Limnol. Oceanogr., 55(5), 2010, 2097–2106
2010, by the American Society of Limnology and Oceanography, Inc.
doi:10.4319/lo.2010.55.5.2097
E
High incidence of invertebrate–chemoautotroph symbioses in benthic communities of
the New Zealand fjords
Rebecca J. McLeod,a,b,* Stephen R. Wing,a and Jennifer E. Skiltona
a Department
b Department
of Marine Science, University of Otago, Dunedin, New Zealand
of Chemistry, University of Otago, Dunedin, New Zealand
Abstract
In the New Zealand fjords, hydrogen sulfide production from decomposing forest litter is used by
chemoautotrophs to fix CO2[aq] and support benthic food webs. We used quantitative surveys and stable isotope
analyses to investigate the contribution of chemoautotrophy to shallow (50 m) and deep (400 m) benthic
communities in Doubtful and Bradshaw Sounds. Prevalence of bivalve–chemoautotroph symbioses varied
between shallow sites where large-bodied (# 50 mm) Solemya parkinsonii (Solemyidae) were common, and deepbasin sites where small-bodied (, 2 mm) Nucinella maoriana (Manzanellidae) dominated assemblages. d13C and
d15N of sediment indicated that the basal carbon source supporting chemosynthesis was likely decomposing forest
litter at 50 m, and decomposing marine algae at 400 m. An isotopic mass balance model weighted to community
composition and biomass indicated that the majority of carbon supporting communities at 50 m originated from
chemoautotrophy. Concentration of fatty acid biomarkers for heterotrophic bacteria (C15 and C17) were
correlated with the estimated amount of carbon from terrestrial sources, indicating that decomposing forest litter
is important in the system. Analysis of the trophic level of these macroinfaunal communities normalized to
biomass indicated that the communities sampled from 50 m were on average chemoautotrophic, whereas those
sampled at 400 m were on average heterotrophic. The reliance of benthic invertebrate communities on
decomposing forest litter and chemoautotrophy, particularly in shallow habitats, demonstrates close connectivity
between terrestrial and marine ecosystems in this region and illustrates how diverse food webs can be supported in
the shaded and quiescent inner fjord environments.
Since the discovery of communities supported wholly by
chemoautotrophy at deep-ocean hydrothermal vents (Corliss et al. 1979), numerous systems have been investigated
where methane and sulfide gases enable chemoautotrophic
bacteria to flourish and form the nutritional basis of food
webs (reviewed by Levin 2005). Observations of chemosynthetic communities on whale carcasses (Smith et al.
1989) led to predictions that production of hydrogen sulfide
within other types of organic deposits, such as forest litter,
likely provides conditions suitable for abundant production
by chemoautotrophic bacteria (Schmaljohann et al. 1990;
Bennett et al. 1994). Invertebrate–chemoautotroph symbioses have since been documented in sunken trees retrieved
from the deep sea (Dell 1987; Distel et al. 2002). In such
cases, the size and decomposition rate of the organic
deposit limits the lifetime of the assemblage. In areas where
inputs of forest litter are continuous, such as adjacent to
pulp mills (Louchouarn et al. 1997) or intact temperate
forests (McLeod and Wing 2009), the presence of
invertebrate–chemoautotroph symbioses are likely to be a
persistent feature. Global trends of deforestation (Ramankutty and Foley 1999), particularly in coastal areas, have
decreased natural inputs of forest litter to nearshore
environments and may therefore have altered the prevalence of such fauna.
Fiordland, in southwestern New Zealand, provides an
example of an intact remnant of coastal habitat, with
extensive temperate rainforest extending to the water’s
edge. The forest is encompassed in the Fiordland National
* Corresponding author: [email protected]
Park, and the coastal marine environments contained
within the 15 fjords are excluded from commercial
extraction under the Fiordland Marine Management Act
2005. The result is a relatively pristine marine and
terrestrial system. Fiordland therefore provides an excellent
setting to study connectivity between intact terrestrial and
marine environments in terms of spatial subsidies of
organic matter (OM). Large inputs of forest litter into the
fjords result in highly organic marine sediments (Glasby
1978; McLeod and Wing 2009; Smith et al. 2010) and there
are indications that widespread fermentation occurring
within the sediment drives methanogenesis (Schlesinger
1997) and extensive production of hydrogen sulfide (Brewin
et al. 2008). In a descriptive study of macroinfauna
inhabiting the deep basins (# 420 m) of the DoubtfulBradshaw fjord complex, Brewin et al. (2008) reported the
common yet patchy occurrence of taxa that are likely hosts
to chemoautotrophic bacteria, including Solemyidae, Manzanellidae, Lucinidae, Thyasiridae (all Mollusca: Bivalvia)
and Pogonophora. This finding highlights an interesting
question: What proportion of the biomass in these
communities is derived from chemoautotrophy?
Chemical tracer techniques including natural abundance
of stable isotopes and fatty acids (FAs) provide a powerful
means to detect and quantify relative inputs of sources of
OM to marine food webs (Alfaro et al. 2006; McLeod and
Wing 2007). Marine algae, terrestrial plants, and chemoautotrophic bacteria have characteristic values of d13C,
d15N, and d34S, which are transferred to consumers in a
predictable manner (DeNiro and Epstein 1978; Fry 2006).
In the New Zealand fjords, isotopic differences are
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McLeod et al.
particularly pronounced for d34S among marine algae
(, 18.8%), terrestrial plants (, 0%), and chemoautotrophic bacteria (, 220%; McLeod and Wing 2007). FAs
provide a complementary approach to stable isotopes, as
primary producers often have characteristic FAs that are
incorporated by consumers (Sargent et al. 1987; Arts et al.
2009). Chemoautotrophic bacteria that form symbioses
with clams including Solemya spp. (Solemyidae), Lucinidae, and Thyasiridae have FA profiles that are distinct
from heterotrophs, being dominated by cis-vaccenic acid
(18:1v7c; Conway et al. 1994; Fullarton et al. 1995;
McLeod and Wing 2007). This compound provides a
tracer for chemoautotrophic bacteria in food web studies
(McLeod and Wing 2007). Similarly, FAs containing 15
and 17 carbons are often employed as biomarkers of
heterotrophic bacteria (Alfaro et al. 2006; McLeod and
Wing 2009).
These chemical tracer techniques have been used in
recent years to unravel food webs in the New Zealand
fjords, where the importance of carbon fixed by bivalve–
chemoautotroph symbioses to the nutrition of higher
trophic level species has become apparent. Hagfish
(Eptatretus cirrhatus) are abundant scavengers and predators in the Doubtful-Bradshaw fjord complex and therefore
provide an isotopic integration of carbon sources used by
the benthic invertebrate community. Using a multiple
stable isotope approach (d13C, d15N, d34S), McLeod and
Wing (2007) demonstrated that hagfish in Doubtful Sound
obtain 38–51% of carbon from chemoautotrophic bacteria.
Further, evidence from d13C of bacterial biomarkers
indicated that the basal source of dissolved carbon fixed
by these bacteria was likely decomposing forest litter.
Carbon from free-living chemoautotrophic bacteria and
bivalve–chemoautotroph symbioses can, in some circumstances, make up a large proportion of the basal carbon
sources to important consumers in the system including sea
urchins (Evechinus chloroticus; Wing et al. 2008), blue cod
(Parapercis colias; Rodgers and Wing 2008), and the red
rock lobster (Jasus edwardsii; Jack et al. 2009), particularly
in the inner reaches of the fjords. These findings, along
with those of Brewin et al. (2008), suggest that a significant component of the macroinfauna inhabiting the
shallow deltas and deep basins of Doubtful and Bradshaw
Sounds feed upon, or symbiotically host, chemoautotrophic bacteria.
Using d13C and d15N of sediment and invertebrates
combined with quantitative infaunal surveys at 50- and
400-m strata, we investigated what proportion of the
macroinfaunal assemblages in Doubtful and Bradshaw
Sounds obtain carbon via chemoautotrophic bacteria.
Then, using the natural abundance of FA biomarkers, we
questioned whether those invertebrates with indeterminate
isotopic values were obtaining their nutrition from
chemoautotrophic bacteria or terrestrially derived OM via
heterotrophic bacterial pathways.
Methods
Site description—Doubtful and Bradshaw Sounds comprise a pair of interconnected fjords that extend , 40 km
Fig. 1. Location of benthic sampling sites in the DoubtfulBradshaw Sound fjord complex, Fiordland.
landwards of the open coast (Fig. 1). Sills are present at the
seaward end of all fjords in the complex, resulting in a
series of basin habitats that differ in depth. Deep sites were
positioned in Kellard Basin and Bradshaw Basin (both .
400 m maximum depth), which are the deepest basins
within Doubtful and Bradshaw Sounds respectively (see
Fig. 1). Shallow sites were positioned on fluvial deltas
offshore from river mouths in Crooked Arm and Bradshaw
Sound. These sites were representative of the soft sediment
habitat that comprises 78.5% of all shallow habitat within
the fjord complex (Wing et al. 2003). The fjord catchments
are contained within the Fiordland National Park where
there is extensive cover of intact temperate rainforest,
including a mixed assemblage of Nothofagus spp. and
podocarps (Baylis and Mark 1963). Steep topography and
high precipitation (6200–8000 mm yr21; Sansom 1984)
cause deposition of forest litter into the fjord marine
environment, resulting in highly organic sediment (Glasby
1978; McLeod and Wing 2009). The deep waters of the
main channels of Doubtful and Bradshaw Sound appear to
be well oxygenated; however, there are indications that
some of the tributary fjords experience hypoxia (Pickrill
1987; Brewin et al. 2008).
Sample collection and treatment—Samples were collected
in February 2008, in the inner reaches of Doubtful and
Bradshaw Sounds, at stations situated at , 50-m and ,
400-m depth (Fig. 1). At each station, six benthic samples
were collected with a box core sampler (surface area
0.06 m2, penetration depth # 500 mm), operated remotely
Benthic food web chemoautotrophy
from aboard the R/V Polaris II. The location of each
sample was positioned haphazardly within areas of
constant depth, as determined by an onboard depth
sounder. Within each box a subsample core (50-mm Ø,
400-mm depth) was taken, sliced into 100-mm lengths, and
frozen awaiting sediment analyses. The remaining sample
was divided into two, the upper 100 mm sieved through 1mm mesh, and the lower , 400 mm sieved through 5-mm
mesh. These mesh sizes were selected because of the highly
detrital nature of sediment, particularly at shallow sites,
coupled with the large volume of the samples making
sieving through finer mesh impractical. As the majority of
macroinfauna inhabit the upper 100 mm of sediment
(Quijón and Jaramillo 1996), a coarser mesh size was used
for sediment deeper than 100 mm, to detect large-bodied
burrowing taxa such as clams and shrimp. Extracted
infauna were sorted onboard and specimens removed for
chemical analyses. Invertebrates were placed in seawater to
allow gut contents to clear, then frozen (220uC). The
remaining sample was preserved in 70% ethanol with
seawater and returned to the laboratory.
In the laboratory remaining macroinfauna were picked
from samples, identified to the highest practical taxonomic
level, and counted. Generally, Polychaeta were identified to
family, Mollusca to species, and Crustacea to order. The
remaining taxa were mostly identified to phylum (e.g.,
Nemertea). Estimates of soft tissue biomass were made for
each taxon at each site. These estimates were based on
averages of measurements of soft tissue dry weight (dry
weight; dried in a desiccator at 40uC for 3 d) of up to five
individuals that represented the size range of each taxon.
Estimates of biomass density were then calculated.
Differences in the density of total macroinfauna and
total biomass were tested using a two-factor mixed model
with fjord (two levels random) and depth (two levels fixed,
orthogonal) as factors. We tested for interaction between
factors and also quantified the total number of taxa for
each site. Using PRIMER version 6 (PRIMER-E), BrayCurtis similarity indices of invertebrate abundance data
were calculated and the similarity percentages (SIMPER)
function used to determine the species accounting for 90%
of similarity in species composition within each site.
Analysis of d13C and d15N—Samples of sediment (from
the top 100 mm of three randomly selected cores at each
site) and macroinfauna were dried at 60uC for 3 d.
Invertebrate samples comprised either one whole individual, or many individuals if the quantity of one individual
was insufficient for analyses. Shells were removed from
mollusks. Samples were ground to a fine powder using a
mortar and pestle and sub samples of , 1 mg of
invertebrates and , 15 mg of sediment were analyzed for
d13C and d15N. Analyses were performed on a Europa Geo
(2) 20-20 mass spectrometer coupled with a Europa
automated nitrogen and carbon elemental analyzer in
continuous flow mode (precision: 0.2% for d13C and
0.3% for d15N). Analysis was calibrated to ethylenediaminetetraacetic acid laboratory standard reference (Elemental Microanalysis) and normalized to a range of
internal standards. Results are expressed in standard delta
2099
notation where, for example, d13C 5 [(Rsample/Rstd) 2 1] 3
1000 where Rsample 5 13C 12C and Rstd 5 13C 12C of Peedee
belemnite limestone. Rstd for d15N was atmospheric
nitrogen.
Isotopic mixing model—Invertebrates with values of
d15N significantly more deplete in 15N than terrestrially
derived OM (, 0%) indicated that they hosted chemoautotrophic bacteria. All taxa treated in this way were also
from taxonomic families that contain species known to host
chemoautotrophic bacteria. Values of d15N and d13C of
taxa believed to be primary consumers were then entered
into the IsoError mixing model (Phillips and Gregg 2001)
to estimate the contribution of macroalgae, suspended
particulate OM (SPOM), terrestrial OM, and chemoautotrophic bacteria to nutrition. Prior to modeling, isotopic
values of these taxa were corrected for trophic-level
associated fractionation using values of 22.3% for d15N
and 20.4% for d13C (McCutchan et al. 2003). A model was
constructed for each taxon and site combination and the
mean estimated source contributions were weighted to
biomass using the estimations described previously. Differences in the total biomass of carbon from primary
production by chemoautotrophic bacteria were tested using
a two-factor mixed model with fjord (two levels random)
and depth (two levels fixed, orthogonal) as factors. We
tested for interaction between factors.
Analysis of community trophic level—Using information
from a two-source isotopic mixing model for d13C with new
production and recycled production as basal carbon end
points, we estimated the d15N for the mixture of basal
nitrogen sources from these two end points for each taxon.
We then calculated site-specific trophic level for each taxon
based on isotopic enrichment of +2.3% d15N per trophic
level. These data on taxa-specific trophic level were then
used to calculate trophic level by sample, normalized to
biomass of each taxon. We then tested for differences in
average trophic level, normalized to biomass for the
macroinfaunal community using a two-factor mixed model
with fjord (two levels random) and depth (two levels fixed,
orthogonal) as factors. We tested for interaction between
factors.
Quantification of FAs—Lipid was extracted from 25-mg
subsamples (n 5 18) of dried homogenized macroinvertebrates that ranged considerably in values of bulk tissue
d13C and d15N following Bligh and Dyer (1959). The lipid
extract was treated with analytical grade sulfuric acid in
methanol solution and underwent acid-catalyzed transesterification at 80uC for 3 h. All chloroform and hexane used
were pesticide residue analysis grade and the methanol used
was analytical reagent. FA methyl esters (FAMEs) were
extracted in hexane and water, evaporated under nitrogen,
reconstituted in 700 mL dichloromethane, and stored at
8uC.
FA composition was determined by gas chromatography
mass spectrometry on a 6890N Network GC System
(Agilent Technologies) equipped with a 5975B inert XL
EI/CI MS (Agilent Technologies). FAMEs were separated
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McLeod et al.
two depth zones (Fig. 3), with the highest estimated
biomass occurring at the 50 m sites (. 0.5 g dry weight
0.06 m22), and the lowest biomass at the deepest sites
(, 0.1 g dry weight 0.06 m22). Results of ANOVA with
depth nested within fjord revealed these differences to be
significant between depth zones (F3,21 5 8.89, r2 5 0.56,
p 5 0.0005; see Fig. 3). There was no significant interaction
between fjord and depth in the model.
Fig. 2. Density of macroinfauna at four sites in the
Doubtful-Bradshaw fjord complex (mean values 6 1 SE). Results
of a pair-wise Tukey’s test indicate significant differences among
sites not connected by the same letters. The number of taxa
recorded at each site is given.
on a Zebron (ZB) Wax Plus capillary column, 30 m 3
0.25 mm i.d., 0.25 mm film (Phenomenex). The column
oven temperature was ramped from 120uC to 250uC at 8uC
min21 and then held at this temperature for 9 min. FA
peaks were identified by retention time matching with
composite standards (Sigma-Aldrich: polyunsaturated FA
No. 1, Supelco 37 component FAME mix) and confirmed
using mass spectrometry. FAs were then expressed as the
percentage of the sum of short-chain FA (, 20 C chain
length).
The abundances of C15 and C17 FAs, previously used as
biomarkers for heterotrophic microbes (Boschker et al.
1999; Pancost and Sinninghe Damsté 2003), and cisvaccenic acid (18:1v7c), commonly used as a biomarker
for chemoautotrophic bacteria (Conway and McDowell
Capuzzo 1991; McLeod and Wing 2007), were determined
for each taxon, and compared to estimations of incorporation of terrestrial OM from the isotopic mixing model.
We used general linear models to test these relationships
with pair-wise data per taxon on the estimated fraction of
terrestrial OM from the mass balance mixing model and
concentration of each FA biomarker.
d13C and d15N of sediment—Isotopic values of surface
sediments ranged between 228.05% and 219.74% for
d13C and 20.21% and 4.35% for d15N (Fig. 4a). For both
d13C and d15N, there was a trend of increased values with
depth, with the most 13C- and 15N-enriched values
occurring at 400 m depth in Doubtful Sound. The isotopic
values for sediment from 50 m sites was similar to
terrestrially derived OM, whereas the isotopic values for
sediment from the 400 m sites was similar to marine algae.
d13C and d15N of macroinvertebrates—Macroinfaunal
taxa varied considerably in d13C (from 231.56% to
217.18%) and d15N (from 213.12% to 11.66%; Fig. 4b).
A complete list of taxon-specific isotopic values is provided
in Table 2. The majority of taxa sampled had values of
d13C and d15N similar to marine algae (phytoplankton and
macroalgae). For example, the filter-feeding bivalve Neilo
australis collected at 50 m and 400 m depth in Bradshaw
Sound had values of d13C and d15N similar to SPOM (N.
australis d13C , 219% and d15N , 5%). Some depositfeeding infauna, including Capitellidae and Flabelligeridae,
had values of d13C that suggested partial contribution of a
13C-depleted source (chemoautotrophic bacteria and/or
terrestrial OM). Five taxa had isotopic values that were
not consistent with incorporation of marine algae or
terrestrial OM (values of d15N , 21%). These taxa
included the bivalves Solemya parkinsonii, Nucinella
maoriana and Thyasira peregrina. Predatory nemerteans
varied considerably in both d13C (from 231.00% to
219.72%) and d15N (from 211.38% to 8.45%). There
were no significant relationships between isotopic values
and depth or fjord; however, the most negative values of
d13C and d15N were measured only at the 50-m sites
(Fig. 4b).
Results
Description of macroinfaunal assemblages—Results of
analysis of variance (ANOVA) with depth nested within
fjord revealed significant differences in the abundance of
macroinfauna among sites (F3,24 5 3.39, r2 5 0.29, p 5
0.034; Fig. 2), with a significant effect of fjord (t 5 22.49, p
5 0.021). Infauna were measured at higher abundance at
Doubtful Sound 50 m than at the same depth stratum in
Bradshaw Sound. Although there was a trend of Doubtful
Sound 50 m having the highest infaunal abundance of all
sites in the study, this pattern was not statistically
significant. There was no significant interaction between
fjord and depth in the model. A summary of the abundance
of each taxon is provided in Table 1.
Estimates of total macroinfaunal biomass (soft tissue dry
weight) show strong patterns in total biomass between the
Isotopic mixing models—Results of the isotopic mixing
models, weighted to estimates of taxon biomass density,
suggest that multiple sources of OM supported standing
macroinfaunal biomass at all sites studied, including
chemoautotrophic bacteria, macroalgae, SPOM, and terrestrial OM. At all sites, terrestrial OM incorporation (not
including that indirectly incorporated by chemoautotrophic
bacteria) was the smallest contributor. Chemoautotrophic
symbionts were present in all of the assemblages studied,
and comprised between 0.57 and 1.06 g dry weight 0.06 m22
of biomass (Fig. 5), or 21–65% of the total biomass in the
communities at 50 m, and 10–35% of the biomass of
communities at 400 m.
Results of ANOVA revealed significant differences in
biomass of carbon from primary chemoautotrophy among
depth strata, with higher amounts of chemoautotrophic
Benthic food web chemoautotrophy
2101
Table 1. Mean (6 1 SE) percentage of total density of taxa recorded at each site. Taxa identified by SIMPER as accounting for
#90% of within-site similarity are in bold.
Bradshaw Sound
Taxon
Doubtful Sound
50 m
400 m
50 m
400 m
0.3160.31
2.60±0.97
0.0060.00
8.09±4.35
4.69±2.20
0.0060.00
13.72±3.76
5.22±1.72
0.0060.00
14.20±5.52
9.57±3.89
5.12±2.99
0.0060.00
2.35±1.10
0.3160.31
0.6360.63
0.0060.00
0.7460.74
4.1764.17
0.0060.00
0.0060.00
8.01±3.60
1.8861.13
0.5160.51
2.6761.70
0.0060.00
0.0060.00
1.0060.64
3.0661.94
1.1561.15
0.4360.43
0.0060.00
1.6960.79
0.0060.00
0.0060.00
1.5861.14
0.4360.43
1.2861.28
0.5460.54
2.84±1.46
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.7260.72
0.5760.57
0.0060.00
44.35±7.00
0.4360.43
0.0060.00
1.2861.28
1.54±0.70
1.4560.78
0.2460.24
0.0060.00
13.07±2.89
1.1860.75
0.0060.00
8.27±2.71
0.5360.34
0.0060.00
6.71±1.63
0.0060.00
0.1760.17
0.0060.00
0.0060.00
0.1760.17
0.3460.34
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.0060.00
47.39±9.71
2.8661.20
0.0060.00
0.6260.62
2.1360.87
0.0060.00
2.6961.39
0.0060.00
0.5760.57
0.0060.00
0.9860.64
12.43±4.39
0.0060.00
0.0060.00
2.53±1.12
3.59±1.41
2.2962.29
0.0060.00
0.5760.57
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.3660.36
12.84±3.42
0.0060.00
0.6560.65
0.0060.00
1.6061.23
Mollusca
Solemya parkinsonii
Neilo australis
Thyasira peregrina
Nucinella maoriana
Divaricella huttoniana
Nucula bollonsi
Other bivalves
Gastropods
Scaphopods
Opisthobranchs
0.9160.62
0.6060.60
2.5261.90
0.0060.00
0.8860.56
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.0060.00
3.1261.98
4.60±3.18
1.3960.91
21.66±7.49
0.0060.00
0.4360.43
0.0060.00
0.0060.00
0.0060.00
0.7260.72
2.41±0.60
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.6760.67
0.0060.00
0.0060.00
0.5760.57
40.29±14.65
0.0060.00
1.7161.15
1.5960.80
0.4160.41
0.5760.57
0.0060.00
Echinodermata
Echinocardium cordatum
Ophiuroidea (.20-mm disc diameter)
Ophiuroidea (,10-mm disc diameter)
Holothurians
2.5561.90
2.1861.02
3.30±1.62
0.3760.37
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.0060.00
4.29±1.58
0.0060.00
0.0060.00
0.0060.00
0.0060.00
0.8260.82
0.0060.00
Annelida
Acoetidae
Capitellidae
Cirratuliidae
Cossuridae
Dorvilleidae
Eunicidae
Flabelligeridae
Glyceridae and Goniadidae
Longosomatidae
Lumbrineridae
Maldanidae
Nephtyidae
Onuphidae
Ophellidae
Orbiniidae
Paraonidae
Pectinariidae
Phyllodocidae
Polynoidae
Scallibregmatidae
Sigalionidae
Spioniidae
Syllidae
Terebellidae
Trichobranchiidae
Unidentified polychaete A
Nemertea
0.0060.00
1.0861.08
0.8860.88
1.3061.30
Crustacea
Amphipoda
Large crustacea (e.g., Thalassinia, Galathea)
0.9460.94
0.9760.64
3.69±1.73
0.0060.00
5.97±2.06
0.6760.67
6.96±3.08
1.7661.21
Sipuncula
0.0060.00
0.4360.43
0.0060.00
1.7961.22
biomass at the 50-m depth stratum (F3,21 5 5.64, r2 5
0.446, p 5 0.0054). There was no significant interaction
between fjord and depth in the model.
FA composition of macroinvertebrates—The composition
of FA compounds differed among invertebrates selected
from across the range of d13C and d15N values. FAs were
analyzed specifically to question whether those invertebrates with values of d15N between 0% and 5% were
obtaining carbon from terrestrial OM or chemoautotrophic
bacteria. Results of a general linear model indicated that
there was a significant positive relationship between the
proportion of nutrition derived from terrestrial OM and
the concentrations of the FA biomarkers for heterotrophic
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McLeod et al.
Fig. 3. Biomass of macroinfauna from the four study sites in
the Doubtful-Bradshaw fjord complex (mean values 6 1 SE).
Results of a pair-wise Tukey’s test indicate significant differences
among sites not connected by the same letters.
bacteria (C15 and C17; F1,16 5 15.70, r2 5 0.495, p 5 0.0011;
Fig. 6). The relationship between 18:1v7c, a biomarker for
chemoautotrophic bacteria, and the fraction of carbon
from terrestrial OM was not significant, suggesting that the
relatively 13C- and 15N-depleted values of the macroinvertebrates analyzed were not due to partial contributions of
chemoautotrophic bacteria, but rather to terrestrial OM via
heterotrophic bacteria.
Analysis of community trophic level—Results of ANOVA
revealed significant differences in the mean trophic level of
infaunal communities (normalized to biomass) among
depth strata (F3,21 5 13.168, r2 5 0.653, p 5 0.0001;
Fig. 7). At the 50-m depth stratum at Doubtful Sound, a
mean trophic level for the community between 0 and 0.5
indicated dominance of autotrophy, and similarly a value
between 0.5 and 1 at the 50 m depth stratum in Bradshaw
Sound indicated a large influence of autotrophy. Mean
trophic levels greater than 1 in the two 400-m sites
indicated a higher biomass of secondary consumers. An
interaction between fjord and depth was detected ( p 5
0.0068).
Discussion
The results of this study highlight the significance of
microbial processing of detritus in a nearshore community
inhabiting highly organic soft sediment. Of particular note
is the contrast between assemblages inhabiting 50 m and
400 m depth strata, and the origin of OM that is supporting
microbial activity at each stratum. Assemblages in the
shallow stratum inhabit highly organic sediment that has
originated from adjacent temperate rainforest. These
assemblages are relatively high biomass that is dominated
by the large-bodied chemoautotrophic bacterial–clam
symbiosis S. parkinsonii, which comprises 21–65% of the
total infaunal biomass at this stratum. In contrast,
assemblages at 400 m have lower infaunal biomass and
are characterized by high abundances of the chemoautotrophic bacterial–clam symbiosis N. maoriana. These
Fig. 4. Values of d13C and d15N (mean values 6 1 SE) of (a)
sediment samples and (b) macroinfaunal primary consumers
collected from sites in Doubtful Sound (squares) and Bradshaw
Sound (circles). Values for the 50-m sites are given in gray, and
400-m sites in black. The isotopic values of sources of OM
(McLeod and Wing 2007) are indicated (open squares). Isotopic
values have not been corrected for trophic level–associated
fractionation. ter OM: terrestrially derived OM.
assemblages inhabit organic sediment that is likely of
marine algal origin. These conclusions are supported by
measurements of stable isotope ratios of carbon, nitrogen,
and sulfur, and of FA compounds of microbial origin.
Large differences in values of d13C and d15N for
terrestrial OM and marine algae provided a basis for
determining the origin of the organic component of
sediment from each stratum, and these values indicated a
shift in the origin of OM with depth. Although sediment at
the shallower depth stratum (50 m) was dominated by
Benthic food web chemoautotrophy
2103
Table 2. Values of d13C and d15N (%), and % carbon and nitrogen content of macroinfauna collected from sites in Doubtful (Dbt)
and Bradshaw (Brd) Sounds, Fiordland (see Fig. 1 for site locations). For taxa where three or more samples were analyzed from a site,
mean values (6 1 SE) are given.
d13C (%)
d15N (%)
%C
%N
Fjord
Depth (m)
Polychaetea
Capitellidae*
Capitellidae
Capitellidae*
Cirratulidae
Dorvilleidae
Eunicidae*{
Flabelligeridae*
Flabelligeridae*
Flabelligeridae*
Flabelligeridae*
Goniadidae or Glyceridae*
Lumbrineridae*{
Lumbrineridae{
Maldanidae{
Maldanidae*{
Nephtyidae*
Nephtyidae
Onuphidae
Orbiniidae
Polynoidae
Polynoidae
Scalibregmatidae
Scalibregmatidae
Spionidae*
Spionidae*
Spionidae*
Terebellidae{
Terebellidae{
Trichobranchidae{
222.00
223.60
220.76
221.63
222.08
221.67
222.18
224.86
224.35
221.44
219.46
221.04
222.94
221.45 (0.59)
220.83
218.29
222.35
219.20
222.69
219.51
221.47
222.95
221.00
219.03
220.51
219.49
220.63
219.71
221.81
5.63
7.06
8.43
8.48
6.35
8.09
3.42
0.73
20.39
5.67
10.12
6.80
4.11
5.30 (1.87)
9.18
6.70
3.02
9.36
6.76
8.57
7.66
7.70
8.32
7.00
6.38
7.47
4.27
11.06
10.12
38.31
33.94
32.00
28.39
38.95
42.92
18.39
11.46
22.83
23.06
44.86
42.16
37.53
18.41 (1.61)
39.38
30.58
34.49
38.76
33.17
39.32
42.36
30.53
30.00
40.37
39.01
34.24
31.29
40.72
40.86
10.82
5.87
6.94
5.22
7.63
10.64
4.39
2.70
5.75
5.35
11.23
10.22
10.62
4.25 (0.29)
9.57
7.96
9.47
9.88
8.02
8.23
10.60
6.67
8.18
8.75
9.13
7.83
6.62
10.63
10.86
Brd
Brd
Dbt
Brd
Brd
Dbt
Brd
Dbt
Dbt
Dbt
Brd
Brd
Dbt
Brd
Dbt
Brd
Dbt
Brd
Brd
Brd
Brd
Brd
Dbt
Brd
Brd
Dbt
Brd
Dbt
Brd
50
400
400
400
50
400
50
50
50
400
50
50
50
50
400
50
50
400
50
50
400
400
400
50
400
400
50
400
50
Bivalvia
Neilo australis{
N. australis*{
Nucinella maoriana*{
Solemya parkinsonii{
S. parkinsonii{
Thyasira peregrina*
219.08
218.98
233.60
231.07 (0.16)
231.00 (0.30)
224.82
4.13
6.12
22.10
211.93 (0.48)
212.22 (0.46)
27.51
38.79
37.02
41.69
40.72 (1.80)
39.52 (0.57)
41.89
8.93
9.30
8.48
10.42 (0.25)
10.03 (0.12)
6.40
Brd
Brd
Dbt
Brd
Dbt
Brd
50
400
400
50
50
400
Echinodermata
Ophiuroidea
Echinocardium cordatum{
Holothuria{
219.25 (1.31)
220.73
220.57
6.62 (0.27)
11.66
7.81
23.57 (2.27)
40.25
34.14
3.61 (0.52)
11.20
9.91
Dbt
Dbt
Brd
50
50
50
231.00
219.72
228.50
224.94
227.06
211.38
8.45
1.74
26.87
20.38
46.06
40.15
43.71
44.01
41.97
11.57
10.63
12.42
12.15
11.06
Dbt
Dbt
Brd
Brd
Dbt
50
50
400
400
400
Nemertea
Nemertea{
Nemertea
Nemertea
Nemertea
Nemertea{
* Samples comprising multiple individuals.
{ Samples analyzed for FA composition.
terrestrial OM, at the deeper sites (400 m) values of d13C
and d15N more enriched in 13C and 15N were consistent
with a larger input of OM from marine algae. The source of
this algae could potentially include particulate OM from
the pelagic food web and particulate macroalgae from the
reefs that fringe the fjords. These findings are consistent
with scanning electron microscopy analyses of suspended
sediment loads conducted throughout Fiordland by Pickrill
(1987), and analysis of surface sediment samples for
terrestrial and marine biomarkers by Smith et al. (2010).
Of all the infaunal taxa analyzed for stable isotopes from
both strata, only a small proportion had values that were
consistent with dominance of chemoautotrophic bacteria,
present either endosymbiotically or as a major food source.
Although d13C is similarly deplete in 13C for chemoautotrophic bacteria (S. parkinsonii , 231%), terrestrial OM
2104
McLeod et al.
Fig. 5. Estimated biomass of carbon coming from primary
production by chemoautotrophs in the macroinfauna from the
four study sites in the Doubtful-Bradshaw fjord complex (mean
values 6 1 SE). Results of a pair-wise Tukey’s test indicate
significant differences among sites not connected by the
same letters.
(229%; McLeod and Wing 2007), and some species of red
algae (e.g., Hymenena offinis 232%; C. Hurd unpubl.),
values of d15N , 0% appear to be unique to chemoautotrophs (Conway et al. 1994), which in this study were
defined as S. parkinsonii, N. maoriana, and T. peregrina.
These species belong to families that contain multiple
chemoautotrophic bacteria–clam endosymbioses (Beesley
et al. 1998). Despite these species comprising large
proportions of the total infaunal biomass, the majority of
taxa appeared to be supported predominantly by OM of
marine algal origin at both strata. These taxa represent a
wide range of functional feeding guilds, including suspension feeders, grazers, and surface deposit feeders. A small
proportion of taxa had isotopic values that were intermediate between marine algae and a 13C- and 15N-deplete end
member, and it was therefore not possible to distinguish
among the multiple potential end members fueling these
taxa based solely on d13C and d15N. For these taxa, we
analyzed the abundances of FAs that were indicative of
Fig. 6. Estimates of the proportion of nutrition derived from
terrestrially derived OM (fter OM) vs. the percentage of the
heterotrophic bacterial biomarkers C15 and C17 compounds (% of
total short-chained FAs), for individual macroinfaunal taxa
(Table 2).
Fig. 7. Estimated mean trophic level for macroinfauna from
the four study sites in the Doubtful-Bradshaw fjord complex.
Results of a pair-wise Tukey’s test indicate significant differences
among sites not connected by the same letters.
chemoautotrophic or heterotrophic bacteria. A lack of
correlation between estimates of the contribution of
terrestrial sources (from mass balance models using d13C
and d15N) and abundance of the chemoautotrophic
indicator cis-vaccenic acid suggested that these taxa were
unlikely to have had partial contributions of chemoautotrophic bacteria. However, there was a significant positive
relationship with estimates of the contribution of terrestrial
sources and the abundance of heterotrophic microbial
biomarkers (C15 and C17 FAs; McLeod and Wing 2009),
which indicated that these taxa had incorporated a mixture
of marine algae and heterotrophic bacteria. To the best of
our knowledge, heterotrophic microbes are the only source
of these FAs, and animals are not believed to be capable of
biosynthesizing these compounds.
By coupling site- and taxon-specific estimates from mass
balance models with quantitative measurements of community composition, we were able to construct estimates at
the community level for incorporation of OM sources and
trophic structure. At the 50-m depth contour, the majority
of carbon contained within the entire macroinfaunal
community had chemoautotrophic origins, resulting in a
community that was, on average, chemoautotrophic.
Although a small proportion of the taxa sampled appeared
to support chemoautotrophic endosymbionts, mass balance
models at these sites estimated that their collective biomass
contributed a majority of the total carbon sequestered by
the entire macroinfaunal community. Further, an analysis
of the trophic level for Doubtful 50 m and Bradshaw 50 m
indicated that these shallow communities were on average
autotrophic (trophic level , 1). In contrast, the communities at the 400-m sites had higher average trophic levels
(. 1), which is consistent with heterotrophy dominating,
and a larger fraction of primary and secondary consumers
being present. It is also likely that the OM fueling these
deeper communities had undergone more extensive microbial processing as it settled through the water column,
which may also contribute to higher mean trophic levels for
these communities.
In this comparatively intact coastal landscape, we have
found that a large proportion of the benthic macroinfaunal
Benthic food web chemoautotrophy
community obtains chemosynthetically fixed carbon and
that at a depth of 50 m in close proximity to river mouths,
chemosynthesis is fueled by fermentation of forest litter.
This community forms the basis of the benthic food web
and supports a rich diversity of species in the New Zealand
fjords. Evidence that carbon from this pathway directly
enters the fjordic food web comes from studies of higher
trophic level benthic consumers such as hagfish (E.
cirrhatus) and estuarine populations of the common wrasse
(Notolabrus celidotus) (McLeod and Wing 2007; McLeod et
al. 2010). There is also evidence that this chemoautotrophic
production forms an important alternative carbon source
for inner fjord subpopulations of coastal fish and
invertebrates such as red rock lobster (J. edwardsii) and
blue cod (P. colias), as well as critical kelp forest species
such as sea urchins (E. chloroticus; Rodgers and Wing 2008;
Wing et al. 2008; Jack et al. 2009). This mechanism for food
web connectivity demonstrates a strong coupling between
terrestrial and marine systems and helps to explain how
diverse food webs can be supported in the shaded and
quiescent inner fjords where both pelagic and benthic
production are low.
The findings of this study are highly likely to be
applicable to similar settings worldwide. Extensive networks of temperate fjords with intact forest occur on the
west coasts of South America (Patagonia) and North
America (British Columbia and Alaska). These regions
similarly experience very high precipitation and levels of
sedimentation (Silva and Prego 2002; Nuwer and Keil 2005;
Sepúlveda et al. 2009), although to the best of our
knowledge similar studies of OM flux through infaunal
communities have not been conducted to date. Such
knowledge would be particularly relevant given the
exploitation of higher trophic level species in these regions
that are likely supported by such macroinfaunal communities, and potential changes to sediment chemistry caused
by the dramatic increase in aquaculture developments in
the Chilean fjords (Pascual et al. 2009).
Connectivity in food webs is an important source of
stability, and in this case the connectivity among a large
range of basal carbon sources including forest litter and
chemoautotrophy provides an important carbon subsidy to
the marine food web. Though these food webs are largely
supported by autochthonous sources such as phytoplankton and macroalgae, the pathways for incorporation of
allochthonous sources are an important structural feature
of this relatively intact coastal landscape for maintenance
of productivity and biodiversity.
Acknowledgments
We thank Russell Frew, Kim Hageman, Karen Lavin, Ruma
Ghosh, and Robert Alumbaugh (Department of Chemistry,
University of Otago), and staff at the National Isotope Centre at
the Institute of Geological and Nuclear Sciences, Wellington, for
providing technical support for isotopic and fatty acid analyses.
Thank you also to staff at the Department of Marine Science and
the Portobello Marine Laboratory, crew of the R/V Polaris II,
Andy Hicks, Michelle Beritzhoff, Nicola Beer, Lucy Jack, Chelsie
Archibald (Otago University), Bruce Marshall (Te Papa), Kareen
Schnaebel, and Ashley Rowden (National Institute of Water and
Atmospheric Research, Wellington). Comments from two anony-
2105
mous reviewers were gratefully received. This research was funded
by a University of Otago Research Grant (S.R.W.).
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Associate editor: H. Maurice Valett
Received: 01 March 2010
Accepted: 26 May 2010
Amended: 15 June 2010