Phycologia Volume 55 (6), 659–664 Published 19 August 2016

Two newly discovered Grateloupia (Halymeniaceae, Rhodophyta)

species on aquaculture rafts on the west coast of South Africa,
including the widely introduced Grateloupia turuturu
JOHN J. BOLTON1*, OLIVIER DE CLERCK2, CAITLYNNE M. FRANCIS1, FRIDAH SIYANGA-TEMBO1 AND ROBERT J. ANDERSON1,3
1
Department Biological Sciences and Marine Research Institute, University of Cape Town,
Private Bag X3, Rondebosch, 7701, South Africa
2
Phycology Research Group, Ghent University, Krijgslaan 281-S8, Ghent, Belgium
3
Fisheries Research, Department of Agriculture, Forestry and Fisheries, Private Bag X2, Roggebaai 8012, South Africa

ABSTRACT: Compared with other world regions, very few species of marine macroalgae have been demonstrated to be
recent introductions into South Africa. Collections of red seaweeds growing on ropes on an oyster farm in Saldanha Bay
on the west coast of South Africa included two species of Grateloupia. The most abundant one is foliose, and has identical
rbcL and cox1 sequences to that of Grateloupia turuturu, indigenous to Japan/Korea but introduced into many world
regions. The other species is finely branched and presumably also an introduction, being closest in rbcL sequence to G.
carnosa from Japan but not identical. Our findings highlight the continuous risk imposed by the translocation of oysters
for mariculture purposes to spread and introduce non-native and potentially invasive species worldwide. In addition, our
inability to identify the second species, despite its sister relationship to a species from the Western Pacific Ocean, calls for
the establishment of a reference DNA-barcode library of seaweeds from the temperate Western Pacific Ocean to facilitate
the early detection of introduced and potentially invasive seaweeds. South Africa now has three foliose and two
filamentous species of Grateloupia sensu lato. Although the newly introduced species have not been recorded outside the
Saldanha Bay area so far, continuous monitoring is advised to document the future spread of the species and their effects
on native coastal ecosystems.
KEY WORDS: cox1, Halymeniaceae, Invasive species, Marine macroalgae, Oyster farming, rbcL, Saldanha Bay

INTRODUCTION (De Clerck et al. 2005b) and Grateloupia doryphora

Grateloupia, a genus of foliose or branched red seaweeds, is
rated sixth among seaweed genera for the number of species
which have been recorded as introductions (Thomsen et al.
2016). For example, five species of Grateloupia have been
recorded as introductions into the Thau Lagoon in
Mediterranean France (Verlaque et al. 2005), and six of
eight confirmed species of Grateloupia recorded in Korea
have been recorded as introductions into Europe, North
America or Australasia (Lee et al. 2009). One of the most
widespread introduced seaweed species is Grateloupia
turuturu Yamada, originating from Japan or Korea and
recorded as introduced into the Western and Eastern
Atlantic, New Zealand, Australia, Pacific Mexico and Brazil
(Simon et al. 2001; Villalard-Bohnsack & Harlin 2001;
Bárbara & Cremades 2004; Saunders & Withall 2006;
D’Archino et al. 2007; Aguilar-Rosas et al. 2012; De
Azevedo et al. 2015). It has become invasive in some regions,
dominating areas of seashore in the North-western and
Eastern Atlantic (Simon et al. 2001; Araujo et al. 2011;
Janiak & Whitlatch 2012). Many species of Grateloupia are
morphologically variable and difficult to identify, and until
the introduction of molecular sequencing a small number of
species names were widely used, especially Grateloupia
filicina (Lamouroux) C.Agardh for finely branched species
* Corresponding author (john.bolton@uct.ac.za).
DOI: 10.2216/15-104.1
Ó 2016 International Phycological Society.
(Montagne) Howe for broad, foliose species (Gavio &
Fredericq 2002). Such broad, foliose specimens considered
introduced into the Atlantic Ocean were previously recorded
under the name G. doryphora (type locality Callao, Peru) but
were later shown by molecular methods to be G. turuturu
(type locality Hokkaido, Japan; Gavio & Fredericq 2002;
Verlaque et al. 2005). In South Africa, Stegenga et al. (1997)
described the morphology of two species that were included
in the apparently widespread G. filicina and G. doryphora,
identifications also used in neighbouring Namibia (Lluch
2002). Subsequently, De Clerck et al. (2005b) carried out a
molecular study of G. filicina around the world, using rbcL
sequences. They documented extensive species-level varia-
tion and described the new species Grateloupia capensis De
Clerck for South African material, which was previously
referred to as G. filicina. Also in De Clerck et al. (2005c),
broad, foliose material from South Africa was returned to
Grateloupia longifolia Kylin, and a further species was
transferred to South African Grateloupia, Grateloupia
belangeri (Bory de Saint-Vincent) De Clerck, Gavio,
Fredericq, Cocquyt & Coppejans (formerly Phyllymenia
belangeri (Bory de Saint-Vincent) Setchell & N.L.Gardner).
These three species, all endemic to southern Africa, form a
closely related South African clade, sister to the Mediterra-
nean Grateloupia proteus Kützing (Gargiulo et al. 2013), and
were referred by the latter authors to the genus Phyllymenia.
Given the currently unstable genus level classification of the
Grateloupia-clade in the Halymeniaceae, with genera contin-
ually being described, resurrected or merged again, we retain

659
660 Phycologia, Vol. 55 (6)
Fig. 1. Grateloupia spp. growing on an aquaculture rope in Saldanha Bay, South Africa.
Fig. 2. Grateloupia turuturu.
Fig. 3. Grateloupia sp. 1.
a broad concept of Grateloupia, following Wang et al. (2001),
Gavio & Fredericq (2002), De Clerck et al. (2005b), Lin et al.
(2008) and Lin & Liang (2011).
There have been surprisingly few records of introduced
seaweeds into South Africa (four considered introduced and
three ‘‘cryptogenic’’ by Mead et al. 2011), with the first as
late as 2002 (De Clerck et al. 2002), despite considerable and
continuous study into seaweed diversity in the region in the
last 30 years (Stegenga et al. 1997; Bolton 1999; De Clerck et
al. 2005a; Anderson et al. 2009). This compares with 86
introduced and 36 ‘‘cryptogenic’’ marine and estuarine
animal species in South Africa documented by Mead et al.
(2011). In other world regions many introductions of
seaweeds, as with other marine organisms, have been
associated with the movements of animals in aquaculture,
particularly the Pacific oyster Crassostrea gigas Thunberg
(Mineur et al. 2014). The South African marine aquaculture
industry is small, largely consisting of land-based culture of
abalone (Troell et al. 2006) but culture of both oysters (C.
gigas) and mussels (the introduced invasive Mytilus gallo-
provincialis Lamarck) has been carried out for many years in
the few large, sheltered bays along the coasts of South Africa
and neighbouring Nambibia, and has resulted in numerous
introductions of marine animals (Haupt et al. 2010).
A collection of seaweeds from ropes on oyster rafts in
Saldanha Bay on the west coast of South Africa consisted
largely of specimens of two species of red algae, which we did
not recognise as being recorded in the region, despite a
number of previous detailed collections in the Bay (Simons
1977; Stegenga et al. 1997; Schils et al. 2001). These seaweed
finds are described here, their identity being investigated by
gene sequencing of rbcL and cox1 markers.
MATERIAL AND METHODS
The seaweeds were sampled by boat on aquaculture rafts at
33800 0 30 00 S, 17858 0 35 00 E on 31 May 2012. Ropes lying just
below the surface of the water were covered in short red algae,
mostly foliose (Fig. 1). On investigation in the laboratory,
most of the red algal material consisted of a foliose species
(Fig. 2), with a few other plants with a single flattened main
axis and many short fine laterals positioned in an irregularly
opposite manner. The latter (Fig. 3) was similar to the
 Bolton et al.: Two newly discovered Grateloupia species
‘Grateloupia filicina’ morphology, which has been shown to
include many species (De Clerck et al. 2005b). The plants
appeared somewhat different from the usual morphology of
Grateloupia capensis (Stegenga et al. 1997, as G. filicina), which
generally has a branched main axis but is morphologically
quite variable. A second collection on the same aquafarm (11
June 2013) yielded only foliose plants of Grateloupia, similar to
the more undivided specimens in Fig. 2.
Specimens of both morphotypes were sequenced using
the rbcL and cox1 markers, widely used for species-level
diversity assessment and barcoding studies of red algae
(Saunders 2005; Robba et al. 2006; Maggs et al. 2007;
Saunders & Moore 2013). DNA-extraction, amplification
and sequencing of the rbcL gene followed De Clerck et al.
(2005b). In order to sequence the cox1 gene we modified the
original forward and reverse cox1 primers from Saunders
(2005) to fit the Grateloupia cox1 sequence better:
GazF2_Grat ¼ CTAATCACAAAGATATAGGAAC and
GazR1_Grat ¼ ACTTCGGGATGACCAAAAAATCA.
Sequences of the specimens collected in the aquaculture
facilities were added to an alignment of representative
Grateloupia sequences, aligned by eye in MEGA v.6
(Tamura et al. 2013) and subjected to maximum likelihood
analysis using RAxML under a General Time Reversible
model with the CAT approximation to accomodate for rate
heterogeneity (GTRþCAT) model (Stamatakis 2006). The
robustness of the resulting phylogeny was tested using 1000
replicates of a rapid bootstrap heuristic (Stamatakis et al.
2008).
RESULTS
The foliose species (Fig. 2) was identical in its rbcL (1292 bp)
and cox1 sequence (630 bp) to published sequences of
Grateloupia turuturu, both indigenous Japanese G. turuturu
and introduced material from around the world (Fig. 4). The
finely branched Grateloupia sp. 1 (Fig. 3) did not exactly
match any rbcL sequence on GenBank (Fig. 4) but was most
closely related to the Japanese species Grateloupia carnosa
Yamada & Segawa, from which it differed by 6% p-distance.
It can be considered to be a different species from G. carnosa,
as values of interspecific divergence in the rbcL marker in
Grateloupia usually vary from 5% to 10%, with the odd
divergence as low as 1.5% or 2.8% (De Clerck et al. 2005b).
The position of Grateloupia sp. 1 was not resolved in the
cox1 phylogeny. The specimen forms a polytomy with two
clades containing G. turuturu, G. phuquocensis Tanaka &
Pam-Hoáng Hô, G. subpectinata Holmes, G. taiwanensis
M.Lin & H.Y.Liang, G. californica Kylin, on the one hand
(Fig. 5), and G. asiatica S.Kawaguchi & H.W.Wang, G.
divaricata Okamura, and several Prionitis species on the
other hand.
DISCUSSION
It is very difficult to separate many species of Grateloupia
based on their gross morphology and anatomy, and in
addition many species are morphologically plastic. Follow-
661
ing the discovery of G. turuturu, there are now three foliose
species on the South African west coast: G. longifolia, G.
belangeri and G. turuturu. None of these have been recorded
on the south coast (east of Cape Agulhas, Anderson et al.
2009). Grateloupia belangeri is easily identifiable by its
consistently corrugated thallus with irregular perforations
(Stegenga et al. 1997). Grateloupia longifolia (Stegenga et al.
1997, as G. doryphora) is common and abundant in the lower
regions of sand-inundated rocky shores, where it forms large
monospecific stands usually consisting of smooth, elongated
strap-shaped blades with wavy edges. There are also plants
with ‘‘broader blades proliferating irregularly from the
margins’’ which were considered conspecific by Stegenga et
al. (1997). Without considerable further collections and
sequencing it would not be possible to ascertain whether any
of these proliferous foliose plants occasionally found on
rocky shores in the region are G. turuturu, or indeed some
other foliose species of Grateloupia. The same difficulties
have been documented in separating G. turuturu from the
indigenous Grateloupia lanceola (J.Agardh) J.Agardh in the
Iberian Peninsula (Barreiro et al. 2006) and Grateloupia
lanceolata (Okamura) Kawaguchi in the Mediterranean Sea
(Barreiro et al. 2006; Figueroa et al. 2007). Because of the
impossibility of separating proliferous plants, which may be
G. longifolia, from G. turuturu by morphology alone, it
would not be possible to speculate on the time of
introduction into, or the distribution of, the latter in South
Africa. As this species was not discovered in the South
African collections sequenced by De Clerck et al. (2005) and
it was found on an aquafarm, a usual site for Grateloupia
introductions worldwide, there is clearly good evidence that
it is a recent introduction. Further sequencing of new
collections and potentially of herbarium specimens may shed
light on the date of introduction; although, this is rendered
more difficult by the preservation of many older South
African collections in 5% formalin in seawater before
pressing.
The other species (Grateloupia sp. 1) is rather difficult to
differentiate from specimens of Grateloupia capensis, and as
we do not know its identity, we cannot comment on its
distribution. Again, as it was not discovered in the specimens
sequenced by De Clerck et al. (2005) and was discovered on
an oyster raft, it is very likely that it is a recent introduction.
It appears somewhat different morphologically from Grate-
loupia carnosa, which tends to have a wider, more branched
main axis.
Our inability to identify the second introduced species
highlights the need for a framework enabling early detection
of introduced species. Even though accurate and fast
identification is crucial to detect putative invaders among
the native flora, this process is extremely difficult for marine
macroalgae, resulting in alien species often being discovered
years to tens of years after being introduced. Traditionally,
taxonomic identification methods of marine macroalgae
have emphasized vegetative and reproductive features that
are either subject to high variability or largely ineffective for
discriminating species (reviewed in Cianciola et al. 2010; Le
Gall & Saunders 2010; De Clerck et al. 2013). Developing a
database of sequences against which unknown biological
materials can be compared will greatly increase the speed at
which routine identification can be carried out. The fact that
662 Phycologia, Vol. 55 (6)

Figs 4–5. Maximum likelihood phylogeny of Grateloupia estimated under a GTRþCAT model in RAxML based on the rbcL (Fig. 4, left) and
cox1 gene (Fig. 5, right). Shaded boxes corresponds to species that are known to be introduced (light shading) and South African specimens
sequenced in this study (dark shading). Numbers associated with edges correspond to bootstrap values.
 Bolton et al.: Two newly discovered Grateloupia species
the great majority of introduced and invasive seaweeds in the
Atlantic Ocean have their origin in the temperate North-west
Pacific region is to our advantage in establishing an early
detection system. Establishment of a reference DNA-
barcode library of seaweeds from the temperate Western
Pacific Ocean could serve this need.
Following the summary of Mead et al. (2011) and the
additions of Bolton et al. (2011), this report has increased the
published records of introduced seaweeds into South Africa
from six to eight. It is clear from this and other studies that
reporting introduced or ‘‘cryptogenic’’ species of marine
macroalgae based on records of species names without
molecular evidence is very often inaccurate. A good example
is the long list of seaweed species names considered
cryptogenic in Port Phillip Bay, Australia, by Hewitt et al.
(2004), many of which have also been reported in the South
African literature. Further sequencing of South African
seaweeds will undoubtedly reveal further endemics (e.g.
Grateloupia capensis) and introductions (e.g. G. turuturu).
ACKNOWLEDGEMENTS
RJA and JJB acknowledge support from the NRF/SANBI
SeaKeys project, as well as UCT and DAFF. ODC is
indebted to the EU FP7 ERANET Project (SEAS-ERA/
INVASIVES) for financial support. We also thank Sofie
Dhondt and Maggie Reddy for their assistance in the
molecular lab, Mark Rothman for assistance with figures,
and Kevin Ruck for access to oyster rafts.
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Received 30 September 2015; accepted 3 June 2016
Associate Editor: Charles Yarish