Marine Biology 116, 147-160 (1993)
Marine
=-=BiOlOgy
@ Springer-Verlag 1993
High turnover of inorganic carbon in kelp habitats as a cause
of 6 3C variability in marine food webs
C. A. Simenstad 1, D. O. Duggins 2, p. D. Quay 3
x Fisheries Research Institute, M/S WH-10, School of Fisheries, University of Washington, Seattle, Washington 98195, USA
2 Friday Harbor Laboratories, M/S NJ-22, 620 University Road, Friday Harbor, Washington 98250, USA
3 School of Oceanography, M/S WB-10, University of Washington, Seattle, Washington 98195, USA
Received: 3 September 1992 /Accepted: 4 January 1993
Abstract. In a study to assess qualitatively the importance
of organic matter derived from kelp production in the
Aleutian Islands of subarctic Alaska, replicated samples
of autotrophic sources and primary and secondary consumer organisms were sampled for 613C among sources,
sites, (treatment) islands, and years. Unanticipated variation in the ~ 3C of kelps occurred among overtly similar
sites at different islands. Variation in the 6~3C of the
surface canopy-forming kelp Alariafistulosa was particularly extreme, ranging from - 15.5 to - 2 8 . 0 %0compared
to the understory kelps, Laminaria spp. A.fistulosa 6~3C
varied by as much as 6 to 7%o among similar sites at a
given island within years, and by as much as 3 to 4%o
between years at the same sampling site. In several cases,
~ 3 C variation was weakly tracked by some consumer
organisms, suggesting that even detritus pathways
through the food web can be localized and tightly coupled. Dynamic cycles in the concentration and 6~3C of
dissolved inorganic carbon (DIC) and aqueous CO2 concentration ([CO2]aq) were measured at three sites on one
island. The 613C or organic carbon fixed by A.fistulosa,
calculated from diurnal DIC concentration and 613C
measurements, varied by 15%o and varied inversely with
[COz]aq concentrations. Local DIC variability, probably
resulting from high productivity and decreased turbulence in dense kelp habitats, provides a possible mechanism of variation in kelp 6 ~3C. The short-term variability
in the 6~3C of organic carbon fixed by kelps indicates that
sampling methodology and design must assess this potential variation in marine macrophyte 013C before making
assumptions about the transfer of 613C_invariat e organic
matter to higher trophic levels. On the positive side, a
predictable relationship between [CO2Lq concentration
and kelp 613C offers a potentially robust means to assess
productivity effects on CO 2 limitation in kelps and other
complex aquatic macrophyte habitats,
Introduction
Stable carbon isotope ratios (I3C:12C or 613C) of consumer organisms have been used, either singly or in combi-
nation with other stable isotopes, to elucidate sources and
pathways of organic matter in marine and estuarine food
webs (reviewed by Fry and Sherr 1984, and further exemplified by Peterson et al. 1985 and 1986, Simenstad and
Wissmar 1985, Dunton and Schel11987 and Duggins et al.
1989). The utility of fi13C as a natural tracer of food-web
pathways has been based upon several precepts that are
pervasive in the literature: (1) plant taxa differ in 613C
principally through differences in photosynthetic pathways, and (2) there is a minor, and relatively predictable,
change in 613C as the organic matter moves through the
trophic levels of the food web. In addition, inherent in
most of these studies is the critical assumption that isotopic composition of the organic carbon sources, including
both living plants and their detrital products, is constant
over space and time. In particular, 613C studies involving
marine macroalgae such as kelps tend to presume low site,
habitat, ecosystem, and annual variability, justifying minimal replication over these spatial and time scales.
Depending upon the hypothesis being tested, significant variation in 613C of the organic carbon source could
obscure interpretation of consumer 61 aC (Fry and Sherr
1984, Cifuentes et al. 1988, Fenton and Ritz 1989).
Stephenson et al. (1984) illustrated that the di~3C values
of an individual kelp (Laminaria longicrUris) plant could
vary by as much as 8%0 ( - 1 2 to -20%0) over a spatial
gradient across the blade, and 3.5%0 at the same position
on the blade over a 13 mo period. The authors argued
that differential storage and translocation of biochemical
components of different isotopic composition was the
most likely explanation for this variation, as opposed to
changes in the isotopic composition of inorganic source
carbon, differential utilization of HCO a- and dissolved
CO 2 gas, variation in the photosynthetic pathway, and
contamination by epiphytic biota. Neither Stephenson
et al. nor any other authors presenting evidence of 613C
variation in macroalgae (e.g. Simenstad and Wissmar
1985, Wefer and Killingley 1986, Dunton and Schell
t987, Cooper and McRoy 1988, Wiencke and Fisher
1990) examined the scope of this variation on larger spatial (i.e., habitat, site, or region) or temporal (season,
year) scales.
148
C.A. Simenstad et al.: Kelp ~3C variability
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Fig. 1. Location of central and western
Aleutian Islands (a), and sites at the four
island groups (five islands) sampled for
(5t3C variability (b-e). Sites at Attu Island (b) were Murder Point (MP), Halibut Rocks (HR), and Orea Rocks (OR);
at the joined islands Alaid-Nizki (c),
Sea Lion (SL), West Nizki (WN), MidNizki (MN); at Shemya Island (c), Cobra Dane (CD7) Ebony Cliff (EC), and
White Alice (WA); at Amchitka Island
(d), Breakwater Rocks (BR), Constantine
P o i n t (CP), a n d Tvankin P o i n t (IP); at
Adak Island (e), Gannet Rocks (GR),
South Lucky Point (SL), and Razorback
Mountain (RB). Depth contours in m
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Islands
Documentation of spatial and temporal ~ ~3C variability was a critical element of studies we conducted to assess
the importance to detritus-based nearshore food webs in
the northern Pacific Ocean of organic carbon derived
from kelps (Duggins 1988, Duggins et al. 1989). We utilized ~3C:~2C ratios to separate the suspected sources and
fates of organic matter supporting consumers in two disparate nearshore communities: (1) a community with extensive kelp (principally the canopy-forming AlariafistuIosa and understory Laminaria spp.) habitats sustained
by sea otter (Enhydra lutra) predation on benthic herbivores (the sea urchin Strongylocentrotus polyacanthus),
and (2) a community without sea otters and consequently
with sparse kelp beds due to sea urchin grazing. We hypothesized that food webs in otter/kelp-dominated communities are based upon primarily kelp-derived organic
carbon, and those in urchin-dominated communities
upon phytoplankton. We tested our hypotheses by experimental transplantations and by sampling the 6~3C of
organic carbon sources ("source ~13C") and consumers
in different islands (i.e., treatment) over 3 yr.
To establish if significant 6~3C separation existed
among the potential organic carbon sources, it was neces-
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sary to determine the magnitude of the natural variability
in source 613C, the propagation of this unique 613C value, or "signature," along the food web up to assimilation
by indicator consumers, and the degree of 613 C variation
within consumer taxa. While we were successful in minimizing within-plant variation by systematic subsampling
of the kelps, we encountered unexpected among-site
(within-island) variation in kelp ~13C in the two dominant subtidal kelps, and among-island variation in Alaria
fistulosa. To investigate the potential origin of this variation, we conducted ancillary sampling of the concentration and 613C of dissolved inorganic carbon (DIC) over
spatial (nearshore- offshore) and temporal (diel) scales in
the kelp habitat in the last year of our 3 yr study. We
report herein: (1) patterns and magnitudes of long-term
(annual) 613C variability in three of the prominent kelps,
(2) related (~13C variability in three representative kelphabitat consumers, and (3) short-term (diurnal) variation
in kelp-habitat DIC concentration and 6~3C. We offer
several potential explanations for the observed variability
in kelp ~13C, and implicate [CO2]aq concentration within
dense kelp habitats as a possible source of the observed
~13C variability in kelps.
C.A. Simenstad et al.: Kelp 13C variability
Materials and methods
Sampling locations
Kelps and consumer organisms were Sampled at five locations during three excursions to the central and western Aleutian Islands
(Fig. 1) between 1985 and 1987. In 1985, we initiated experiments at
two islands and conducted preliminary 6 ~ C sampling to evaluate
methodologies; because the methods of sampling kelp 6a3C
changed between 1985 and 1986, only 1986 and 1987 data are used
in the present evaluation. Adak and Amchitka are sea otter/kelpdominated islands; Alaid-Nizki ~ and Shemya are urchin-dominated islands; and Attu is an island whose nearshore community is in
dramatic transition to a sea otter/kelp-dominated community because of a rapidly expanding sea otter population (Estes 1990).
Adak, Amchitka, Shemya, and Attu were visited during both 1986
and 1987; Alaid-Nizki was visited only during 1987.
From six total sample sites at each island, three (Fig. 1) were
selected for documentation of spatial and temporal variation. Table
1 shows the sampling design for both spatial and temporal analyses.
Within the constraints of field logistics, all sites were chosen
haphazardly but met the common criteria of being relatively waveexposed and having rocky subtidal substrate at between 5 and 15 m
depth. At four of the five islands, all sites were located on the Bering
Sea; at one (Attu), sites were exposed to the North Pacific Ocean,
but did not apparently differ in terms of wave exposure. Within
islands, we chose sites with comparable Alariafistulosa and Laminaria spp. populations; the intertidal kelp L. longipes, (which is
common to all islands because it grows in refuges protected from
urchin grazing) was also sampled.
149
Table 1. Sampling design, indicating Aleutian islands from which
organic carbon source and consumer 8 t 3C samples were obtained
for analysis of spatial and temporal variation. Unbalanced design is
due to nonuniform distribution of species among islands and to
logistical and budgetary constraints. The same three sites were sampled at each island in both years. *: samples (island) used for temporal analyses
1986
Kelp
Alaria fistulosa
l Adak*
Amchitka*
Attu
Shemya*
Adak*
Amchitka
Attu
Shemya *
Laminaria longipes
Laminaria dentigera
Shemya*
Alaid-Nizki
Adak *
Shemya *
Alaid-Nizki
Adak *
Amchitka *
Adak*
Amchitka
Attu
S hemya *
Adak*
Consumers
Anonyx sp.
Kelp sources
Mytilus edulis
Because the two islands, Alaid and Nizki, are physically joined,
we considered them as one island, "Ataid-Nizki"
2 Previously identified as L. groenlandica, but subsequently determined to be predominantly L. dentigera based upon our 1987 R.V.
"Alpha Helix" cruise along the western and central Aleutians (K. A.
Miller, University of Puget Sound, personal communication). Three
species of Laminaria (L. dentigera, L. longipes and L. yezoensis)
occur prominently in the shallow subtidal, of which L. yezoensis is
readily identifiable (Setchell and Gardner 1925, Drueh11968, Seagel
et al. 1989)_ Because stipe length and blade morphology ofL. groenlandiea are notoriously variable and L. groentandica lives in habitats
very similar to those occupied by L. dentigera, this assemblage is
comprised of both L. dentigera and L. groenlandiea; we have designated the assemblage by the former species because of its predominance
Adak *
Amchitka *
Adak*
Amchitka*
Attu
-
The kelps sampled for documentation of 613C variability included
the three dominant species: (1) Alaria fistulosa, an annual which
forms dense nearshore "beds" (down to 20 m depth) in sea otter/
kelp-dominated communities and is present in reduced patches in
urchin-dominated communities; (2) subtidal understory Laminariales (predominantly Laminaria dentigera2), which are perennial
kelp prominent only in the otter/kelp-dominated community; and
(3) the intertidal kelp, L. longipes, also a perennial present at all
islands. Because of the transient nature of the nearshore community
at Attu, we did not process either kelp or consumer samples for
6~3C from the 1987 visit. Five whole-kelp specimens (separated
directly above holdfasts) of approximalely equal size were collected
by SCUBA (subtidal) or hand (intertidal) at each of the three sites
at each island. The kelp blades were subsampled for 613C by taking
1 mm-diam plugs at uniform distances along the length of the blade
using an acid-washed (5% HC1)~ 13 hypodermic needle; all plugs
from a given plant were pooled for analysis in order to eliminate
within-plant variation.
1987
Adak*
Amchitka
Attu
Shemya *
-
Hexagrammos lagocephalus
Adak*
Amchitka
Attu
Shemya *
-
Shemya *
Alaid-Nizki
Adak*
Shemya *
Alaid-Nizki
Adak*
Shemya *
Alaid-Nizki
Consumers
Three nearshore consumers were collected as "indicators" of 6t3C
variability in kelp detritus: (1) intertidal mussels, Mytilus edulis 3,
which are suspension feeders; (2) the subtidal detritivorous/scavenging epibenthic amphipod Anonyx sp.; (3) the dominant fish in the
nearshore habitat, the rock greenling Hexagrammos lagocephalus.
Mussels are sessile and rock greenling are territorial; thus, both
would be likely to reflect spatial or temporal variation in the ~3C
of local kelp. We also assume that local movement ofAnonyx sp. is
not significant. Three to five specimens of each taxon were collected
at the same sites and times as the kelp samples. M. edulis of the same
approximate size (15 to 25 mm) were collected from equivalent tidal
heights. Anonyx sp. of similar size were selected from individuals
collected using an inverted-cone trap baited with fish tissue, and
were placed overnight in ~ 10 m of water at the sampling sites. Only
those Anonyx sp. with obviously empty guts were used, to eliminate
biases imposed by the bait on 613C. The gut cavity was visible and
the absence of food material evident in comparison with those that
had fed on the trap bait; in addition, the bait had always been
completely consumed when the trap was retrieved after ~ 2 4 h~
3 These may be M. trossulus, according to McDonald and Koehn
(1988)
C.A. Simenstad et al.: Kelp ~3C variability
150
during which time the amphipods had evacuated their gut contents.
Specimens of H. lagoeephalus specimens were randomly selected
from individuals caught in a 91 m long • 1,8 m deep trammel net,
equipped with 50 and 10 cm mesh and fished in the same location
for ~ 2 to 4 h. Specimens were utilized either whole (Anonyx sp.) or
subsampled (e.g. mantle tissue form M. edulis; muscle tissue from
11. lagoeephalus).
S a m p l i n g for D I C v a r i a b i l i t y
In 1987, we sampled the concentration and 6~3C of dissolved inorganic carbon at three sites on Amchitka Island during a diel time-series sampling program and along offshore inshore transects. A similar sampling series was conducted at Adak Island, but limited
funding prevented full isotopic analyses at both islands; the DIC
6~3C at Adak displayed trends similar to those at Amchitka. In
order to reveal localized differences in the 613C ofDIC (DIC ~13C)
as the source of kelp 61aC variability, sites were chosen that showed
a large range of mean Alariafistulosa 6~3C values. Our data on the
standing stock of A. fistulosa and Laminaria spp. at these sites
(Table 2) indicate that the only difference among these kelp-bed
habitats was the standing stock of all kelps pooled, which was
highest at Ivankin Point (IP) and Constantine Point (CP), and
lowest at Breakwater Rocks (BR). It should be noted that the density and standing stock of Laminaria spp. were generally comparable, if not higher, than those of A. fistulosa. Water samples were
taken at two depths (near-bottom and near-surface, ~ 10 and 0.5 m,
respectively); they were fixed with HgC1 z, and refrigerated in glass
bottles with poly-seal stoppers for later 6~3C analysis of the DIC.
In all cases, isotopic values are reported as per mil enrichment
of sample 13C:12C relative to PDB marine carbonate standard,
where 613C = ([13C:12Cs,,~0~e/13C:12CpDB].l). 1000. We use the term
"enrichment" to indicate samples with higher, i.e., more positive,
3~C values and "depletion" to indicate relatively lower, more negative values.
The in situ dissolved CO 2 gas concentrations, i.e., [COz]aq concentrations, were calculated for each water sample collected using
the manometrically determined DIC concentration and pH measurements. The equations and constants relating [CO/L q to pH and
DIC were taken from Broecker and Takahashi (1978). pH was
measured immediately onboard the vessel with an Orion model
601-A meter. The measurement precision of pH, DIC, and DIC
613C was +0.02 pH units, ___0.007 mM and ___0.02%0,respectively.
Statistical tests
Spatial variation in kelp and consumer ~t3C was tested using an
hierarchical ANOVA with sites nested within islands. There were
always three sites per island, but the number of islands varied
between analyses depending on species and year (Table 1). Differences in 613C between years (1986 and 1987) were tested using a
Wilcoxon paired-sample test. We chose this non-parametric analog
of a paired t-test because of small sample size and the consequent
inability to satisfy the assumptions of ANOVA. For each species,
the mean of three samples per site (Table 1 and Fig. 1) was used in
the analysis. Relationships between 6a3C of kelp and consumer
species (nine comparisons) within sites were tested by simple linear
least-squares regression of pairs of kelp and consumer 6t3C values
from each of the 2 years.
613C a n d D I C a n a l y s e s
Results
All kelp and consumer samples were acid-washed (5% HC1) on
precombusted glass-fiber filters and stored in sealed vials with desiccant for later processing; isotopic analyses were conducted by
Coastal Science Laboratories, Austin, Texas, using a VG SIRA
Series 2 mass spectrometer. Samples were combusted in quartz
tubes at 590~
sample replicability was generally _+0.02 to
+0.05%0 (K. Winters, CSL, personal communication).
Analysis of DIC 6 ~3C was accomplished by stripping ~ 100 ml
of acidified seawater samples with helium for 20 min and cryogenically collecting the CO 2 (Kroopnick 1974). The volume of water
analyzed was determined by using a constant-volume burette that
was gravimetrically calibrated, and the amount of CO 2 generated
was measured manometrically. The CO2 was then transferred, using
liquid nitrogen, to sample bottles for analysis on a Finnigan MAT
251 mass spectrometer. Replicate analyses of 2 mM Na2CO 3 standards resulted in a yield of 100.1 ___0.2% for dissolved inorganic
carbon.
Table 2. Alaria fistulosa, Laminaria spp. (L. longipes, L. dentigera,
L. yezoensis) and total of all kelps. Standing stock (g wet
0.025 m-z) of subtidal kelps at three coastal sites at Amchitka
Island studied for 6~3C variability, 1987. Values are means
(_+ 1 SD). Methods of determining standing stock were presented in
Duggins et al. (1989)
Site
Breakwater Rocks
Constantine Point
Alaria
fistulosa
Laminaria
All kelps
spp.
1 181.7
(+_3 178.7)
491.9
2 036.4
(+3 121.7)
(•
1 250.0
(_+1 866.5)
(•
1 466.7
132.4)
3 414.7
(-+1 952.4)
1 560.5
589.2)
(•
1 773.7
508.1)
3 481.6
(-+3 574.2)
Ivankin Point
(•
K e l p 6~3C v a r i a t i o n
The ~13C d i s t r i b u t i o n o f the three k e l p s o v e r l a p p e d cons i d e r a b l y , w i t h p o o l e d values e x t e n d i n g f r o m - 1 2 . 6 to
- 2 8 . 0 % 0 (Fig. 2). Alariafistulosa a c c o u n t e d for m o s t o f
the 13C-depleted tail ( b e y o n d the 9 5 % c o n f i d e n c e interval) o f the d i s t r i b u t i o n . E x a m i n a t i o n o f the s p a t i a l a n d
t e m p o r a l differences in k e l p 613C (Fig. 3 a - c ) a n d the
results o f the h i e r a r c h i c a l A N O V A testing s p a t i a l v a r i a t i o n at t w o scales - a m o n g sites w i t h i n i s l a n d s a n d a m o n g
islands (Table 3) - i n d i c a t e s several clear p a t t e r n s . W i t h i n
islands, 613C was significantly different a m o n g sites f o r
b o t h A. fistulosa a n d Laminaria dentigera in b o t h 1986
a n d 1987. I n several cases ( A m c h i t k a 1986 a n d S h e m y a
1987), A. fistulosa fi* 3C (Fig. 3 a) v a r i e d b y as m u c h as 6
to 7%0 a m o n g sites in a given year. Site differences f o r L.
longipes (Fig. 3 b) were n o t significant in either year. Differences at the i s l a n d level were significant for A.fistulosa
a n d m a r g i n a l l y significant for L. longipes in 1987. I n 1986
there were n o differences a m o n g islands for a n y species.
E x a m i n a t i o n o f Fig. 3 suggests t h a t i s l a n d differences
were largely the result o f i n c l u d i n g A l a i d - N i z k i in the
analysis for 1987. L. dentigera was n o t f o u n d at A l a i d N i z k i , so we d o n o t k n o w i f this p a t t e r n extends to the
t h i r d k e l p species.
B e t w e e n - y e a r differences were significant for o n l y
Alaria fistulosa ( W i l c o x o n p a i r e d - s a m p l e test, p = 0 . 0 5 ) .
A t 8 o u r o f 9 sites, A.fistulosa was m o r e d e p l e t e d in a3C
in 1987 (Fig. 3 a). A. fistulosa also d i s p l a y e d the g r e a t e s t
b e t w e e n - y e a r difference in 613C at a n y one site (4%0).
C.A. Simenstad et al.: Kelp 13C variability
30tAL,, KELPS '
10
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u}
4
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.
.
.
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151
.
.
.
1 2 l'Lam'inaria Io'noi~s
.
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Laminaria dentigera
. . . . . . . . .
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.~4
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513C(%0)
Fig. 2. Alaria fistulosa, Laminaria longipes and Laminaria dent#
gera. Frequency (absolute) distributions of 6~3C in kelp from the
western and central Aleutians in 1986 and 1987
Table 3. Hierarchial analysis of variance with sites nested among
and within islands
Islands
Sites within
islands
F
p
F
p
0.95
0.24
0.77
3.69
2.49
14.19
NS
NS
NS
NS
NS
0.003
28.50 <0.0001
4.75 0.001
2.03
NS
2.22 0.042
11.19 <0.0001
1.09
NS
9.32
2.47
7.98
28.9
11.2
15.8
0.010
NS
0.050
0.003
0.010
0.005
10.09 <0.0001
4.59 0.018
2.49
NS
0.76
NS
1.35
NS
3.07 0.032
1986
Alariafistulosa
Laminaria dentigera
Laminaria longipes
Anonyx sp.
Mytilus edulis
Hexagrammos lagocephalus
1987
Alariafistulosa
Laminaria dentigera
Laminaria longipes
Anonyx sp.
MytiIus edulis
Hexagrammos lagocephalus
Laminar& longipes and L. dentigera exhibited no significant between-year differences but, like A. fistulosa,
L. dentigera was more deplete in 13C at 5 of 6 sites in 1987
(Fig. 3 b - c ) .
Consumer t~13C variation
With one exception, 613C variation of the three consumers was both spatially and temporally less than that
of kelps. Within islands, sites differed in 3 of 6 analyses
(Mytilus edulis and Anonyx sp. in 1986, and Hexagrammos lagocephalus in 1987; Table 3). However, betweenisland differences were significant in 4 of 6 analyses. N o
significant island differences existed for Anonyx sp.
(0.1 > p > 0 . 0 5 ) and M. edulis ( 0 . 2 5 > p > 0 . 1 ) in 1986. Island differences in consumer 6 ~3C reflect the role of kelps
in the nearshore food web. In all cases where islands were
significantly different, differences resulted from enrichment of consumers at kelp-dominated islands, as discussed by Duggins et al. (1989). In one of the remaining
two cases (Anonyx sp. 1986), individuals were again enriched in 13C at kelp-dominated islands. The most variable consumer was Anonyx sp., which ranged by as much
as 4%0 between sites at Amchitka in 1986, and by as m u c h
as 3%0 between years at one site on Adak. The maximum
interannual variation in Anonyx sp. 613C was only a third
that of A. fistulosa and, among consumers, only Anonyx
sp. showed a significant difference between years
(Wilcoxon paired-sample, p = 0.025). As with the kelps
that showed between-year differences, Anonyx sp. was
depleted in 613C in 1987.
Regression correlations between 6t3C of kelps and
consumers within sites were insignificant in 7 o f the 9
comparisons. Only Anonyx sp. and Hexagrammos lagocephalus were significantly correlated (p=0.0005 and
0.0115, respectively) with the respective Alariafistulosa
value for the same sites (Fig. 4). The slope of these two
regression lines also differed from that expected (e.g. 1:1
with 0.5 to 1.5%o enrichment in the consumers, Fry and
Sherr 1984) for a uniform trophic enrichment; this suggests larger consumer depletion factors when A. fistulosa
was most depleted.
DIC fia3C and CO2 variation
The mean concentrations of DIC and 61aC measured
were, respectively, 0.0_+0.14%o and 2.23 +0.02 m M at
BR, 0.27___0.31%o and 2.18_+0.06mM at CP, and
0.25 + 0.39%0 and 2.19 -t-0.05 m M at IP. This similarity in
the DIC 613C values measured at the three sites was not
sufficient to explain the magnitude in the 61aC variation
of Alariafistulosa. A. fistulosa blades collected from the
same kelp beds at BR, CP and IP within hours o f collection of the water samples had mean (n = 3) 61aC values of
-19.13_+1.96, -18.53_+0.65, and -22.3+0.30%0, respectively. This 3.77%0 range was not as large as that
(6.40%0) observed in 1986, but followed the same order
among all three sites (Fig. 3 a).
Between morning
(~09.00 hrs) and
evening
(19.00 hrs) (Table 4, Fig. 5) at the CP and IP sites, pH and
DIC 6aac increased and DIC concentration decreased.
The observed diel trends in these three parameters probably resulted from photosynthetic uptake of inorganic
carbon. No strong diel trends were observed at BR. Diel
variability in pH, DIC, and DIC ~ 3 C at CP and IP was
higher than the inter-site variability, i.e., mean morning
pH, DIC concentration and DIC 61ac values at all three
sites was 7.88 _+0.04, 2.22 _+0.010 m M and 0.04_+ 0.07%0,
respectively (n = 12). At CP and IP, the mean changes
152
C.A. Simenstad et al.: Kelp 13C variability
-10 '
ADAK
AMCHITKA
SHEMYA
1986
1986
ALAID-NIZKI
(a)
ATTU
-12 1
1986
1987
1987
1987
1986
1987
-14 1
_161
-/
..=~
0
0
c~
~F
iI
~/) - 2 6 -
-22 9
_2,1
-26 1
Alaria fistulosa
-28 1
-30 "
-10
lit
Ill
GR~
I
I
I
I
I
i i i i i i
~WA
I
MASLWN
CD~WA
I
I
I
HRMPOR MEAN
(b)
-
-12
-
~
-14
-
Z
-16
4986
1986
1986
1987
ALAID-NIZKI
SHEMYA
AMCHITKA
ADAK
_o
I
BRCPIP BRCPIP
SITE
~SL
1987
ATTU
1987
1986
F-~ -18
2
~
-2(?
0
t~
~
-22
-24 -
-26 -
Laminaria Iongipes
-28
-
f l i r T ?
-30
~
I
I
J
I
i
I
I
I
CDECWA CDECWA
BRCPIP
~SL
I
i
MASL
I
I
I
H R M P O R MEAN
SITE
-,~ 1
-12
(c)
ATTU
AMCHITKA
ADAK
'
1986
1986
1987
1986
1987
-14
A
=~ - 1 6
z
0 -19
tO -20
0..
=E
0 -22
o
~
-24
-26
Laminaria dentigera
-28
-30
I
I
I
I
I
I
GRRBSI_GRRBSL
I
l
l
I
I
BRCPIP BRCPIP
SITE
I
i
t
HRMPOR
MEAN
Fig. 3. 313C composition of representative kelps (Alariafistulosa, Laminaria longipes, L. dentigera) and consumer organisms (Mytilus edulis,
Anonyx sp., Hexagrammos lagocephalus) in nearshore waters of five Aleutian Islands, Alaska, 1986-1987. Full names and locations of sites are
given in Fig. 1. G r a n d mean is indicated on far right of each graph
C.A. Simenstad et al.: Kelp 13C variability
153
-10
AMCHITKA
ADAK
SHEMYA
ALAID-NIZKI
ATTU
(d)
-12
1986
1986
1987
1986
1987
1986
1987
-14
o
Z
O
-18
I--.
U)
O -20
a.,
O
to
-22
-24
-26
Mytilus edulis
-28
1 1 1
-30
i i i
~
i i i
~
I
BRCPIP
i
i
i
COECWA CDECVVA
i
i
HR MP OR
MEAN
SITE
-10
ADAK
AMCHITKA
SHEMYA
ATTU
ALAID-NIZKI
(e)
-12
1986
1987
-14
~
-16
I
1986
1986
1987
1987
1986
I-O -2o a,.
=E
~
22
~
-24-26
-
-
Anonyx sp.
-26 9
-30
I
i
I
i
i
I
GRI~ ~I. GRFEt~_
I
I
I
i
BRCPIP
I
i
I
I
I
BPECWA BPECWA
I
I
I
MASLWA
I
i
i
HRMPdR
MEAN
SITE
-10
ADAK
AMCHITKA
BHEMYA
ALAID-NIZKI
ATTU
(f)
-12
1986
-14
= -16
Z
0
E
O
=E
1987
1986
1986
1987
1987
1986
i}..t
t..{{
-18
-20
13.
O
-22
to
~
-24
-26
Hexagrammos lagocephalus
-28 -
-36
I
I
I
I
I
I
GRRBSL GRRBSL
i
i
i
i
BRCPP
i
i
CD ECWA ~ECWA
SITE
i
,
,
HR MP OR
MEAN
Fig. 3 (d) - (f)
C.A. Simenstad et al.: Kelp ~3C variability
154
Table 4. Alaria fistulosa. Concentrations and 5x3C of inorganic
carbon over diel period in kelp habitat, Amchitka Island, Alaska,
4 - 5 July 1987. Water temperature was uniformly 9.0 to 9.5~
throughout sampling period. BDT: Bering Daylight Time; DIC:
Site and date
(i987)
Breakwater Rocks
4 July
5 July
Constantine Point
4 July
5 July
Ivankin Point
4 July
5 July
dissolved inorganic carbon; Pco~ : partial pressure of carbon dioxide.
[CO2]~q was calculated from measured pH and DIC at in situ
temperatures (Broecker and Takahashi 1978); Pco~ was calculated
from dissolved CO 2, [CO2],q, using in situ solubilities (Weiss 1974)
BDT
(hrs)
Depth
(m)
Salinity
(%0)
pH
DIC
(raM)
[CO2],q
(raM)
Pco~
(ppm)
DIC 613C
(%Q
09,30
09.40
19.55
20.09
10
1
10
1
33,109
33.075
33.206
33.107
7.82
7.86
7.93
7.96
2.244
2.240
2.245
2.219
0.030
0.028
0.023
0.022
665
620
510
488
-0.08
-0.13
-0,11
0.06
09.35
09.45
10
1
33.212
33.102
-
-
2.244
2.207
-
-
09.10
09.20
19.30
19.43
10
1
10
1
33,118
33,043
33.080
33,037
7.87
7.90
8.06
8.11
2.237
2.209
2.120
2.100
0.026
0.025
0.016
0.014
576
554
354
310
-0.14
0.13
0.60
0.68
09.00
09.10
10
1
33.019
33.004
7.97
-
2.205
2.216
0.021
-
466
-
0.31
0.19
08.45
08.55
19.07
19.12
10
1
10
1
32.988
32.980
32.971
32.957
7.87
7.89
7.94
8.01
2.218
2.210
2.150
2.100
0.027
0.025
0.022
0.018
598
554
488
399
-0.20
-0.02
0.57
0.82
08.35
08.45
10
1
33.133
33,011
7.82
7.93
2.213
2.222
0.029
0.024
643
532
0.13
0.03
-
0.03
0.25
o
g
-14
y = - 10.705 + O.36915x
R2 =
0
0,520
-14-
t-,e5
y = - 12.90q ,~ 0.18084x
R2 =
0,300
-15-
~ -16
mr
9
~.~
~. -16-17t~
~-2Q
-lB.
-22 ["/
-30
%
-25
9
(a),
-2'0
-15
-10
(b)
j
-19
-30
-25
-~0
is
Fig. 4. Alariafistulosa. Simple
linear regression of mean 613C
of the kelp compared with
that of the amphipod Anonyx
sp. (a) and the fish Hexagrammos lagocephalus (b) from the
same sites for each of two
years
J0
A/aria fistulosa 513C (%0)
Alaria fistulosa ~,13C (%,,)
1.0
0.8
-%
~o
cC
O
0.6
IP
CP
!'.!I!!11==:......
..,
0.4
Fig. 5. Concentration (mmol/1) and 61aC (%0) of dissolved inorganic carbon (DIC) from surface (continuous
lines) and bottom (hatched lines) waters at three kelp
habitat sites at Amchitka Island, Alaska, in the morning
(I) and evening (ta) of 4 July and following morning (o)
of 5 July 1987. BR: Breakwater Rocks; CP: Constantine
Point; IP: Ivankin Point
0.2
0.0
-0.2
-0.4
......
.......
CP
I
2.10
I
I
2.14
I
I
2.18
I
I
2.22
CO~ CONCENTRATION (mmollliter)
I
2.26
C.A. Simenstad et al.: Kelp 13C variability
between morning and evening measurements (n = 4) were
0.15 _+0.06, - 0.10 _+0.02 m M and 0.73 __0.12%0, respectively, substantial variations bearing in mind the precision of the measurements.
Discussion
In Duggins et al. (1989), we reported that representative
consumers were significantly enriched in ~aC at sea otter/
kelp-dominated islands compared to sea urchin-dominated islands, consistent with the utilization of kelpderived organic carbon by these organisms. It is important to note that these differences were significant, in
part, because within-site kelp and consumer 613C variation were extremely low; variation of the kelps at this
spatial scale (e.g. within-site) was often __0.2%o. These
results indicate that, on the scale of the island ecosystems,
there is significantly greater accumulation of kelp carbon
by nearshore consumers at sea otter/kelp-dominated islands. However, finer-scale examination of 6~3C variation among sites (at a given island) and between years (at
a given site) provides valuable insight into the magnitude
and potential sources of spatial and temporal variability
in 613C within a taxa and among closely related taxa (e.g.
kelps). These data illustrating extensive kelp 6~3C variation are uniquely comprehensive and indicate that the
results of marine and estuarine food web studies using
~3C as a tracer may be misinterpreted without systematic evaluation of this variation. Furthermore, isotopic
variability can provide valuable information about the
processes producing the source carbon.
Within-species variation in macroalgal 613C has been
described frequently (see Fry and Sherr 1984), but the
mechanisms responsible have not been identified. Variable outcomes of carbon-isotope fractionation in aquatic
autotrophs is generally considered to reflect differences in
either photosynthetic pathways (Fry and Sherr 1984),
isotopic signature of the inorganic carbon source (e.g.
Deuser and Degens 1967, LaZerte and Szalados 1982), or
the rate-limiting step(s) in the photosynthetic process
(O'Leary 1988). In the literature, other potential causes
of 3~3C variation observed in aquatic plants include contamination from epiphytic biota with different 613C values (Fry and Sherr 1984, Faganeli etal. 1986) and
translocation and storage of nitrogenous compounds
(Stephenson et al. 1984, Fenton and Ritz 1989).
Although we do not interpret differential photosynthetic pathways as a likely source of the 613C variation
we document, the dynamic processes involved in carbon
fixation in kelps, the environmental conditions modifying these processes, and the resulting effects on ~3C
fractionation are still obscure. Although all kelps
(Phaeophyceae) are considered to fix carbon predominantly via ribulose-l,5-bisphosphate (RuBP) carboxylation (Kremer 1981 a), some seaweeds are thought to utilize light-independent fixation using phosphoenolpyruvate carboxykinase for as much as 20% of the their total
fixed carbon (Lobban et al. 1985, Reiskind et al. 1988,
1989). However, light-independent carbon fixation is
considered to be significant only in the young tissues of
/55
kelps and fucoids and to predominate primarily under
conditions of reduced irradiance and low nitrogen
availability (Kremer 1979, 198/a, b).
Because we sampled systematically from only the
blade regions of the plants above the meristem and ensured that the surfaces of the blades were clean of epiphytes before sampling, biases due to light-independent
carbon fixation, contamination from epiphytes, and differential distribution of storage products should have
been minimal. Light-independent carbon fixation occurs
primarily in the meristematic region of kelps, which we
intentionally avoided sampling. Also, our sampling
method intentionally integrated the entire blade of the
plant above the meristem in order to eliminate any biases
imposed by heterogeneous distribution of tissue 613C.
We cannot, however, preclude the possibility that the
sampling of only a limited number of 1 mm-diam plugs
along a 15 cm-wide, 10 m-long Alariafistulosa plant may
have induced some of the observed variation. The low
( < 3%0 in most cases) among-plant 61 aC variation within
sites was, however, substantially lower than between sites
and between years, suggesting that it made but a minor
contribution to significant 613C variation over a much
larger scale. Thus, inter-site and interannual variation
more likely indicates differences in the physiological
state, or potentially age, of the kelps at the different sites
and in the different years.
Although there is ample evidence of seasonal variation
in macroalgae 613C (Simenstad and Wissmar 1985, Dunton and Schell 1986, 1987, Wefer and Killingley 1986,
Cooper and McRoy 1988, Wiencke and Fisher 1990),
evidence for mechanisms accounting for this variation is
meagre. Variation in the isotopic composition of diverse
biochemical components, particularly fatty acids and
lipids, is one of the more common explanations for such
long-term variation in 6~3C (Park and Epstein 1961,
Parker 1964, Smith and Epstein 1970, Stephenson et al.
1984, Dunton and Schell 1987). In the present study, we
sampled each island within a relatively short time span
(i.e., 3 d to 2 wk) within any one season; large-scale
changes in kelp physiology related to season should,
therefore, have been minimal. Autecological characteristics such as time of recruitment, growth chronology, and
age composition of the kelp stand may be site-specific
and could affect the metabolism and storage of biochemical components of differing 613C composition on shorter
time scales. This could explain why 6 a3C signature of the
annual AlariafistuIosa is more variable than 6~3C of the
perennials Laminaria longipes and L. dentigera. In addition, if recruitment of A.fistulosa is stochastic at different
sites, this would explain the lack of consistent order in
sites and years evidenced by the A. fistulosa in the central
and western Aleutians. Unfortunately, neither the data
obtained during our study nor that of previous literature
can differentiate whether the observed 6~3C variability
reflects different physiological states of plants as a function of their population characteristics or of the proximate conditions controlling carbon fixation.
Given these constraints, we focus on the kelps' carbon-fixation mechanisms as a potential source of the ob=
served kelp 6 t 3C variability. Although DIC 613C has pre~
156
C.A. Simenstad et al.: Kelp 13C variability
viously been shown to vary significantly both spatially
and temporally in estuaries (Fry and Sherr 1984), we
found low site or diel variation in our study (Table 4). The
mean (0.173%o) and maximum range (1.02%0) for our diel
sampling compared well with the maximum seasonal
variation of 0.7% observed in a similar, coastal kelpdominated system by Stephenson et al. (1984).
For plants which predominantly use the C3-fixation
pathway, a reduced kinetic isotope fractionation during
carbon fixation has been associated with decreased CO 2
availability or switching to the use of HCO3- under CO2
stress (Lucas and Berry ~985, Prins and Elzenga 1989).
For instance, a consistent inverse relationship between
the [CO/],q concentration and plant 613C has been shown
for marine plants (Degens et al. 1968, Calder and Parker
1973, Mizutani and Wada 1982, Rau et al. 1989), and
between primary productivity and plant 613C (Cifuentes
1987). However, many species of marine algae, and particularly kelps, have a greater affinity for HCO 3- than
for CO/, especially when photosynthesis is COz-limited
(Kremer 1981 a, Sand-Jensen and Gordon 1984, Bidwell
and McLachlan 1985); thus, [CO2],q may not constitute a
rate-limiting resource in kelp habitats. It has also been
suggested that kelps are among those aquatic plants
which are capable of metabolically transporting external
HCO 3 - using a "COz pump" that acts energetically as a
CO2 concentrating mechanism independent of limitations on passive diffusion (Badger et al. 1978, Raven
et al. 1987, Farquhar et al. 1989, Prins and Elzenga 1989,
Surif and Raven 1989, 1990, Raven and Farquhar 1990,
Raven and Osmond 1992).
Our diel sampling of the kelp habitat at three Amchitka sites in 1987 (Table 4) clearly indicates short-term
changes in [CO2].q availability and 6a3C. To gain further
insight into how this variability affects the 613C of kelps,
we estimated the 613C of the net organic carbon fixed by
the kelp during a daily photosynthetic cycle, utilizing the
measured changes in the concentration and 613C of DIC.
The 613C of the net organic carbon fixed equals the 613C
of the inorganic carbon removed from the D I e pool during the day; this can be estimated from changes in the
D I e and D I e 6x3C occurring from morning to evening,
following the approach used by Smith and Kroopnick
(1981) for a coral reef community. For a simple closed
system, the carbon mass and isotope balances are as follows:
D I C , , - OC DICe
DIC,.613Cm_OC,613C0 c = D I C e , 613Ce '
---
where m represents morning, C~ represents evening, and
Coc is the net carbon fixed. This simplified inorganic
carbon balance ignores effects by CO 2 gas exchange and
mixing. Although these simplified assumptions may underestimate the net carbon-fixation rate derived from the
decrease measured in the daytime DIC, they should have
much less effect on the D I e 6~3C data, because the isotopic equilibration time of the D I e pool to the CO2 gas
exchange at these sites ( ~ 20 m depth) is > 1 yr (Broecker
and Peng 1981) and mixing results in D I e with a 6~3C
value similar to that measured in the kelp habitat (see
Table 4).
-10
'~,,,,,.,,,~
~13C = -1683 [CO2 aq]+13.6
-15
0
-20"
-25
-30
0.012
0.0'14
0.0'16
0.0'18 0.()20 0.022 0.(~24
CO 2 aq (rnmol/liter)
Fig. 6. Estimated 6 1 3 C of net carbon fixed between morning and
evening as a function of dissolvedCO2 gas concentration in evening
at Ivankin Point (.) and Constantine Point (.), Amchitka Island,
Alaska. ~513Cof fixedcarbon was derivedfrom change in concentration and c513Cof DIC (see "Discussion"). [CO2],q: dissolved CO2
The values calculated for the 613C of the organic carbon fixed kr613C OC/,~ based on surface- and bottom-water
samples, were - 10.4 and - 13.2%o at CP and - 16.0 and
-23.8%0 at IP, respectively. The mean value of - 1 6
+ 6%0 calculated for the organic carbon fixed at CP and
IP compares well with the mean 613C of - 1 8 + 3%0 for
the three dominant kelp species at these sites and is significantly enriched compared with the mean 6~3C of - 2 4
+ 1%o recorded for phytoplankton (Duggins et al. 1989).
The range in the calculated 613C for organic carbon
fixed by kelps (Coc) is also of the same order as the - 1 4
to -28%0 range in kelp 6~3C (Fig. 3). Thus, whatever
mechanism controls the variability in the 613C of carbon
fixed over the short-term diel cycle could potentially control the inter-site variability in kelp 6~3C. Calculated
6~3Coc values are inversely correlated to the late afternoon concentration of dissolved CO2 gas (Fig. 6), similar
to the correlation between phytoplankton 613C and dissolved CO2 gas in the surface ocean reported by Rau
et at. (1989, 1992) and in earlier laboratory culture experiments (Degens et al. 1968). In fact, our measured A613C/
A[CO2]aq slope of 1.8%o ~tM [CO2]~ 1 (Fig. 6) is essentially
the same as the slope of 1.7%o laM [CO2],q reported by
Rau et al. (1992). Whether this inverse relationship between 6~3C and CO2,q is a direct consequence of CO2
diffusive limitation or active transport of HCO;- cannot
be interpreted either from the present data or from the
literature.
Although a high diffusive supply of CO 2 to the kelps
might be expected in such a high-energy environment as
that off the Aleutian coast, Jackson and Winant (1983),
Jackson (1984), Duggins (1988) and Eckman et al. (1989)
have aptly illustrated that the complex, dense structure of
coastal kelp bed habitats can significantly modify turbulence and flow regime within kelp habitats. If such modification in the kelp hydrodynamic environment results in
the formation of a thicker diffusional boundary layer at
the kelp/water interface, significant CO2 depletion could
occur, particularly if CO2 were the sole carbon substrate.
CO z limitation was experimentally demonstrated by
Wheeler (1980), who found that higher boundary-layer
turbulence adjacent to the blade of Macrocystis pyrifera,
obtained by increasing water velocities from 0 to 4 cm
s- 1, increased the kelp's photosynthetic output by 300%.
C.A. Simenstad et al.: Kelp 13C variability
EXPOSURE CONSTANT
157
KELP BIOMASS CONSTANT
b
v
TURBULENCE
DIFFUSIVE
BOUNDARY
LAYER
THICKNESS
CO 2 DEMAND
AND DEPLETION
13C ENRICHMENT
",,'/~M/MM/////M~/~-
--/7~//..,/zz/zz//z//z//~
Fig. 7. Conceptual model of effect of kelp biomass and environmental exposure on 613C of organic carbon fixed by kelps in coastal
habitats
Arguing simply from the standpoint of CO 2 utilization,
high kelp biomass could lead to enriched kelp signatures
through two interaction mechanisms: (1) decreased flow
(or turbulence) promotes a thicker diffusive boundary
layer, thus limiting CO 2 transport to the plant; and (2)
high photosynthetic demand decreases CO 2 availability
outside the diffusive boundary layer (Fig. 7).
Thus, the interaction between kelp productivity and
the hydrodynamic environment, both of which differ often dramatically within and among the Aleutian islands
studied, could contribute some of the site variation observed in kelp 6~3C through mediation of the kinetic processes affecting fractionation. In contrast to sea urchindominated islands, where the canopy-forming kelp Alariafistulosa is sparse and a complex understory kelp assemblage (e.g. Laminaria spp.) virtually absent, dense
kelp habitats such as at the sea otter-dominated islands in
the Aleutians could be likely sites for CO2 limitation.
Alternatively, exposure to high wave energy and strong
along-shore currents would counter the baffling effect of
dense kelps. Under conditions of limited CO/supply, the
net 6~3C of the carbon fixed by the kelps would tend to
be more enriched than at sites where water circulation
rates are higher and/or carbon fixation rates are lower.
We propose a conceptual model that argues where
kelp structure (e.g. standing stock) is highest, [CO2]aq
availability is reduced; this, in turn, promotes ~3C enrichment during carbon fixation by the subtidal kelps
(Fig. 7). Where kelp structure is less dense and/or higher
wave energy exists, the kelps are depleted in 13C. In fact,
there is a general trend toward 13C enrichment of Alaria
fistulosa in dense kelp habitats both among and within
the different Aleutian Islands (Fig. 3 a). For instance, the
extremely 13C-depleted signatures of A. fistulosa in the
Alaid-Nizki island group may well be due to the fact that
not only are these the most wave-exposed islands of those
we studied but, in addition, because of the absence of sea
otters, they have only sparse stands of A. fistulosa and
virtually no understory kelps. ~5~3C variation among sites
at one and the same island also implied similar mechanisms. For example, all three study sites at Amchitka had
comparatively high total kelp biomass (particularly Constantine Point and Ivankin Point, Table 2), but differed in
their exposure to waves and currents. Ivankin Point is
more exposed than Constantine Point, it lies in a region
of particularly strong currents and contains the most
3C-depleted A. fistulosa stands. The 613C of A. fistulosa
at Breakwater Rocks was consistently intermediate between the other two sites; this may reflect the fact that the
kelp biomass is somewhat lower (reducing enrichment)
and the site more protected and not as exposed to wave
and current action (promoting enrichment). ~13C of the
Laminaria spp. at these three sites followed the same general pattern (cf. Fig. 3 c and Table 2), supporting these
interpretations. Thus, under our conceptual model
(Fig. 7), the 613C values typically reported for macroalgae in most studies, which are more enriched compared
to phytoplankton, would represent situations where CO 2
diffusion is limited and/or HCO~ active transport occurs; in contrast, 13C-depleted kelps such as we have
found at certain sites (i.e., high energy and/or high kelp
biomass) represent conditions of unrestricted photosynthesis.
Factors that affect kelp photosynthesis and growth
rates (e.g. light, nutrients, inorganic nitrogen sources)
will also influence kelp 613C by directly controlling carboxylation rates (Wefer and Killingley 1986, DescolasGros and Fontugne 1990, Wiencke and Fischer 1990).
However, we did not measure light, nutrients, or the
growth rates of the kelps at the different sites, and therefore have no indication of the magnitude and dynamics
of these factors. Variations in the rate of photosynthesis
arising from light or nutrient limitation probably do not
play a significant role in ~ 3C variability in A laria fistulosa, which is a surface-canopy kelp and thus unlikely to
experience dramatically different light regimes between
islands or sites. The understory Laminaria species may
experience some light limitation under dense A. fistulosa
canopies. The dynamic interaction of factors influencing
photosynthetic rates and inorganic carbon supply relative to the effect upon the f~3C of organic carbon fixed by
kelps requires further investigation (Prins and Elzenga
1989).
Finally, the general lack of site-specific correlations
among kelp and consumer 6~3C imply that detritus from
various sources and different 6~3C values are generally
mixed throughout the nearshore ecosystem of these islands despite strong site-specific variability. The three
consumers considered here for 613C variation were representative of divergent feeding strategies-suspension
feeding (Mytilus edulis), scavenging-detrivory (Anonyx
sp.), and benthic predation (Hexagrammos lagocephalus).
Higher within-site variation in Anonyx sp. (Fig. 3d)
probably reflects its differential utilization of the diverse
detritus sources available within the same kelp habitat. In
the high-energy nearshore environs of the Aleutian Islands, kelps frequently break loose from the substrate
and degrade within the kelp-bed habitat, where they are
available to herbivores and detritivores. In the sea
urchin-dominated islands, grazing by the urchins is also
a continuous source of kelp detachment. Thus, kelps
which undergo prolonged exposure to conditions that
either limit [C < O2]aq availability or induce HCO 3 transport, and as a result have measurably different fi~3C signatures, subsequently enter the detritus pool, contributing spatial and temporal pulses of a3C-enriched carbon to
detritivores. The lack of significant intra-site correlations
between the 613C of most kelps and consumers (except
158
for Alaria fistulosa-Anonyx sp. and - 11. lagocephalus,
Fig. 4) suggests variable among-site transport, deposition, and degradation of kelp in the nearshore habitat,
rather than direct utilization of in situ POC/DOC. The
fact that OI3C variation also decreased with increasing
trophic level and longevity of the consumer, with fish
displaying the least variability, presumably reflects the
prolonged incorporation of organic carbon from isotopically different prey available to long-lived secondary consumers (e.g. 12 to 15 yr for H. lagocephalus) compared
with short-lived primary consumers (e.g. 2 to 5 yr for M.
edulis; months for Anonyx sp.).
In summary, we hypothesize that complex interactions between the high productivity of kelps and the variable hydrodynamic flow regimes of kelp habitats influence [CO2]~q availability and/or HCO;- active transport,
resulting in variable 613C content of kelp carbon in
nearshore food webs. In the Aleutian Islands, the interaction of variable kelp standing-stock and degree of site
exposure appears to result in considerable between-site
variability in kelp 6~3C. However, the kelp 613C signature at each island was still sufficiently distinct to explain
much of the differences in consumer 6~3C (Duggins et al.
1989). Habitat characteristics that affect CO2 limitation
and kinetic fractionation apply heavy constraints to the
assumption that 6~3C is an invariant tracer of food-web
carbon fixed by aquatic macrophytes such as kelps. Such
6~3C variability can produce complications where kelp
standing stock is the primary independent variable. In
contrast to nearshore kelp habitats in which Laminaria
spp. and other understory kelps probably constitute a
source of kelp carbon which, if not predominant, is at
least equal to that of Alaria fistulosa (Duggins 1980),
food webs in habitats in which A. fistulosa and similar
canopy kelps are the dominant sources of kelp production may be particularly influenced by variation in kelp
613C. In an earlier mixing model for estimating the 6t3C
contribution of kelp carbon to nearshore consumers in
the Aleutian Islands (Duggins et al. 1989), we employed
a mean of all sites to represent kelp signature for each
island. In order to evaluate the impact of site variation on
our original interpretation, we recalculated the model
individually for each site. Results using the revised model
indicate that most consumer species exhibited an increased dependency on kelp carbon, with consumers
from the islands with a3C-depleted A.fistulosa (e.g. Shemya) displaying greater (,-~45%) changes than those
from islands with more enriched A. fistulosa (e.g. Adak
and Amchitka Islands). However, our original conclusion that kelp carbon is more important for consumers in
the sea otter/kelp-dominated systems than in the sea
urchin-dominated systems was not affected; the contribution of kelp carbon was still highly correlated with consumer growth and production (Duggins et al. 1989).
Despite the complicating effect of high short-term
613C variability in kelps on elucidating carbon pathways
in nearshore marine food webs, the strong diel relationship between the 6~3C of the carbon fixed by photosynthesis and dissolved COz concentration suggests that
6t3C variability in DIC might be utilized as a tracer of
productivity by aquatic plants such as kelps. Diel shifts in
C.A. Simenstad et al.: Kelp ~3C variability
the 6~3C of DIC in relation to kelp photosynthesis and
growth rates and as a function of nutrient and light
availability and water-flow rates in kelp habitats need to
be examined experimentally and in considerable detail.
The present results reinforce the arguments of Fry and
Sherr (1984), Cifuentes et al. (1988) and Fenton and Ritz
(1989) that the prevalent protocol of assigning an isotopic value to a particular photosynthetic source, particularly a macroalgal species, based upon a single sample at
one point in time is not representative of dynamic shortterm (e.g. diurnal), long-term (e.g. seasonal) or spatial
variability in the 613C of the carbon fixed. This is in stark
contrast to pelagic-based systems, where inter- and intraannual variation in primary producer 613C within
oceanographic regions is quite small, although geographic variation may persist among regions (Saupe et al.
1989). In macrophyte-based systems, however, ecologists
utilizing 613C as a tool to explore organic carbon pathways would be well advised to carefully examine the spatial and temporal breadth of 613C variability in both
photosynthetic sources and consumers, as well as the dynamics between the inorganic carbon supply, kelp photosynthesis and growth rates, and nutrient availability. A
more complete appreciation of the mechanisms behind
the observed variability in ~ ~3C would contribute significantly to a better understanding of the autotrophic processes potentially driving the "bottom-up" dynamics of
aquatic food webs.
Acknowledgements. This research was supported by the National
Science Foundation, Division of Polar Biology and Medicine,
Grant ~ DPP-8421362. In addition to the agencies which provided
critical logistical support - U.S Coast Guard, Kodiak Air Station
and Adak Loran Station, U.S. Navy Airstation Adak, and U.S. Air
Force Air Base Shemya - we express our gratitude to the crew of the
RV "Alpha Helix" and the "gang of eleven" colleagues without
whom the 1987 cruise would not have accomplished half of its
objectives. We thank K. Winters and the staff of Coastal Science
Laboratories, Austin, Texas, for their concerted efforts in processing our multitude of ~ 1aC samples. D. Wilbur, School of Oceanography, conducted the DIC and CO 2 analyses. We also thank: B. Fry
and K. Dunton for their insightful interpretation of the initial kelp
613C variation data; M. Dethier, K. Dunton, B. Ebbesmeyer, E
Prahl and R. Thom for their review comments; and two anonymous
reviewers for their critical but constructive and enlighteningsuggestions. B. Feist, Fisheries Research Institute, University of Washington, provided valuable assistance in producing the figures. This
information was presented originally, and in part, in a poster at the
1988 Marine Science Meeting, New Orleans by Simenstad and Duggins (1988).
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