Marine Biology (2018) 165:172

https://doi.org/10.1007/s00227-018-3430-z

ORIGINAL PAPER

Biological characteristics of the rafting bivalve Gaimardia trapesina

in the Southern Ocean
Eleonora Puccinelli1   · Charles E. O. von der Meden2   · Christopher D. McQuaid3   · Isabelle J. Ansorge1

Received: 27 January 2018 / Accepted: 1 October 2018 / Published online: 13 October 2018
© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract
Rafting invertebrate species represent an important link for the dispersal and colonisation of islands in the Southern Ocean.
They are sensitive to changes in hydrodynamics through effects on transport and food availability, particularly in the case of
filter-feeding species. This gives them the potential to act as sentinels of environmental change. The rafting kelp-associated
Gaimardia trapesina is one such species, widely distributed in the Southern Ocean. In 2015 and 2016, the size structure, diet,
and distribution of G. trapesina were examined around the Sub-Antarctic Prince Edward Islands (PEI) to establish benchmark
data and explore their potential use for monitoring long-term change. Gaimardia trapesina and its potential food sources
were collected and analysed for size structure, attachment strength, and diet, using stable isotope and fatty acid analyses.
The populations examined were dominated by relatively small individuals. The strength of attachment to kelp blades was
low and the byssal threads showed high elasticity. The PEI lie in the path of the west–east flowing Antarctic Circumpolar
Current and the highest abundances of G. trapesina were found on the downstream sides of both islands, while the species
was absent from the western, upstream coasts. Both diet analyses and SIAR mixing models indicated that G. trapesina feeds
on suspended particulate matter, while kelp particles contribute minimally to the diet. Considering the wide distribution of
G. trapesina, its importance as food for birds and fish, and its sensitivity to environmental conditions, there is good potential
to use this species as an indicator of environmental change in the Southern Ocean.

Introduction

Rafting invertebrate species represent an important link in

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* Eleonora Puccinelli
eleonorapuccinelli@gmail.com
1
Department of Oceanography, Marine Research Institute,
University of Cape Town, Rondebosch, Cape Town 7701,
South Africa
2
South African Environmental Observation Network
(SAEON), Egagasini Node, Foretrust Building, Martin
Hammerschlag Way, Roggebaai, Cape Town 8012,
South Africa
3
Department of Zoology and Entomology, Rhodes University,
P.O. Box 94, Grahamstown 6140, South Africa
the dispersal of marine invertebrates that colonise islands
and mainland coasts (Norkko et al. 2000; Fraser et al. 2011).
Such species are generally characterized by wide geo-
graphic distributions, having the ability to survive as adults
and recruits on floating material or ‘drifters’ for extended
periods (Scheltema 1988; Kinlan et al. 2005; Nikula et al.
2010). These characteristics allow population exchange and
genetic structure on local and trans-oceanic spatial scales
that can exceed the long-distance dispersal of swimming
larvae (Worcester 1994; Cowen et al. 2000; Weersing and
Toonen 2009; Fraser et al. 2011).
Several factors determine the dispersal and successful
establishment of rafting species, including the presence of
floating objects or surface drifters, current speed and direc-
tion, availability of food for adult and juvenile stages, and
the physiological ability of the organism to settle on and
remain attached to the raft (Helmuth et al. 2005; Gutow et al.
2009; Fraser et al. 2011). Drifters, such as macroalgae or
plastic debris, provide alternative and transitional habitats

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for invertebrates and fishes, potentially offering refuge from
predators and, in some instances, acting as feeding grounds,
as is the case for juvenile fishes associated with floating
seaweed clumps (Helmuth et al. 1994; Tzetlin et al. 1997;
Norkko et al. 2000; Vandendriessche et al. 2007).
Ocean currents represent one of the main drivers of spe-
cies distribution (Pineda et al. 2007; Leese et al. 2010) and
the speed and direction of water flow can influence the set-
tlement location of marine species. Species can, for instance,
be transported to areas that lack suitable substratum or pro-
vide unsuitable environmental conditions for settlement
(Cowen and Sponaugle 2009; von der Meden et al. 2015).
Food availability is a central factor for the survival, repro-
duction, and distribution of both adult and juvenile stages
(Connell 1985; Figueiras et al. 2002). Quality and quantity
of food for adults can influence the reproductive rate and
metabolism of species (Puccinelli et al. 2016c). Likewise,
food is extremely important for juveniles and propagules,
which drift for variable periods, especially in the case of
species which rely on food resources in the water column
(Daly 1990; Kelly et al. 2000).
Gaimardia trapesina is a rafting bivalve species of near-
shore Sub-Antarctic and Antarctic waters that lives attached
to the giant kelp Macrocystis pyrifera (Smith 2002). It is
widely distributed in the Southern Ocean, from the Antarctic
peninsula, Tierra del Fuego, and the Falkland Islands east-
wards to South Georgia, Prince Edward, Crozet, and Ker-
guelen islands to Heard and McDonald Island, and at least
as far as Macquarie and New Zealand’s Auckland Islands
(Kenny and Haysom 1962; Powell 1979; Adami and Gor-
dillo 1999; Castilla and Guiñez 2000; Ituarte et al. 2001;
Zelaya 2005; Barnes et al. 2006). The species does not have
a free-living larval stage, but broods its young internally,
making it possible to drift over large scales with juveniles
recruiting to the drifting kelp (Helmuth et al. 1994; Itu-
arte 2009). It is a substantial food source for intertidal and
inshore feeding birds in Sub-Antarctic areas, most signifi-
cantly for the kelp gull (Larus dominicanus), but also for
the lesser sheathbill (Chionis minor) which is an endemic
shorebird at the Prince Edward Islands (PEI; Blankley 1981;
Hockey 1988). Gaimardia trapesina is also a food source of
the nototheniid fish Paranotothenia magellanica (Gon and
Heemstra 1990). Studies have suggested that the oceano-
graphic conditions close to the PEI are changing as a con-
sequence of a southward shift of the Sub-Antarctic Front
(SAF; Perissinotto and Duncombe Rae 1990), resulting in
a shift in food availability for benthic organisms living in
close proximity to these islands (Allan et al. 2013; von der
Meden et al. 2017).
Under scenarios of global climate change, the marine
environments through which benthic populations disperse,
feed, and settle are likely to change as a consequence of
ocean acidification, alteration of the ocean currents that
13
Marine Biology (2018) 165:172
transport larvae and rafting species, and effects on food
sources (Harley et al. 2006). Investigating the biology of
rafting species is, therefore, increasingly important to our
understanding of population vulnerability and persistence.
Together with data on food quality and availability, there is
a need to understand the mechanical ability of rafting organ-
isms to remain attached to floating material and to recruit in
the extreme conditions of the Southern Ocean.
Susceptibility to physical disturbance is a fundamental
part of this dynamic, as demonstrated for several marine
invertebrates that rely on morphological resistance and
attachment strength for defense against mobile predators
and hydrodynamic forces (Denny 1987; Silva et al. 2008).
The biological characteristics of bivalves, including shell
morphology, reproductive ability, and attachment strength,
have been examined to gain insight into their capacity for
invasion, competition, and resilience (Denny 1987; Zardi
et al. 2007; Silva et al. 2008; Nicastro et al. 2010). As such,
attachment strength is a particularly useful feature to study,
since it depends on an energetically intensive, rapid response
to short-term changes in environmental conditions. With the
strong back and forth movement of swell and wave action,
organisms attached to flexible seaweeds and kelp experi-
ence strong inertial forces that are completely unlike the
forces experienced by those attached to immobile benthic
substrata (Davenport and Wilson 1995). Investigating how
mesoscale conditions (food regime) and physiological ability
(attachment strength) shape populations of G. trapesina at
the PEI presents a useful case study for bivalves living on
macroalgae rather than rocky substrata.
The PEI are recognised as ‘sentinels’ of climate change
(Ansorge et al. 2014), and G. trapesina presents an acces-
sible, sessile, widely distributed indicator species for long-
term ecological research in the Southern Ocean. It is directly
dependent on a keystone habitat-forming species (the giant
kelp), and, being a filter feeder, is likely to be affected by
local oceanographic conditions. Currently, little is known
about the local distribution, size structure, attachment
strength, diet, or trophic position of G. trapesina (Adami
and Gordillo 1999). This study aims to establish some of
these fundamental biological, physiological, and trophic
characteristics at the PEI to provide benchmarks for future
studies using G. trapesina as a bioindicator.
Materials and methods
This study was conducted on board the SA Agulhas II during
the annual relief voyages to the PEI under the South African
National Antarctic Programme. The samples were collected
from the kelp Macrocystis pyrifera, which was present at all
near-shore stations around the PEI (Fig. 1). Four stations
Marine Biology (2018) 165:172 Page 3 of 17  172
Fig. 1  Map showing stations
off Prince Edward archi-
pelago where kelp was present,
sampled in April 2015 (A,
red color) and 2016 (B, black
color). Gaimardia trapesina
was present at stations: 1A/B,
2A, 2B, 3A, 3B, 4A, 7B, 10B,
11B. See Table S1 for station
coordinates
were sampled in 2015 and 12 additional stations were sam-
pled in 2016.
Sample collection
Size structure and attachment strength
Samples of kelp frond were collected at each of nine stations
around Marion Island and six stations around Prince Edward
(Fig. 1). Using the ship’s dinghy, collections involved visu-
ally searching for G. trapesina on kelp fronds at the water’s
surface. Where no G. trapesina were observed, samples of
kelp were collected haphazardly. At each station, five 1-m
sections of fronds were brought back to the ship’s laboratory,
where the shell lengths of all G. trapesina were measured.
Shell-length measurements were made on all individuals
found on five haphazardly selected blades collected at each
site where G. trapesina was present (Fig. 1). Shell length
was measured as the maximum length from the umbo to the
growing edge using Vernier calipers (± 1 mm). To evaluate
differences in size structure between islands and among sta-
tions, the shell-length data were divided in five size classes
expressed in mm: Class A (≤ 5 mm), Class B (5 < 10 mm),
Class C (10 < 15 mm), Class D (15 < 20 mm), and Class E
(≥ 20 mm).
The byssal attachment strength of G. trapesina was
immediately investigated in the shipboard laboratory soon
after collection. Kelp blades with undisturbed, attached G.
trapesina were held in troughs of slowly circulating sea-
water. Thirty-three individuals spanning the range of shell
lengths were haphazardly selected for testing. Attachment
strength was measured using an adaptation of an in situ tech-
nique for testing attachment strength of rocky shore mussels
(Denny 1987; Bell and Gosline 1996). Selected individuals
on the kelp blades were attached to a soft, custom-designed
harness from which gradually increasing weights were
sequentially hung. The weight at which the byssus broke
was recorded in Newtons (N).
Trophic analyses
To gain information on the dietary signatures of G. trapes-
ina, three freshly collected individuals per station were
processed using stable isotope and fatty acid techniques. In
addition, to have information on the food sources available
for G. trapesina at each station, kelp samples were obtained
from near-shore kelp beds (n = 3 per station and technique)
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Page 4 of 17
as were samples of suspended organic matter (SPM, n = 3
per station and technique). SPM samples were obtained from
5-L replicates of surface water from the area surrounding the
kelp beds where G. trapesina occurred. These water samples
were filtered through pre-combusted (450 °C) GF/F filters
(0.7-μm pore size and 47-mm diameter). To obtain signa-
tures of decomposing kelp, additional samples of whole kelp
from Station 1A were placed in buckets of non-circulating
seawater in the laboratory and allowed to degrade naturally
for 3 weeks under artificial light and at ~ 18 °C. After col-
lection, individuals were immediately dissected. The body
tissues (excluding the gut) and the kelp samples were rinsed
with Milli Q water to remove pieces of shell, epiphytes, and
other material, and placed in 2-mL cryotubes. All samples
were frozen at − 80 °C for storage on board the ship, and
later transferred to a liquid nitrogen container for transporta-
tion from the ship to the laboratory and stored in a − 80 °C
freezer until processed.
Diet analyses
Isotopic analyses
In the laboratory, SI samples were dried at 60 °C for 48 h.
The samples were ground to a fine powder and 1-mg sub-
samples were placed in tin foil capsules. Samples were ana-
lysed for SI ratios of carbon (13C/12C) and nitrogen (15N/14N)
using a Flash EA 1112 Series coupled to a Delta V Plus
stable light isotope ratio mass spectrometer via a ConFlo
IV system housed at the Stable Isotope Laboratory of the
Mammal Research Institute (University of Pretoria, South
Africa). Results are expressed in the standard unit notation
as follows:
([ ]/[ ])
𝛿X(‱) = Rsample − Rstandard Rstandard − 1
where X is 13C or 15N and R represents the ratio of 13C/12C
or 15N/14N. Analytical precision was < 0.15‰ for δ13C
and < 0.1‰ for δ15N. Merck gelatin was used as an internal
standard and calibrated against several International Atomic
Energy Agency reference materials. All results are refer-
enced to Vienna Pee-Dee Belemnite for carbon isotope val-
ues, and to air for nitrogen isotope values.
Fatty acid analyses
Total lipids were extracted and trans-esterified using a modi-
fied Indarti one-step procedure (Indarti et al. 2005). All sam-
ples were taken from the − 80 °C freezer and immediately
transferred to a freeze-dryer (VirTis BenchTop K) for 24 h
and subsequently transferred back into a − 80 °C freezer
until FA extraction. Samples were homogenized into 4 mL
of a fresh mixture of methanol, concentrated sulphuric acid,
13
Marine Biology (2018) 165:172
and chloroform containing 0.01% of an anti-oxidant, butyl-
ated hydroxytoluene (BHT) (1.7:0.3:2.0 v:v:v), and closed
under nitrogen in lipid-clean test tubes. A precise mass of
fatty acid standard (19:0) was added to each sample to quan-
tify the total FA (TFA). The extraction and transesterifica-
tion reactions occurred at 100 °C for 30 min. The FA methyl
esters (FAME) formed were then stored at − 80 °C until
gas chromatography (GC) analyses. FAME composition of
each sample was determined by GC (Agilent Technologies
6850, at the InnoVenton and the Downstream Chemicals
Technology Station of the Nelson Mandela Metropolitan
University, Port Elizabeth, South Africa) equipped with a
ZB-Waxplus Zebron column (30 m, 0.25-mm ID, 0.25-µm
film thickness), with nitrogen as the carrier gas at a flow
rate of 2 mL min−1. The injector was at 250 °C and split-
less injection was used for all samples. The flame ionization
detector was set at 260 °C, and the oven was initially set at
70 °C. After 1 min, the oven temperature was increased by
40 °C min−1 until 170 °C and then raised to 250 °C at a rate
of 2.5 °C min−1 and held for 4.5 min. Peaks were integrated
using GC ChemStation software (Agilent Technologies,
version B.04.02), identified by comparison with retention
times of external standards (37 component FA methyl ester
mix Supelco, marine PUFA no. 1 Supelco, menhaden oil
PUFA no. 3, bacterial acid methylesters mix Supelco). Each
FA was measured as a proportion of the TFA composition
(weight% of TFA) and peak areas were corrected according
to the FID response to FA chain length (Ackman 2002).
Using the known mass of standard 19:0 in each sample, the
mass of each FA was also calculated and expressed as μg
of FA m­ g−1 dry weight (μg mg−1). FA are reported using a
shorthand notation of A:Bn-x, where A indicates the number
of carbon atoms, B is the number of double bonds, and x
indicates the position of the first double bond relative to the
terminal methyl group (Budge et al. 2006). Amongst the
× 1000,
common FA, it is possible to identify bacterial FA (BAME)
which are the sum of iso- and anteiso-branched chain FA and
unbranched 15:0 and 17:0 FA (Wakeham and Beier 1991).
The FA 16:1n-7 and 20:5n-3 are characteristic of diatoms
and the FA 22:6n-3 and 18:4n-3 are prevalent in dinoflagel-
lates (Parrish et al. 2000), while kelps are characterized by
20:4n-6 (Hanson et al. 2010). Essential fatty acids (EFA)
are 20:4n-6, 20:5n-3, and 22:6n-3 (Alkanani et al. 2007).
Data analysis
Size distribution
We evaluated differences in size distribution of G. trapesina
between Marion and Prince Edward Islands using a two-
tailed Kolmogorov–Smirnov test. The analyses were per-
formed using STATISTICA v12 (StatSoft Inc. 2012). Mussel
shell length (SL) was the dependent variable, with 364 and
Marine Biology (2018) 165:172 Page 5 of 17  172

455 valid individual replicates collected from both years, for 1% TFA were considered for the analyses (i.e., 41, 24, and
Marion and Prince Edward Island, respectively. 43 FA used for mussel, kelp, and SPM, respectively). The
analyses were conducted using PRIMER v6 and the PER-
Stable isotopes MANOVA + add-on package.

Differences among stations in the stable isotope signatures

of samples were evaluated using a two-way analysis of
variance (ANOVA) with a design consisting of the factors:
Island (two levels and fixed), and Station (two levels, ran-
dom and nested in island). A preliminary analysis indicated
that samples collected in 2015 and 2016 did not differ as a
function of time, and thus these samples were pooled and
year was not considered as a factor in the analyses. This
design was applied separately to the data for SPM, kelp,
and G. trapesina. Significant results were followed by Tukey
HSD post hoc tests to evaluate the hypotheses of interest.
Levene’s test was used to test for homogeneity of variances.
Analyses were performed using STATISTICA v12 (StatSoft
Inc. 2012).
SIAR mixing model
We used the Bayesian mixing model from the package SIAR
for R (Parnell et al. 2010) to estimate the relative contribu-
Results
Attachment strength and size distribution
The attachment strength of Gaimardia trapesina was evalu-
ated in 33 individuals from station 1A. The attachment
strength increased linearly with SL, ranging 0.7–3.2  N
(Fig.  2a). Although the two were significantly corre-
lated (p < 0.01), the coefficient of determination was low
(r2 = 0.29). For most SL (those between 12 and 18 mm),
detachment forces were all between 0.7 and 2.0 N. Only
a
3.5
3.0
R2=0.29
2.5
Detachment force (N)

tion of various food resources to the diet of G. trapesina. 2.0

The potential food sources entered into the model were:
1.5
fresh kelp frond, SPM and degraded kelp. Fractionation fac-
tors between resources and the consumers were assumed to 1.0
be 4% for δ15N and 1.86% for δ13C, based on the previous
studies (Kaehler et al. 2000). 0.5

0.0
Fatty acids 10 12 14 16 18 20 22 24
Shell length (mm)
The FA composition of SPM, kelp, and mussel samples was
compared using the same design as for the SI data analyses; b 70
Marion Island
however, we used only samples from 2015. In the case of Prince Edward Island

60
G. trapesina, we also used samples from 2016 from stations
7B, 10B, 11B, and 12B. All other samples from 2016 were 50
lost due to freezer malfunction. A multivariate permutational
Frequency %

analysis (PERMANOVA; Anderson, 2001) on Bray–Cur- 40

tis dissimilarities was used to assess differences among the

30
factors Island and Station. Each term in the analysis was
tested using > 9999 permutations as the relevant permutable 20
units (Anderson and Braak 2003). In the event of signifi-
cant results, PERMANOVA pairwise tests were performed. 10

Principal component analysis (PCA) was used to explore

0
differences among samples. All the FA with a Pearson cor- ≤5 5<10 10<15 15<20 ≥ 20

relation value > 0.5 [correlation between the variables (FA) Class mussel lenght (mm)

and the PCA axes] were indicated on the PCA plots to high-
light which FA influenced each axis. The combined results
of the PCA and SIMPER (similarity percentage, PRIMER)
were used to assess the FA responsible for the differences
among groups of samples. Only FA forming more than
Fig. 2  a Attachment strength of Gaimardia trapesina for station 1A
(n = 33) and b size-frequency distribution of G. trapesina at Marion
and Prince Edward Islands based on pooled collections from 2015
and 2016 (n = 364 for Marion Island and n = 455 for Prince Edward
Island)

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Page 6 of 17
larger individuals (19–22 mm SL) exceeded a detachment
force of 2 N, with most detaching between 2.5 and 3.2 N
(Fig. 2). It was noted that the byssal threads were extremely
elastic, often stretching to more than three times the shell
length of the mussel. This was evident as a substantial initial
extension of the byssus followed by static resistance and a
final, smaller extension before the breaking point (personal
observation).
The size distribution of G. trapesina differed between
Marion Island and Prince Edward Island (two-tailed Kol-
mogorov–Smirnov test, D = 0.002, p < 0.001). The aver-
age shell length of specimens from Marion Island was
13.92 ± 3.57 mm (n = 364), while, for Prince Edward Island,
it was 12.28 ± 3.16 mm (n = 455). The ranking of size classes
differed between islands (Fig. 2b). Class C (10 < 15 mm)
had the highest number of specimens from both islands,
comprising > 50% of all individuals, followed by class D
(15 < 20 mm) and B (5 < 10 mm) for Marion, and by class
B and D for Prince Edward. Low numbers were recorded
in class A (≤ 5 mm) and class E (≥ 20 mm) at both islands.
Diet analyses
Stable isotope
Stable isotopes analyses of the food sources available for G.
trapesina showed a significant variability in δ13C and δ15N
values among stations and between the two islands. SPM
δ15N ranged between − 2.46 and 4.68‰ (Figs. 3, 4), while
SPM of δ13C ranged between − 25.37 and − 18.89‰. Both
isotopes showed significant effects of the factors Island and
Station (ANOVA, p < 0.05 and p < 0.001 for both factors,
for δ15N and δ13C respectively). Variability was observed
among δ15N values from Marion Island, but with no clear
geographic pattern of variation (Fig. 1S). Similarly, δ13C of
SPM from Prince Edward was lower compared to stations
8
6 Degraded kelp
4
δ15N (‰)
0
-2
-4
-6
-26 -24 -22 -20 -18 -16 -14
δ13C (‰)
Fig. 3  Stable isotope composition of Gaimardia trapesina, SPM,
fresh fronds of Macrocystis pyrifera kelp and kelp detritus at stations
around the PEI. Samples were collected in April/May 2015 and 2016.
Each symbol represents mean ± SD (n = 3)
13
Marine Biology (2018) 165:172
located on the north side of Marion Island (Fig. 4) with sta-
tion 11B showing the highest δ13C value at Prince Edward
(p < 0.001; δ13C = − 18.95 ± 0.82‰). On the other hand,
stations to the south and west of Marion Island had the
lowest δ13C values and were markedly lower than those
to the north and east. Station 1B had the highest values
(− 19.27 ± 0.43‰; Fig. 4).
Kelp isotope compositions were higher compared to SPM
values and showed high variability, with δ15N values ranging
between 1.99 and 6.91‰, and δ13C between − 23.19 and
− 12.12‰ (Figs. 3, 4). In the case of SPM, both isotopes of
kelp were significantly influenced by the factors Island and
Station (ANOVA, p < 0.001 and p < 0.05 for both factors, for
δ15N and δ13C, respectively). Stations on the south-eastern
side of Marion Island showed the highest δ15N values over-
all (Fig. 1S). No such pattern was seen for Prince Edward,
where δ15N values on the eastern and western coasts did not
differ (p > 0.05). In contrast, δ13C of kelp located at Prince
Edward Island gradually increased from the upstream to
downstream sides of the island (i.e., west–east). Variability
was also observed among kelp samples from Marion Island,
with specimens from the northern part of the island (i.e.,
the interisland region) having lower δ13C values than sam-
ples from the southern coast. In general, kelp δ13C values
from the interisland area were low compared to conspe-
cifics from the other stations (Fig. 4). Degraded kelp had
δ15N and δ13C values within the range of 3.01 ± 0.32‰ and
− 17.52 ± 1.03‰, respectively (Fig. 3).
Gaimardia trapesina showed differences among stations
nested in island for both isotopes (p < 0.01 in both cases)
and the factor Island was not significant in any analysis
(p > 0.05). Gaimardia trapesina had values of δ15N and δ13C
closely corresponding to those of SPM (− 2.12/2.39‰ and
− 25.67/− 19.39‰, for δ15N and δ13C respectively; Fig. 3).
Mussel δ15N decreased from upstream to downstream of
both islands, with station 3B showing the highest δ15N val-
ues (Fig. 1S). In contrast, δ13C did not differ among stations
from either island, with the exception of δ13C from station
3B which, as in the case of δ15N, was significantly higher
SPM_2016
SPM_2015
Kelp_2016
compared to the other stations (p < 0.001; Fig. 4).
Kelp_2015
G. trapesina_2016
G. trapesina_2015 SIAR mixing model
Assuming δ13C enrichment (I) of 1.86‰ per trophic level,
the relative contributions of kelp, degraded kelp and SPM
to the diet of G. trapesina were estimated using a Bayes-
ian mixing model. Gaimardia trapesina had δ13C values
-12 closer to those of SPM (− 23.44 ± 1.40‰) than the other
food sources (− 16.64 ± 3.07‰ and − 17.52 ± 1.03‰ for
fresh kelp fronds and degraded kelp, respectively). Con-
sidering that the δ 13C values of several samples of G.
trapesina were lower than the values of SPM, the bivalve’s
expected food source (averaged values between − 27.53
Marine Biology (2018) 165:172 Page 7 of 17  172

Fig. 4  δ13C values of a SPM, b kelp Macrocystis pyrifera, and c Gaimardia trapesina in the vicinity of the PEI. See Fig. 1 for station names and
locations

and − 21.25‰) must, therefore, consist of SPM, mixed Fatty acids

with a food source which is missing in the model. This
was particularly evident for mussels from stations 2A, 2B,
5B, 10B, and 11B. At the other stations, G. trapesina had
values in line with that of SPM and in the case of station
3B, it had a higher value, indicating that G. trapesina had
a mixed diet of kelp and another food source with more
depleted δ13C composition.
FA results partially confirmed the SI outcome, showing no
differences between islands or among stations for kelp sam-
ples, while dissimilarities were present among stations for
SPM and G. trapesina (Table 1). SPM usually had a high
proportion of saturated FA (SFA, 36.14–77.13% TFA), fol-
lowed by polyunsaturated FA (PUFA, 12.0–45.17% TFA)

Table 1  PERMANOVA results POM Kelp G. trapesina

for the fatty acid composition
of suspended particulate matter df MS F P df MS F P df MS F P
(SPM), kelp, and the mussel
Gaimardia trapesina at the Island Station 1 517.31 1.03 0.658 1 84.29 1.37 0.338 1 694.50 2.75 0.079
close proximity of the Prince (Island) Res 2 498.47 2.57 0.014* 2 61.23 0.73 0.619 2 221.56 3.37 0.004*
Edward Islands 8 193.44 8 83.88 6 65.70

Df degree of freedom, MS mean square

*p < 0.05; **p < 0.01; ***p < 0.001

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Page 8 of 17 Marine Biology (2018) 165:172

and monounsaturated FA (MUFA; 10.87–39.12% TFA,
Table 2, Fig. 5). The most abundant FA were represented
by: 14:0, 16:0, 18:0, 18:4n-3 and 20-PUFA (Table  2).
EFA accounted for a small proportion in all the samples
(6.83 ± 4.87% of TFA; Fig. 5). No differences were found
in the SPM composition between islands; however, stations
3A and 4A from Prince Edward Island differed from each
other (PERMANOVA pairwise test, p < 0.05). SIMPER
showed that the differences were mainly driven by bacterial
FA (BAME), 14:0, 16:0, 16:3n-4, and 16:4n-1 which were
more abundant at station 3A, while station 4A was enriched
in 20-PUFA and 22:5n-3 (explaining 55% of the variance).
The main component of kelp FA was represented
by PUFA (43.31–53.93% TFA), followed by SFA
(31.46–39.99% TFA) and MUFA (12.63–19.73% TFA;
Table  3, Fig.  5). Amongst PUFA, 18:4n-3, 20:4n-6 and
20:5n-3 comprised the highest proportion (Table  3),
although 14:0, 16:0, and 18:1n-9 contributed greatly towards
the TFA (Table 3). EFA accounted for 11.27 ± 4.06% of TFA
(Fig. 5). No significant differences were recorded in the kelp
FA composition either between islands or among stations
(Table 1).
Gaimardia trapesina was characterized by similar
proportions of PUFA (34.71–51.51% TFA) and SFA

Table 2  Total fatty acid Island Station Suspended organic matter Kelp Detritus
composition of suspended
particulate matter (SPM; Marion Island Prince Edward Island Marion Island
mean ± SD, n = 3 per station)
obtained within the kelp beds 1A 2A 3A 4A 1A
near the Prince Edward Islands
14:0 9.66 1.94 9.63 3.56 10.68 6.00 4.30 0.88 10.06 6.46
in April/May 2015
14:1n-7 0.48 0.50 0.94 0.29 1.24 0.42 0.14 0.01 1.76 0.08
16:0 40.22 2.36 26.21 14.94 25.02 11.92 15.02 4.84 21.90 7.39
16:1n-7 2.18 0.80 2.65 0.94 3.63 0.68 1.68 0.46 13.46 8.73
16:2n-4 0.37 0.09 0.56 0.02 0.56 0.49 0.38 0.19 0.05 0.03
17:0 0.92 0.20 0.99 0.09 0.89 0.45 0.54 0.09 0.87 0.32
16:3n-4 0.40 0.20 0.83 0.61 3.80 2.21 0.11 0.10 0.68 0.12
18:0 21.69 2.24 9.78 6.33 8.25 2.22 11.03 7.20 1.96 0.12
18:1n-11 1.77 1.32 0.60 0.05 1.05 0.57 0.72 0.33 7.12 4.77
18:1n-9 1.26 1.58 0.32 0.11 0.59 0.20 0.25 0.08 15.02 4.68
18:2n-6 0.46 0.16 1.15 1.14 1.40 1.39 2.66 1.02 1.15 0.96
18:3n-3 0.34 0.08 0.58 0.56 1.11 1.00 1.91 1.83 0.81 0.32
18:4n-3 0.85 0.63 3.16 0.47 4.61 3.12 3.46 2.02 1.23 0.92
20:0 1.08 0.21 2.09 2.20 1.26 0.37 2.41 1.65 0.61 0.03
20:1n-11 1.03 0.36 1.32 0.32 0.60 0.29 2.49 1.99 0.26 0.01
20:1n-9 1.58 1.50 1.85 0.34 5.07 4.29 5.67 3.82 0.58 0.68
20:1n-7 0.53 0.52 1.90 0.47 3.82 4.37 2.92 1.77 0.33 0.01
20:4n-6 0.51 0.20 3.00 2.12 0.84 1.21 3.11 3.06 3.83 0.10
20:3n-3 1.28 0.63 4.04 2.35 3.36 1.97 7.94 5.94 0.23 0.17
20:4n-3 1.47 1.09 4.30 3.71 2.96 3.23 8.12 0.77 1.21 0.78
20:5n-3 1.21 0.31 3.41 3.51 1.80 0.62 5.17 2.96 2.26 0.89
22:1n-9 2.04 1.75 2.25 2.54 1.49 0.18 4.81 0.43 0.60 0.50
22:2n-6 2.78 1.22 2.93 3.07 5.54 3.21 4.32 2.09 3.11 1.66
22:5n-3 0.45 0.19 8.62 8.93 0.89 0.18 4.11 1.04 0.96 1.05
22:6n-3 1.88 0.48 2.28 2.34 1.35 0.47 3.88 2.22 0.00 0.00
BAME 3.56 1.40 4.62 1.72 8.20 3.69 2.84 1.10 9.96 0.34
SFA 77.13 3.57 53.32 28.84 54.30 16.55 36.14 12.05 45.35 13.04
MUFA 10.87 2.70 11.82 3.41 17.49 7.60 18.69 6.77 39.12 8.40
PUFA 12.00 1.02 34.85 25.43 28.21 8.94 45.17 7.08 15.53 4.64
EFA 8.69 7.97 3.99 1.72 12.16 5.70 3.60 0.95 6.09 0.79
n-3/n-6 2.23 1.11 3.46 0.96 2.93 2.33 3.41 0.27 0.81 0.45
∑ TFA 12.59 0.53 4.81 0.74 3.3 0.56 9.51 0.36 9.71 0.38

Only FA > 1% were displayed below

PUFA polyunsaturated fatty acids, MUFA monounsaturated fatty acids, SFA saturated fatty acids, EFA
essential fatty acids (20:4n-6, 20:5n-3, 22:6n-3), BAME bacterial fatty acids, TFA total fatty acids (µg L−1)

13
Marine Biology (2018) 165:172 Page 9 of 17  172

Fig. 5  Fatty acid (FA) propor- a 100

tion of saturated FA (SFA), SFA
monounsaturated FA (MUFA),
Suspended Particulate Matter
MUFA
polyunsaturated FA (PUFA), PUFA
and essential FA (EFA) of a EFA
SPM, b kelp Macrocystis pyrif- 80
era, and c Gaimardia trapesina,

Percentage (%)
collected at stations located at
the close proximity of the PEI.
See Fig. 1 for station locations 60

40

20

0
b 1A 2A 3A 4A
100

Kelp- Macrocystic laevis

80
Percentage (%)

60

40

20

0
1A 2A 3A 4A Degraded kelp
c
100

Gaimardia trapesina
80
Percentage (%)

60

40

20

0
1A 2A 3A 7B 10B 11B 12B
Station

13
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Page 10 of 17 Marine Biology (2018) 165:172

Table 3  Total fatty acid Island Station Macrocystis pyrifera

composition of the kelp
Macrocystis pyrifera Marion Island Prince Edward Island
(mean ± SD, n = 3 per station)
collected at stations at the 1A 2A 3A 4A
proximity of the Prince Edward
14:0 14.61 6.47 12.16 2.86 13.49 2.50 12.43 0.41
Islands in April/May 2015
16:0 16.12 3.66 14.63 2.01 16.70 2.49 13.36 2.28
16:1n-7 0.81 0.26 0.95 0.31 0.88 0.10 0.93 0.05
17:0 0.22 0.14 0.14 0.03 0.52 0.73 4.85 8.16
17:1n-7 0.79 0.23 1.07 0.74 1.89 2.57 1.89 1.62
18:0 0.92 0.20 0.59 0.16 1.11 0.06 0.61 0.04
18:1n-9 11.35 4.49 12.59 7.57 16.95 2.28 9.81 1.79
18:2n-6 4.93 0.60 5.43 0.21 5.54 0.48 5.53 0.83
18:3n-3 6.43 3.63 7.24 3.74 3.16 0.50 6.08 3.51
18:4n-3 12.88 7.22 12.83 6.89 4.79 0.41 10.45 5.97
20:0 0.52 0.16 0.79 0.22 0.91 0.34 0.91 0.66
20:4n-6 15.11 1.16 16.35 3.47 19.74 1.45 14.30 1.29
20:4n-3 1.38 0.74 1.32 0.53 1.99 2.07 1.33 0.90
20:5n-3 10.53 3.70 10.75 4.34 8.09 1.71 9.69 4.67
BAME 3.39 0.86 3.15 0.17 4.23 1.06 7.83 8.13
SFA 35.79 10.62 31.46 4.99 36.96 2.81 39.99 13.57
MUFA 12.96 4.36 14.61 7.13 19.73 0.42 12.63 3.45
PUFA 51.26 14.86 53.93 11.93 43.31 2.66 47.38 17.00
EFA 11.90 4.42 12.07 4.87 10.08 3.77 11.02 5.43
n-3/n-6 1.56 0.74 1.57 0.88 0.72 0.23 1.34 0.65
∑ TFA 99.80 0.45 139.96 0.41 353.23 0.80 135.32 0.38

Only FA > 1% were displayed below

PUFA polyunsaturated fatty acids, MUFA monounsaturated fatty acids, SFA saturated fatty acids, EFA
essential fatty acids (20:4n-6, 20:5n-3, 22:6n-3), BAME bacterial fatty acids, TFA total fatty acids (µg L−1)

(26.53–53.06% TFA) which varied among stations, fol-
lowed by MUFA (6.25–12.83% TFA; Table  4, Fig.  5).
EFA accounted for 29.17 ± 5.82% of TFA (Fig. 5). The
more abundant FA were: 16:0, 18:1n-9, 18:4n-3, 20:5n-3,
and 22:6n-3 (Table 4). The factor Island was not signifi-
cant in the analyses, and there were differences among sta-
tions (Table 1); however, the only dissimilarity found was
between station 3A and 11B (PERMANOVA pairwise test,
p < 0.01). FA content per mg of dry weight/litre showed that
kelp had the highest content of FA (99.80–353.23 µg mg−1)
among the components examined, followed by G. trapes-
ina (15.75–41.86 µg mg−1) and SPM (3–12.59 µg mg−1;
Tables 2, 3 and 4).
Discussion
The PEI lie between the Sub-Antarctic Front (SAF) to the
north and the Antarctic Polar Front to the south, placing
them directly in the path of the fast eastward flowing Ant-
arctic Circumpolar Current (ACC; Lutjeharms and Valentine
1984; Orsi et al. 1995). Although this location suggests that
rafting G. trapesina should arrive on the west coasts of the
islands, it was not found on any western kelp beds but rather
on the kelp of the eastern coasts, a pattern that we hypoth-
esized to be due to the physical conditions.
The western coastlines are extremely exposed, get-
ting upwards of 100 day year−1 of gale force winds and
unconstrained, long fetch, ocean swell (De Villiers 1976).
In addition, the average speed of the ACC in this region is
5–15 cm s−1, but exceed 30 cm s−1 when the SAF is close to
the PEI (Nowlin et al. 1977; Perissinotto et al. 2000; Hunt
et al. 2008). The presence of kelp without G. trapesina sug-
gests that the attachment strength of the bivalve is exceeded
under such highly exposed conditions. Thus, the absence of
G. trapesina from the western kelp beds, despite the pres-
ence of suitable habitat could be explained: either by new
kelp rafts carrying G. trapesina failing to establish them-
selves off the western coasts; or by G. trapesina being una-
ble to remain attached to kelp under these highly exposed
conditions. Population on drift-kelp and recruits that are
pushed towards the downstream side of the PEI finds a more
hospitable environment where they are more likely to be
retained and settle under productive conditions due to the
retentive mesoscale hydrodynamics of the interisland area
and leeward side of the islands (Boden 1988; Pakhomov

13
Marine Biology (2018) 165:172 Page 11 of 17  172

Table 4  Total fatty acid Year 2015 2016

composition of the mussel
Gaimardia trapesina Island Marion Prince Edward Prince Edward
(mean ± SD, n = 3 per station)
collected at the proximity of the Station 1A 2A 3A 10B 11B 12B 7B
Prince Edward Islands in April/
14:0 2.66 0.25 1.63 1.03 1.06 0.11 2.17 0.12 2.60 0.12 1.22 0.70
May 2015 and 2016
14:1n-7 0.83 1.38 0.08 0.06 0.09 0.07 0.04 0.00 0.07 0.09 0.04 0.01
16:0 27.65 2.03 30.42 2.78 42.45 6.88 16.92 0.19 11.10 7.64 19.97 19.40
16:1n-7 2.39 0.28 1.96 0.88 0.92 0.07 1.97 0.16 2.32 0.58 1.57 1.56
17:1n-7 1.72 0.62 1.67 1.01 1.17 1.33 2.90 0.40 0.65 0.89 2.24 4.71
18:0 4.00 0.10 3.92 0.31 6.25 6.37 5.79 0.01 6.44 2.41 7.18 8.13
18:1n-11 2.69 0.16 3.19 1.04 1.99 0.52 0.05 0.05 0.03 0.02 0.11 0.05
18:1n-9 4.26 0.17 3.24 1.66 1.99 0.65 5.98 1.00 7.40 1.93 3.32 3.00
18:1n-7 0.25 0.05 0.20 0.00 0.21 0.03 2.51 0.16 3.01 0.98 2.07 1.55
18:2n-4 0.61 0.11 0.36 0.25 0.15 0.14 0.00 0.00 0.00 0.00 0.00 0.00
18:2n-6 1.40 0.18 1.46 0.24 0.96 0.27 2.81 0.54 3.43 1.10 1.09 1.17
18:3n-3 1.29 0.12 1.24 0.45 0.62 0.18 2.11 0.02 2.54 0.22 1.14 0.74
18:4n-3 5.96 0.76 5.35 2.80 1.80 0.72 5.70 0.70 3.15 2.98 4.61 1.67
20:0 0.39 0.10 0.28 0.02 0.51 0.23 0.39 0.03 0.79 0.21 0.40 0.29
20:1n-11 0.23 0.14 0.15 0.10 0.27 0.21 0.00 0.00 0.00 0.00 0.00 0.00
20:1n-9 3.17 0.24 3.44 0.71 4.51 0.08 5.12 1.11 7.16 1.62 4.03 4.84
20:2n-6 1.46 0.12 1.56 0.41 2.32 0.03 2.64 0.28 2.57 0.54 2.20 2.65
20:3n-6 0.58 0.15 0.36 0.01 1.16 1.42 1.19 0.03 1.33 1.02 1.22 1.79
20:4n-6 1.81 0.22 2.22 0.67 2.91 0.56 5.31 0.87 5.46 1.08 3.67 7.25
20:5n-3 15.77 0.54 13.26 3.35 12.87 5.60 9.48 0.19 9.40 0.34 9.75 7.92
22:0 0.51 0.33 0.14 0.09 0.18 0.05 0.31 0.01 0.48 0.58 0.47 0.25
22:1n-11 0.66 0.33 0.51 0.03 0.57 0.13 0.00 0.00 0.00 0.00 0.00 0.00
22:1n-9 0.68 0.29 0.52 0.05 0.31 0.15 0.77 0.07 1.31 0.50 1.12 1.19
22:4n-6 1.37 0.30 0.83 0.20 0.88 0.39 1.34 0.12 1.39 0.50 0.73 2.74
22:5n-6 0.83 0.13 0.62 0.41 0.94 0.11 0.81 0.06 1.34 0.86 0.99 1.09
22:5n-3 0.96 0.36 0.40 0.06 0.45 0.24 3.63 0.26 2.66 0.07 4.61 5.35
22:6n-3 9.70 0.33 13.26 3.35 9.65 4.20 15.80 1.74 18.25 7.38 19.63 17.56
BAME 5.84 4.56 7.61 8.08 2.62 0.85 4.26 0.38 5.13 1.66 6.63 4.39
SFA 41.04 2.18 43.99 10.64 53.06 12.49 29.84 0.74 26.53 4.47 35.87 33.17
MUFA 11.66 0.55 9.47 3.36 6.25 0.97 10.55 0.75 12.83 3.56 7.10 6.17
PUFA 41.74 3.04 40.90 9.03 34.71 10.90 50.81 1.59 51.51 6.80 49.64 49.91
EFA 27.28 1.10 28.73 6.08 25.43 10.36 30.59 1.06 33.11 8.12 33.05 32.72
n-3/n-6 2.62 0.44 2.34 0.19 4.02 1.99 4.54 0.28 4.99 2.02 2.78 1.22
Σ TFA 31.54 7.38 41.86 7.74 37.84 17.73 21.64 13.96 15.75 1.34 16.37 3.73

Only FA > 1% were displayed below

PUFA polyunsaturated fatty acids, MUFA monounsaturated fatty acids, SFA saturated fatty acids, EFA
essential fatty acids (20:4n-6, 20:5n-3, 22:6n-3), BAME bacterial fatty acids, TFA total fatty acids (µg L−1)

and Froneman 1999; Pakhomov et al. 2003). Similarly, as
G. trapesina is a brooding species (Helmuth et al. 1994),
juveniles produced by adults already present at the PEI are
likely to be retained close to the parent community as sug-
gested for other species (Pakhomov et al. 2002).
In examining the size structure of the PEI populations
of G. trapesina, the only comparable size-frequency data
come from the Beagle Channel, Tierra del Fuego (Adami
and Gordillo 1999). Although populations from both regions
had low numbers of juveniles (≤ 5 mm), the peak frequency
at PEI was 10–15 mm SL range, while, in the Beagle Chan-
nel, the peak frequency was in the 15–23 mm SL size class
(converting shell height to SL; Adami and Gordillo 1999).
Even if our counts for the 15–20 mm and ≥ 20 mm classes
are added together, the peak frequency in our study remains
in the 10–15 mm class. This means that the contrasting pat-
tern in frequency distribution between the two studies is evi-
dent even when considering a wider range of the larger size
class in our study. Seasonality and spatio-temporal differ-
ences in local hydrodynamics, temperature/salinity regimes,

13
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Page 12 of 17
or differences in food availability may play a role in limit-
ing or promoting growth (Öst and Kilpi 1997; O’Connor
et al. 2007). The difference in size-frequency distributions
between the two studies could be due to a number of factors
including the time of year when samples were taken. Ours
were taken in austral autumn, but it is not clear when Adjani
and Gordillo collected theirs. Intraspecies differences,
including genetic variability between populations, is another
possible explanation for the differences (Luttikhuizen et al.
2003); however, at present, there are no studies that have
looked at genetic variability of populations of this species.
Direct comparisons of attachment strength for G. trapes-
ina with similar (non rocky shore) taxa are not possible.
However, their small size and fragile shells suggest that their
resistance to detachment forces of up to 3.2 N was substan-
tial. Rocky shore mussels of SL 35–45 mm (Perna perna
and Mytilus galloprovincialis) have detachment forces of
40–90 N (Zardi et al. 2007). Extrapolating our data based
on the relationship between SL and detachment force, G.
trapesina of an equivalent hypothetical SL range should
have detachment forces of 8.7–13.3 N. Although these val-
ues remain substantially lower than their rocky shore coun-
terparts, there are important differences in the numbers and
diameter of byssal threads, and in the attachment strategies,
between taxa. In their work on P. perna and M. galloprovin-
cialis, Zardi et al. (2007) recorded large byssus diameters
(ca. 90–200 μm) and numbers of threads (ca. 40–120). In
comparison, the diameter of byssal threads in G. trapesina
is around 60 μm and attachment is usually achieved by rela-
tively few or even single threads (Davenport and Wilson
1995). In addition, unlike rocky shore taxa, G. trapesina do
not appear to aggregate or attach to one another; instead,
they rely on highly elastic byssus and a large, strongly adhe-
sive foot for adhesion (Davenport and Wilson 1995). The
observed elasticity of the byssus during our tests agrees with
the measured extension factor (ratio of resting byssus length
to breaking length) for G. trapesina. Among four sub-Ant-
arctic bivalve species (G. trapesina, Lasaea rubra, Lissarca
miliaris, and Kidderia bicolor), G. trapesina has the greatest
extension factor (4.97), indicating that the byssus extends
by as much as five times its resting length (Davenport and
Wilson 1995). This is more than double the factor of 1.60
measured for K. bicolor, which attaches to rock rather than
macroalgae. Likewise, G. trapesina have streamlined shells
that reduce drag, and are able to produce new byssus rapidly
(within 60 s) which probably allows it to regain attachment
under harsh conditions (Davenport and Wilson 1995). In
combination, these traits allows G. trapesina to dampen or
resist inertial wave forces, and to remain attached to kelp
fronds even when subject to strong wave action and whiplash
action of the fronds.
While several bivalve species respond morphologically
to threats of predation (Kobak and Kakareko 2011; Naddafi
13
Marine Biology (2018) 165:172
and Rudstam 2013), this does not seem to be the case for
G. trapesina. Neither the elasticity of their byssus nor the
fragility of their shells offers protection against predation
by seabirds. In fact, the species responds uncharacteristic to
physical touch, not retracting the foot or closing the valves
(Davenport and Wilson 1995). It is not clear why they do
not appear to respond to predation, but this may be because
dislodgement by wave action is the greater threat, while pre-
dation by seabirds is not as ubiquitous. It is also possible
that the features required to resist inertial wave forces (i.e.,
elasticity, light, and streamlined shells) are mutually exclu-
sive with features that would help resist predation, such as a
more rigid byssus and larger, thicker shells.
Diet analyses indicated that G. trapesina feeds mostly
on SPM, and that kelp detritus only contributes minimally
to the diet of this species. Although δ15N of SPM varied
slightly among stations and islands, the values recorded in
our study were within the range of average values previously
reported for the Southern Ocean (Lourey et al. 2003). In
contrast, the δ13C values of SPM recorded in this study were
relatively low for kelp-associated areas and depleted com-
pared to values from the same area in a previous study (Kae-
hler et al. 2006) who showed that the δ13C value of SPM
was close to that of decomposing kelp in the near-shore and
downstream areas due to the high abundance of kelp detri-
tal fragments. Kelp δ13C values are usually higher relative
to SPM values (Bustamante and Branch 1996; Miller and
Page 2012) and this difference is even more marked when
considering open ocean SPM (Hill et al. 2006; Harmelin-
Vivien et al. 2008). In the present study, the stations were
close (10 s m) to the shore, and phytoplankton production
could have been retained along the coast particularly due to
the presence of the kelp forests, which have been shown to
promote retention and reduce exchange with the open ocean
(Pakhomov et al. 2002; Schapira et al. 2012). This also sug-
gests that near-shore SPM values within kelp beds are likely
to be similar regardless of station location.
The highly variable kelp isotopic composition in our
study is in line with the published values (Kaehler et al.
2000; Miller and Page 2012); however, the values varied
significantly among stations for both δ13C and δ15N. The
variability could be related to differences in nutrient avail-
ability at selected stations since nutrients represent one of
the main factors influencing kelp growth and production
(Konotchick et al. 2012; Miller et al. 2015). Nutrients of ter-
restrial origin (especially guano from the extensive penguin
rookeries on the islands) represent a key source for kelp at
the PEI and enter the marine environment as island-runoff
(Boden 1988; Perissinotto and Duncombe Rae 1990; Peris-
sinotto et al. 1990). This runoff promotes primary produc-
tion in the interisland area, contributing to an “island mass
effect” of enhanced primary production around the archi-
pelago (Perissinotto et al. 2000) that has implications for
Marine Biology (2018) 165:172 Page 13 of 17  172
the benthic communities at the PEI (Kaehler et al. 2000).
Island nutrient-runoff varies in time and space (McQuaid
and Froneman 2008), and this variability may be responsible
for dissimilarities in the isotopic compositions of kelp beds
around the islands. Variability can be accentuated by the fact
that different parts of a single specimen can differ in their
isotopic composition (Fredriksen 2003; Hill and McQuaid
2009), but, in our case, we were careful to collect fronds
from emerging kelp to minimize this effect.
The isotopic composition of G. trapesina did not differ
between islands for either isotope, and δ15N varied among
stations with no clear pattern. Similarity in δ13C among
individuals indicates that they rely on similar food sources
(Tieszen et al. 1983; Zanden and Rasmussen 1999). The lack
of differences in δ13C among populations of G. trapesina
indicates that the species was feeding on similar resources,
regardless of location. The isotope composition of G. trapes-
ina was very close to that of SPM, suggesting that this spe-
cies was most likely feeding on this food source. This pattern
was further confirmed by the SIAR model which highlighted
that, among kelp, degraded kelp and SPM, G. trapesina fed
mainly on SPM, with the exception of station 3B where it
had a mixed diet of kelp and SPM. Although the food source
isotopically closest to G. trapesina was SPM, SIAR high-
lighted that there was a missing food source from the model,
which had lower isotope values than the one recorded for G.
trapesina. One explanation for this is that the missing food
source was represented by picoplankton as was previously
suggested for other benthic invertebrates in the study region
(Kaehler et al. 2000). The particles in the SPM collected in
this study were 7–250 µm in diameter, which would have
included microplankton (20–200 µm) and part of the nano-
plankton (2–20 µm), but not the smaller nanoplankton or the
picoplankton (< 0.2 to 2 µm; Sieburth et al. 1978; Christaki
et al. 1998). Picoplankton usually has a lower δ13C value
than nanoplankton and microplankton (Rau et al. 1990;
Soares et al. 2015), and is abundant in the Southern Ocean
(Wright et al. 1996; Hoffmann et al. 2006). This could sug-
gest that picoplankton is an important component of the diet
of G. trapesina, which is in agreement with the fact that G.
trapesina is a small filter feeder (Adami and Gordillo 1999)
which could influence the size of particles that it feeds on
(Lewis 1981; Rossi et al. 2004; Ward and Shumway 2004;
Puccinelli et al. 2016a). An alternative explanation relates
to the isotopic fractionation factors used in this study. We
used 1.96‰ and 4‰ for carbon and nitrogen isotopes,
respectively, following calculations from the previous stud-
ies (Kaehler et al. 2000). It is possible that these factors were
not appropriate for the study species, and thus, we may have
overestimated the isotope fractionation between food source
and consumer. This is the case, for instance, if the δ15N of a
consumer approaches the original δ15N value of the N source
(e.g., ­NO3 or ­NH4). In addition, the degree of fractionation
is usually lower with more rapid growth and lower N con-
centrations (Wada and Hattori 1978; York et al. 2007). In
our study, SPM was collected from the nearshore, where a
considerable amount of guano and freshwater nutrient-runoff
is present throughout the year (Boden 1988; Perissinotto
et al. 1990; Perissinotto and Duncombe Rae 1990); however,
we do not have information on nutrient isotope composition
or concentrations.
The SI pattern of G. trapesina was in agreement with
the results from analysis of FA, which have faster turnover
signatures than SI (Puccinelli et al. 2016b). These FA results
indicated no differences in the signatures of G. trapesina
between islands and were generally close to phytoplankton
profiles. Dinoflagellates are characterized by 18:4n-3 and
22:6n-3 FA, diatoms by 18:1n-7 and 20:5n-3 (Parrish et al.
2000), while kelp signatures are usually enriched in 20:4n-6
(Hanson et al. 2010). In our results, G. trapesina had a high
proportion of diatom and dinoflagellate trophic markers, but
not clear kelp trophic marker, indicating that kelp played
no role in the diet of this species. This is surprising, since
G. trapesina is located within kelp beds, where macroalgae
can become available for filter feeder’s diet through degra-
dation (Dunton and Schell 1987; Bustamante and Branch
1996; Miller and Page 2012). The high abundances of phy-
toplankton promoted by nutrient runoff from the islands,
perhaps, override the presence of other food sources in the
water, potentially masking the importance of kelp to inter-
tidal filter feeders. The simplest interpretation, however, is
that, kelp-derived material does not play an important role
in the diet of G. trapesina. These results contrast with one
previous study (Schapira et al. 2012), but other studies have
also shown that kelp is not an important food for marine spe-
cies (Porri et al. 2011; McLeod et al. 2013; Puccinelli et al.
2016b), indicating that the importance of kelp may depend
on the species and ecosystem under investigation.
Kelp was characterized by a high proportion of total FA
compared to SPM and G. trapesina, which showed low con-
centrations of FA throughout the study area. A few studies
have indicated that an increase in the proportion of EFA with
a concomitant decrease in the total lipid content indicates
that animals are experiencing starvation (Schlechtriem et al.
2008; McLeod et al. 2013). In our study, the proportion of
EFA and PUFA from samples of G. trapesina from Prince
Edward Island increased with a corresponding decrease of
TFA, which could indicate that these specimens were fast-
ing. This pattern was only observed for samples from Prince
Edward, while specimens from Marion Island did not show
such variability. G. trapesina generally had a high propor-
tion of PUFA, which is characteristic of most species that
live in low-temperature environments, as PUFA are involved
in metabolic activities influenced by temperature, such as
maintaining optimal fluidity and function of cell membranes
(DeLong and Yayanos 1986; Glémet et al. 1997; Copeman
13
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Page 14 of 17
and Parrish 2003). It is important to highlight, however, that
the FA results were derived only from samples from April
2015 and a limited number of stations.
A previous study of the diet of G. trapesina at the
PEI found similar values of δ15N to ours [± 2.5‰ and
2.12/2.39‰, respectively, for Kaehler et  al. (2000) and
this study]; however, the earlier δ13C values for the species
were higher than ours (± − 16‰ for Kaehler et al. (2000)
and − 25.67/− 19.39‰ in this study), giving a value more
indicative of a kelp food source. This discrepancy between
the studies could be attributed to changes in water circula-
tion around the PEI. The PEI receive nutrient input from the
ACC as well as nutrient-runoff from the islands (Kaehler
et al. 2000; Allan et al. 2013; Puccinelli et al. 2018). Nutri-
ents are usually retained around the islands due to the eddy
formations characteristic of the area, which promote phy-
toplankton blooms in the interisland region (Boden 1988;
Perissinotto and Duncombe Rae 1990). Recent mooring data
suggest that high temporal variability in ocean temperatures
exists between the PEI (Von Meden et al. 2017), suggest-
ing the influence of the SAF on the island environment as
it meanders southwards (Ansorge et al. 1999; Ansorge and
Lutjeharms 2002). Indeed, several studies now suggest a
gradual poleward shift of the ACC (Fyfe and Saenko 2005).
This shift has resulted in the dominance of a flow-through
system at the islands, which has decreased eddy formation
and, thus, the development of phytoplankton blooms around
the PEI (McQuaid and Froneman 2008; Allan et al. 2013).
This has caused a change in the balance between autochtho-
nous and allochthonous food resources for benthic popula-
tions at the PEI (Allan et al. 2013) and a concomitant shift
in benthic communities over a period of only 30 years (von
der Meden et al. 2017). These results suggest that the shift
in the δ13C composition of G. trapesina from Kaehler et al.
(2000) to the values observed in our study could represent a
possible consequence of this change in the balance of food
sources, linked to shifts in water circulation around the PEI.
However, the data available are limited and more studies are
required to confirm this pattern.
The present study provides baseline information on the
biological characteristics of G. trapesina, a widely distrib-
uted species in the Southern Ocean. The importance of G.
trapesina as a food source for birds (Blankley 1981; Hockey
1988) and fish (Gon and Heemstra 1990), together with its
potential link to changing environmental and conditions
suggest that it is a useful species for monitoring long-term
change at the Prince Edward Islands and possibly other
Southern ocean archipelagos.
Acknowledgements  This work was supported by funding from the
South African Research Chairs Initiative of the Department of Science
and Technology, the National Research Foundation, the South African
Department of Environmental Affairs and Tourism, and the South Afri-
can National Antarctic Program (SANAP). We acknowledge the Stable
13
Marine Biology (2018) 165:172
Isotope Laboratory of the Mammal Research Institute, University of
Pretoria, and the InnoVenton and the Downstream Chemicals Technol-
ogy Station of the Nelson Mandela Metropolitan University, where the
analyses were conducted. Special thanks go to Captain Syndercombe
and Captain Bengu, and the officers and crew of the SA Agulhas II for
their tireless assistance at sea.
Funding  This study was funded by South African National Antarctic
Program (SANAP) awarded to Prof. Isabelle J. Ansorge, and by the
South African Research Chairs Initiative of the Department of Science
and Technology and the National Research Foundation of South Africa,
awarded to Prof. Christopher D. McQuaid.
Compliance with ethical standards 
Conflict of interest  All authors have declared that no competing in-
terests exist.
Ethical approval  All applicable international, national, and/or insti-
tutional guidelines for the care and use of animals were followed. In
addition, the permit to work on G. trapesina at the Prince Edward
Islands was obtained by the Department of Environmental Affair of
South Africa.
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