6. Euphausiid signatures of (A) d15N (‰; north: d15Neuphausiid ¼
n ¼ 45,
P , 0.001;
south:
0.13(length)þ6.78,
R 2 ¼ 0.30,
d15Neuphausiid ¼ 0.16(length)þ2.31, R 2 ¼ 0.27, n ¼ 23, P , 0.05) and
(B) d13C (‰) relative to body length (mm; d13Ceuphausiid ¼
0.07(length) 2 20.5, R 2 ¼ 0.32, n ¼ 74, P , 0.001). d13C values have
been normalized for variable lipid contents using C:N ratios. Lines
denote the linear regression equations provided.
Food webs
Distinct tropic niches were not apparent among the
taxa analysed. Rather, d15N signatures depicted a
trophic continuum both north and south of the STC,
although not necessarily in the same order of enrichment in the separate water masses (Fig. 7). Euphausiids,
decapods, mysids, myctophids and chaetognaths generally occupied higher trophic positions than the jellyfish,
amphipods, pyrosomes, pteropods, ostracods, copepods
and salps (Fig. 7; Table II). POM did not represent the
lowest trophic level according to d15N signatures, presumably owing to its complex composition. Signatures
of d13C depicted POM as the most distinct grouping,
whereas the faunal groups were remarkably similar to
one another both within and between the north and
south water masses (Fig. 8).
The trophic structures of the euphausiid communities
remained markedly similar north and south of the STC,
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Fig. 7. Signatures of d15N (mean + SD; ‰) in fauna samples collected north, south and mid STC. Taxon groups have been ordered from most
depleted to most enriched according to northern signatures.
with Euphausia similis armata, E. spinifera, E. longirostris and
Stylocheiron abbreviatum maintaining a trophic position of
3.8 on both sides of the margin, and Nematoscelis megalops and Thysanoessa longicaudata maintaining slightly
lower trophic positions of 3.6 and 3.2, respectively
(Fig. 5; Table II). However, the trophic position of
Euphausia similis varied slightly with region (3.5 in the
north and 3.1 in the south). The remaining three
euphausiid species/groups, E. recurva, Thysanopoda pectinata and the pooled euphausiid furcilia, were collected
only in the north. The increase in d15Neuphausiid with
d13Ceuphausiid was not unexpected, as both signatures
show significant increases with body size (Fig. 6) and
stepwise trophic enrichment with increased omnivory
tends to occur simultaneously in the two parameters
(Michener and Schell, 1994).
Of the remaining fauna, the chaetognaths (as well
as some unidentified large mysids) also shared the
highest trophic position in the dataset (up to 4.2).
Interestingly, the chaetognaths increased by an entire
trophic position from south to north (2.7 to 3.8),
although the standard deviation for the southern
group was large and the northern value is probably
more representative of the typically carnivorous habits
of chaetognaths. Other groups having trophic positions
suggesting some carnivorous feeding include the
jellyfish (maximum position 3.5), the myctophid larvae
(3.1 – 3.4), the sergestoid and penaeidean shrimps
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Fig. 8. Signatures of d13C (mean + SD; ‰) in all fauna samples collected north, south and mid STC. Taxon groups have been ordered from
most depleted to most enriched according to northern signatures.
(3.3– 3.5), the small mysids Siriella thompsoni (3.0), and
the amphipods Vibilia armata, Themisto gaudichaudii and
Phronima sedentaria (2.2 –3.0). The large copepods also
occupied a trophic position of 3.2, indicating an
omnivorous diet, whereas the small copepods were
herbivorous with positions between 2 and 2.7. The
pyrosomes, ostracods, pteropods and salps occupied
the lowest positions (as low as 1.8).
DISCUSSION
Signatures of d15N in POM and zooplankton at the
STC were significantly different from north to south.
The primary source of the variation was related to the
latitudinal gradient in nitrate concentrations, with the
secondary influence of salinity being an indirect function of the different water masses on either side of the
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Table II: Trophic position of fauna relative to an isotopic baseline of salps (assigned trophic position 2)
Trophic position (+
+ SD)
Euphausiacea
Amphipoda
Copepoda
Decapoda
Mysidacea
Pyrosomatida
Salpida
Chaetognatha
Ostracoda
Pteropoda
Cnidaria
Osteichthyes
Species or taxonomic category
n
North
South
Euphausia similis
Euphausia similis armata
Euphausia spinifera
Euphausia longirostris
Euphausia recurva
Nematoscelis megalops
Stylocheiron abbreviatum
Thysanoessa longicaudata
Thysanopoda pectinata
Euphausiid furcilia
Phronima sedentaria
Themisto gaudichaudii
Vibilia armata
Large copepods
Small copepods
Penaeidean shrimps
Sergestoid shrimps
Siriella thompsoni
Large mysids
Pyrosoma atlanticum
Salpa thompsoni
Chaetognaths
Ostracods
Pteropods
Jellyfish
Myctophid larvae
8,6
3,3
1,2
3,7
9,0
6,3
5,1
5,1
1,0
4,0
9,0
3,5
11,3
17,4
6,3
6,0a
2,0a
2,0
1,3a
6,3a
2,4
5,3
8,1
3,2
4,2
5,1a
3.5 + 0.2
3.7 + 0.3
3.7
3.8 + 0.2
3.2 + 0.1
3.6 + 0.2
3.7 + 0.5
3.3 + 0.3
3.7
3.2 + 0.3
2.9 + 0.3
2.2 + 0.1
2.6 + 0.2
3.1 + 0.2
2.7 + 0.3
3.3 + 0.4
3.5 + 0.6
3.0 + 0.2
3.8
2.8 + 0.4
2.0
3.8 + 0.3
2.6 + 0.1
2.5 + 0.1
2.9 + 0.2
3.4 + 0.4
3.1 + 0.2
3.7 + 0.1
3.8 + 0.1
3.7 + 0.5
3.6 + 0.2
3.8
3.1
2.9 + 0.1
3.0 + 0.6
3.2 + 0.4
2.0 + 0.0
4.2 + 0.6
2.6 + 0.0
2.0
2.7 + 0.7
1.8
2.0 + 0.1
3.5 + 0.0
3.1
n, sample size (north, south).
a
Samples comprising individual animals, whereas the remaining sample types were represented by pooled individuals.
boundary. Interestingly, much larger shifts from north to
south were seen in some of the animal groups, such as
the ostracods and small copepods (mean differences in
d15N between north and south of up to 6.3‰, Table I).
This finding emphasizes the benefits of using isotope
signatures in primary consumer tissues to show a timeintegrated perspective of changes in oceanic habitat,
whereas POM values are instantaneous measures that
indicate only very recent changes. Signatures of d13C in
the plankton did not exhibit significant changes from
north to south.
Particulate organic matter
Marine d13CPOM signatures typically range between
218 and 228‰ (Goericke et al., 1994), and all of our
d13CPOM measurements (range 221.6 to 224.3‰)
were well within this limit. Rau et al. (Rau et al., 1989)
found more depleted values of d13CPOM to 235‰
south of the polar front, possibly owing to the elevated
availability of CO2(aq) in very cold water causing
greater fractionation of d13C as algae fix dissolved inorganic carbon (DIC). More recent studies have provided
evidence that seasonal and regional variations of phytoplankton d13C are frequently explained by changes in
the isotopic composition of the DIC (Michener and
Schell, 1994), or carbon fixation pathways used by the
dominant species, ultimately influenced by light availability (Goericke et al., 1994). Any changes in these parameters at the scale of our STC study were clearly not
sufficiently pronounced to cause regional effects on the
phytoplankton or zooplankton, and d13CPOM did not
show the marked spatial variations in d13C of particulate organic carbon in an eastern section of the STC
(Francois et al., 1993). The significant negative relationship between C:N ratio and d13CPOM that we found
may relate to variability in lipid content among samples
or in the relative contribution of phytoplankton or bacterial degradation to the bulk POM (Minagawa et al.,
2001), although this was clearly not a regional effect
(Fig. 4).
In addition to all animal taxa analysed, significantly
enriched d15NPOM values were found north of the STC
(mean 5.5 + 0.8‰) relative to south (mean 2.5 +
0.9‰), clearly indicating that the source of the trend in
consumers is a bottom-up phenomenon rather than an
increase in omnivory in northern organisms. All values
of d15NPOM were within the range typical of the
Southern Ocean [reported range 27 to þ8‰ (Wada
et al., 1987; Rau et al., 1991)]. The most depleted
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d15NPOM signatures have been measured in samples
derived from very high latitudes and appear to be
related to the low temperatures in polar regions (Altabet
and Francois, 1994).
Although POM roughly approximated the primary
food source for non-selective particle feeders at the STC,
the d15NPOM signature was more enriched than that of
some consumers (e.g. Themisto gaudichaudii and Salpa
thompsoni, Fig. 7). Significant d15N-enrichment of POM
relative to phytoplankton has also been reported in
Alaskan regions (Goering et al., 1990). This enrichment
was not unexpected, as bulk POM does not comprise
phytoplankton alone, but rather a variety of components
including bacteria and detritus. Furthermore, microbial
occupation and degradation of particles tends to isotopically enrich organic material (del Giorgio and France,
1996). The detrital component of POM is thus likely to
be enriched relative to phytoplankton, and selective
pelagic grazers can exhibit more depleted isotopic signatures than that of bulk POM. As a result, POM did not
represent a reliable measure of the baseline food source
for selective feeders, and, since salps showed the most
depleted d15N in the northern region, they were chosen
as the representative food web baseline from which
trophic positions of the other consumers were calculated.
The distinct isotopic signatures of POM that we
found in water masses north and south of the STC
were consistent with data derived by Altabet and
Francois (Altabet and Francois, 1994), who documented
enriched d15NPOM signatures in transects running from
55 to 308S, with the most pronounced shift occurring at
the STC. Because their latitudinal range was larger
than ours, the most depleted d15NPOM values they
measured in the south were 24‰, and the most
enriched in the north were þ7‰, resulting in an
11‰ range in d15NPOM from north to south (Altabet
and Francois, 1994) rather than the smaller 3‰ difference that we recorded (Table I). The relationship they
found between nitrate levels and d15NPOM was coincidental, as d15NPOM was a function of relative nitrate
utilization by phytoplankton (Altabet and Francois,
1994). In our study region, the primary nitrogen source
for phytoplankton was likely nitrate (Altabet and
Francois, 1994), and since nitrates originating at depth
have a relatively uniform isotopic composition (5 – 6‰)
both vertically and horizontally (Liu and Kaplan,
1989), variations in this baseline signal were unlikely.
Chl a concentrations in surface waters, ranging from
0.03 to 0.42 mg L21 throughout the study region,
indicated the absence of a phytoplankton bloom. As
Chl a (both surface- and depth-integrated concentrations) showed no trend with changing salinity and
temperature (Froneman et al., 2007), variations in recent
phytoplankton productivity do not appear to contribute
significantly to the isotopic shifts in POM from north to
south of the STC. Size-fractionated Chl a concentrations
in the surface water indicated that the picophytoplankton
(,2 mm) tended to dominate over the nano- (2–20 mm)
and microphytoplankton (.20 mm) at the majority
of sampling stations (Daly and Froneman, in press).
The relatively homogeneous nature of the Chl a data
throughout the study area suggests that variability in
phytoplankton species composition or cell size is probably not influential factors on d15NPOM. Although phytoplankton species composition in the different water
masses was not determined, any latitudinal differences
in phytoplankton species composition at the STC would
likely have produced variations in d13CPOM, arising
from alterations in C fixation pathways, which we did
not see.
Chlorophyll concentrations are typically low in the
STC region during austral autumn, with blooms occurring most frequently during austral spring (Llido et al.,
2005). Chl a concentrations .1.0 mg L21 occur north
of the STC during bloom conditions, as demonstrated
using satellite remote sensing and simulated models
(Llido et al., 2005), and do not correspond with the
enhanced nitrate concentrations consistently observed in
the south. When they occur, blooms last from 8 to 60
days and the mean areal bloom extent ranges from
10 000 to 45 000 km2. Such episodic events [Llido et al.
(Llido et al., 2005) documented 263 bloom events in 1
year] are sure to have lasting effects on the planktonic
food webs north of the STC and undoubtedly contribute to a unique biological and isotopic habitat that is
distinguishable from the south (e.g. Barange et al.,
1998). In this manner, residual effects of phytoplankton
blooms can propagate through the entire planktonic
food web so that the effects remain even during nonbloom periods. The episodic enhanced primary production north of the STC, despite continuously low
nutrient levels, likely results from a unique combination
of nutrients, temperature and water column stability,
combined with the physical accumulation effect from
converging currents that appear ideal for increased
algal biomass and growth (Lutjeharms et al., 1985;
Weeks and Shillington, 1996).
Food webs
Of the researchers who have measured isotopic
signatures in consumers and POM, only some have
found consumer signals to vary in concert with seasonal
or regional changes in d15NPOM (e.g. Schell et al., 1998;
Bode and Alvarez-Ossorio, 2004). At the STC, the
differences in zooplankton d15N from north to south,
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mirroring the regional variation in POM values, are
remarkable considering that some of these pelagic
organisms are highly mobile and do not appear geographically constrained by the presence of the STC
boundary (Sterley, 2008). The distinct isotopic signatures of plankton in the two water masses suggest that
individuals tend to remain with one water mass rather
than cross the proximate physical margin, despite individuals of the same species inhabiting both northern
and southern locations. Had there been extensive
migrations, we would have expected individuals with
more variable d15N signatures representing an average
of diet items removed from the more enriched northern
region and more depleted southern region. Rather, it
appears that the relative depletions and enrichments in
the phytoplankton are preserved and passed directly on
to the herbivores, detritivores and carnivores.
Rather than distinct, stepwise increases in trophic
levels, we found a continuum of trophic positions
among taxa consistent with the prevalence of generalist
feeding and opportunistic omnivory in many aquatic
food webs (e.g. France et al., 1998). Furthermore, different food web relationships were indicated by C and N
isotopes. This type of discrepancy is not unexpected
and has been recorded in other works (e.g. Goering
et al., 1990). Fry and Quinones (Fry and Quinones,
1994) recommend that trophic positions not be calculated using d13C, as fractionation of C sources is small
(,1‰) from diet to consumer relative to errors in
sampling. Furthermore, because fractionation steps of N
sources are significantly larger (.3‰) between consumer and diet, there is generally greater confidence
in d15N as an indicator of trophic position even
though the 3.4‰ per trophic level rule of thumb is not
steadfast.
Even at the perspective of an individual organism,
trophic position as indicated by d15N is not necessarily
constant, but varies with dietary state of a consumer
(e.g. will differ if a consumer is metabolizing recently
digested prey vs. stored reserves) and the ecosystem it
inhabits. As we used the default fractionation value of
3.4‰ (which represents an average value based on an
assortment of studies and organisms), our calculations
would not account for the natural variation in trophic
level enrichment among individuals, species and habitats. This natural variation in trophic level enrichment
certainly contributed to the variation in calculated
trophic positions for plankton both within and between
regions. Nevertheless, the trophic position calculations
for some of the taxa, the euphausiids in particular, were
remarkably consistent both within and between the
north and south water masses. The elevated trophic
position (.3) occupied by all of the euphausiid species
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indicated a significant proportion of carnivory in this
group ( primary consumers would occupy a trophic position of 2 in our model), and coincided with the
common finding of increased trophic fractionation and
hence enrichment in d15N with increasing body size
(Fig. 6; Fry and Quinones, 1994; France et al., 1998).
This relatively elevated trophic position for euphausiids,
as indicated by d15N signatures, concurs with the dominance of heterotrophic prey found in the stomach contents of euphausiids collected during earlier research
cruises in the Southern Ocean (Pakhomov et al., 1999).
Euphausiids, along with chaetognaths, have consistently
been categorized as the most important components of
the carnivore populations in pelagic ecosystems within
the Southern Ocean (e.g. Pakhomov et al., 1999 and
references therein). Comparisons of our findings for
Euphausia longirostris and Nematoscelis megalops with those
from a study by Gurney et al. (Gurney et al., 2001) near
the Prince Edward Islands, Southern Ocean, allow us
valuable insights on the dietary plasticity of these
euphausiids. Both species contained significant proportions of phytoplankton ( particularly diatoms) in their
guts and had d15N values 5‰ more enriched than
those of a local herbivore, Calanus simillimus (Gurney
et al., 2001), a copepod that was also abundant in our
STC study region. Nitrogen isotope signatures of the
same euphausiid species from our study differed from
the salp baseline by 5.7, suggesting a relatively larger
incidence of carnivory. These findings suggest an overall
higher level of carnivory at the STC, consistent with the
over-abundance of copepods available as food
(Froneman et al., 2007; Daly and Froneman, in press)
relative to the low phytoplankton biomass, particularly
microplankton cells that would be large enough to
allow direct consumption by euphausiids. Nitrogen
isotope signatures of copepods at the STC, particularly
the smaller size fractions (,3 mm length, trophic positions 2 to 2.7), confirmed their more herbivorous position in the trophic continuum. In contrast, d15N of
large copepods indicated substantial carnivory, as the
calculated trophic position (3.2) was elevated relative
to the small forms (Table II).
Stomach contents analysis of chaetognaths has confirmed the highly carnivorous feeding habits of this
group (Sterley, 2008), thus further validating their elevated trophic position, particularly in the north (trophic
position 3.8). Our findings for euphausiids and chaetognaths are not entirely consistent with other studies, as
d15N signatures recorded by Wada et al. (Wada et al.,
1987) identified euphausiids as strict herbivores along
with salps, but copepods and fish as strict carnivores
occupying the highest trophic level in one pelagic food
web in the Southern Ocean. They positioned the
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chaetognaths and jellyfish at a level in between the strict
herbivores and carnivores (Wada et al., 1987), whereas
our data supported the assignment of a higher trophic
position for both these groups (maximum trophic position for jellyfish 3.5). Jellyfish are commonly classified
as carnivores in the Southern Ocean, in addition to
amphipods, euphausiids, ctenophores, siphonophores,
decapods and fish (Pakhomov et al., 1999). Mysids are
seldom mentioned in Southern Ocean food web studies
owing to their low occurrence in the water column
(Murano, 1999), although our results suggest that they
are highly carnivorous like the decapod shrimps
(trophic positions 3 – 4.2). The biomass and abundance
associated with all the carnivorous groups varies substantially both spatially and temporally, but calculations
of their predation impact have indicated that their
feeding activities can represent a substantial contribution to C flux to depths in the open ocean
(Pakhomov et al., 1999).
Nitrogen isotope signatures of all three amphipod
species at the STC (trophic positions 2.2– 3.0) indicated
a level of carnivory somewhat lower than that of
euphausiids. This trophic shift down relative to the
euphausiids was also apparent in Themisto gaudichaudii
near the Prince Edward Islands (Gurney et al., 2001),
although heterotrophic prey dominated the stomach
contents of this amphipod in South Georgia (Pakhomov
and Perissinotto, 1996). Our results from the STC indicated overlapping trophic habits in the three amphipods
analysed despite the small size of Vibilia armata relative
to the others (V. armata ,9 mm whereas P. sedentaria and
T. gaudichaudii .11 mm length).
Few specimens of myctophid larvae were collected,
but their d15N values indicated carnivorous feeding
habits consistent with previous studies (Pakhomov et al.,
1996). In fact, myctophids were the dominate component of pelagic communities at the STC south of
Africa (Barange et al., 1998), and this group may
consume up to 40% of the annual secondary production in the Southern Ocean (Pakhomov et al., 1996).
Future studies that combine gut contents and stable
isotope techniques are needed to understand the variability in both myctophid and amphipod diets with time,
space and life history.
In accordance with the literature on suspension or
small particle feeders (Angel, 1999; Esnal and Daponte,
1999), the most d15N-depleted and hence herbivorous
consumers included the pyrosomes, ostracods, pteropods and salps (trophic positions 1.8– 2.8). Despite the
varied composition of our pooled pteropod samples,
which included specimens of Limacina retroversa, Clio spp.
and Cavolinia spp., the d15Npteropod signatures showed
remarkably small within-region variability (Table I).
The salps and pyrosomes showed much larger withinregion variability, and possible sources of this variability
remain unclear. Together with the small copepods,
these small particle feeders exhibited the greatest
changes in d15N from north to south (generally .5‰
difference; Table I), whereas consumers at higher
trophic positions in the food web showed much smaller
latitudinal variation (1 – 5‰ difference). This finding
suggests that the regional differences in the biological
component beginning with d15NPOM signatures tend to
attenuate with advancement in trophic level, perhaps to
the extent that top consumers such as fish and birds
would not reflect the significant regional distinctions
shown in the zooplankton d15N values shown here.
CONCLUSIONS
The results derived here suggest that, despite potential
cross-frontal mixing from storms, eddies and meanders,
the STC region southeast of South Africa represents a
strong frontal boundary that manifests latitudinal variability not only at the level of physico-chemical, biogeochemical and hydrological parameters, but also in a
biological manner in the form of stable nitrogen isotope
ratios within the phytoplankton and zooplankton.
These results provide important insights into how zooplankton communities take advantage of available
resources in a unique region of the ocean, and in turn
how their feeding activities may influence higher
trophic levels. Our data have significantly increased our
understanding of the STC as a region of isotopically
distinct feeding habitats for planktonic consumers and
the variability in trophodynamics within adjacent but
isotopically distinct water masses. Future studies that
incorporate samples from top predators will determine
whether such distinctive bottom-up effects are discernable in these larger organisms. Our findings, encompassing the convergence region of the southwest Indian
Ocean and the Southern Ocean where latitudinal gradients in physical and biogeochemical parameters are
strong, may not apply to areas of the STC having
weaker latitudinal gradients such as in the south
Atlantic. Future studies should encompass regions of
less intense convergence to determine whether similar
latitudinal patterns in the food webs occur.
Furthermore, the lack of any latitudinal d13C gradient
despite large differences in the physical properties of
seawater occurring across the STC was a remarkable
finding considering the significant changes in d15N. It
will be interesting to increase the temporal and spatial
ranges in future studies to determine the seasonal
dynamics at the STC and to determine at what scale
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variability in C isotope ratios begin to emerge in the
biological components of the ecosystem.
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Esnal, G. B. and Daponte, M. C. (1999) Salpida. In Boltovskoy, D. (ed.),
South Atlantic Zooplankton. Backhuys Publishers, Leiden, pp. 1423–1444.
France, R., Chandler, M. and Peters, R. (1998) Mapping trophic continua of benthic foodwebs: body size-d15N relationships. Mar. Ecol.
Prog. Ser., 174, 301–306.
AC K N OW L E D G E M E N T S
We thank the officers and crew of the S.A. Agulhas and
scientific personnel from Rhodes University and the
University of Cape Town (UCT) for their assistance
during sampling. Nutrient and oxygen data provided
courtesy of the Oceanography team from UCT. Thanks
also to I. Newton for processing the stable isotope
samples and R. Daly for creating Fig. 1. Collection and
analysis complied with the current laws in South Africa.
Francois, R., Altabet, M. A. and Goericke, R. (1993) Changes in the
d13C of surface water particulate organic matter across the subtropical convergence in the SW Indian Ocean. Global Biogeochem. Cycles,
7, 627–644.
Froneman, P. W., Ansorge, I. J., Richoux, N. B. et al. (2007) Physical
and biological processes at the subtropical convergence in the
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FUNDING
Funding was provided by the Department of
Environmental Affairs and Tourism (DEAT) through
the South African National Antarctic Program
(SANAP) and administered by the National Research
Foundation (NRF). Additional funds and facilities from
Rhodes University and the University of Cape Town
are appreciated.
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