Halimeda incrassata (Bryopsidales, Chlorophyta) in Rhodes, Greece, Eastern Mediterranean

Abstract

The first record of the tropical green seaweed Halimeda incrassata (Bryopsidales, Chlorophyta) in the Eastern Mediterranean Sea is presented, based on several thalli found in the stomach of a silver-cheeked toadfish (Lagocephalus sceleratus), collected off Plimmiri beach, Rhodes, Greece. Species identification was based on morphological and molecular identification using the tufA gene as a molecular marker. The finding comes 10 years after a report on the species in Mallorca (Western Mediterranean Sea), where H. incrassata has spread rapidly. The pathway of its introduction in the Eastern basin is unknown, although shipping or the aquarium trade could be involved in this new introduction. Further studies are necessary for visual documentation of the infested areas around Rhodes and assessment of its possible spread in the following years.

Full text

Mediterranean Marine Science
Vol 24, No 3 (2023)
VOL 24, No 3 (2023)
Halimeda incrassata (Bryopsidales, Chlorophyta) in
Rhodes, Greece, Eastern Mediterranean
GERASIMOS KONDYLATOS, KONSTANTINOS
KALAENTZIS, EIRINI GRATSIA, DIMITRIOS
MAVROULEAS, PANAGIOTIS KASAPIDIS,
KONSTANTINOS TSIAMIS, DIMITRIS KLAOUDATOS
doi: 10.12681/mms.35435
To cite this article:
KONDYLATOS, G., KALAENTZIS, K., GRATSIA, E., MAVROULEAS, D., KASAPIDIS, P., TSIAMIS, K., &
KLAOUDATOS, D. (2023). Halimeda incrassata (Bryopsidales, Chlorophyta) in Rhodes, Greece, Eastern
Mediterranean. Mediterranean Marine Science, 24(3), 633–638. https://doi.org/10.12681/mms.35435
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633
Medit. Mar. Sci., 24/3 2023, 633-638
Halimeda incrassata (Bryopsidales, Chlorophyta) in Rhodes, Greece, Eastern Mediterranean
Gerasimos KONDYLATOS1, Konstantinos KALAENTZIS1, Eirini GRATSIA2, Dimitrios MAVROULEAS1,
Panagiotis KASAPIDIS2, Konstantinos TSIAMIS3 and Dimitris KLAOUDATOS4
1 Hellenic Centre for Marine Research, Hydrobiological Station of Rhodes, Cos Street, 85131 Rhodes, Greece
2 Hellenic Centre for Marine Research, Institute of Marine Biology, Biotechnology and Aquaculture.
P.O. Box 2214, 71003 Heraklion, Crete, Greece
3 Karaiskaki 16 Voula, Athens, 16673, Greece
4 University of Thessaly (UTh), School of Agricultural Sciences, Department of Ichthyology and Aquatic Environment (DIAE),
Fytokou Street, 38446, Volos, Greece
Corresponding author: Gerasimos KONDYLATOS; gkondylatos@hcmr.gr
Contributing Editor: Sotiris ORFANIDIS
Received: 19 September 2023; Accepted: 05 October 2023; Published online: 21 November 2023
Abstract
The rst record of the tropical green seaweed Halimeda incrassata (Bryopsidales, Chlorophyta) in the Eastern Mediterranean
Sea is presented, based on several thalli found in the stomach of a silver-cheeked toadsh (Lagocephalus sceleratus), collected o
Plimmiri beach, Rhodes, Greece. Species identication was based on morphological and molecular identication using the tufA
gene as a molecular marker. The nding comes 10 years after a report on the species in Mallorca (Western Mediterranean Sea),
where H. incrassata has spread rapidly. The pathway of its introduction in the Eastern basin is unknown, although shipping or the
aquarium trade could be involved in this new introduction. Further studies are necessary for visual documentation of the infested
areas around Rhodes and assessment of its possible spread in the following years.
Keywords: Non-Indigenous Species (NIS); Chlorophyta; Levantine; DNA barcoding.
Introduction
During the last decades, intensication of human ac-
tivities in the Mediterranean Sea has resulted in accel-
erated phenomenon marine biological invasions (Pan-
cucci-Papadopoulou et al., 2012; Bianchi et al., 2014;
Zenetos et al., 2022). The marine waters surrounding the
island of Rhodes, especially along the southern part of
the island that is constantly inuenced by the Asia Minor
Current (AMC; Gaines et al., 2006), present subtropical
environmental characteristics that are ideal for the colo-
nization of non-indigenous species (NIS) of tropical or
subtropical origin (Papaconstantinou, 2014).
Macroalgae consist of an important group of species in
terms of their ecosystem services, acting as carbon sinks,
storage sites, habitat-engineering and nutrient removers
(Granier, 2012). In the Mediterranean Sea, macroalgae is
the fourth most successful group of NIS in terms of es-
tablishment success, with 77% of the 161 species consid-
ered established (Zenetos et al., 2022). NIS macroalgae
in Hellenic marine waters (Aegean, Cretan, Ionian and
Levantine Seas) include four species of Ochrophyta, 12
Rhodophyta and four Chlorophyta, excluding cryptogen-
ic and questionable taxa, according to the latest published
data (Tsiamis, 2012; European Commission et al., 2021).
In the southern Aegean Sea, 11 species are classied as
established NIS, of which ve are invasive, one is casual
and two are questionable as regards their establishment
status (Zenetos et al., 2020), whereas the potential path-
way of introduction of the majority is shipping, followed
by angling/shing, unaided and intentional/unintentional
release.
Halimeda incrassata (J. Ellis) J.V. Lamouroux (Bry-
opsidales, Chlorophyta) is a calcied green macroalgal
species, considered as NIS in the Mediterranean Sea,
and was rst reported in the basin from Mallorca in 2011
(Alos et al., 2016). In Mallorca, H. incrassata exhibit-
ed invasive behaviour due to its rapid population growth
within a few years. The species has also been reported
from Madeira, north-eastern Atlantic (Wirtz & Kauf-
mann, 2005) and the Canary Islands (Sangil et al., 2018).
The species has been agged as top-priority NIS in the
EU-scale Horizon Scanning of marine NIS (Tsiamis et
al., 2020). Naturally, it is distributed in the tropical west-
ern Atlantic, the Indo-Pacic Ocean and the Red Sea
(Guiry & Guiry, 2021; Fig. 1).
Within its natural range, the species usually inhabits
shallow sandy bottoms, although it has also been found in
Mediterranean Marine Science
Indexed in WoS (Web of Science, ISI Thomson) and SCOPUS
The journal is available on line at http://www.medit-mar-sc.net
www.hcmr.gr
DOI: http://doi.org/10.12681/mms.35435
Short Communication

634 Medit. Mar. Sci., 24/3 2023, 633-638
deeper than 60 m waters (Littler & Littler 2000 in Sangil
et al., 2018). In the invaded marine waters of the Canary
Islands, it was found to dominate the mid and deep-water
habitats, whereas in Mallorca the species was not found
below 20 m (Alos et al., 2016; Sangil et al., 2018).
Halimeda incrassata can reproduce both sexually and
asexually by rhizoidal extension and fragmentation (van
Tussenbroek & Barba Santos, 2011), having considerable
growth rates (Multer, 1988; Multer & Clavijo, 2004 and
references within). It is characterized as an ecological en-
gineer with a great potential for modifying native habitats
(Vivó-Pons et al., 2020), with both positive and negative
impacts (Tsirintanis et al., 2022). The species is involved
in the formation of carbonate sediments with a consid-
erable annual production of calcium carbonate (CaCO3),
depending on the solar cycle (Freile & Hillis, 1997; van
Tussenbroek & van Dijk, 2007). Furthermore, the species
provides oxygen (e.g. 25.1 mg of O2 per g of decalcied
dry weight per day in Tahiti: Payri, 1988), nourishment
(e.g. for the sea-urchin Diadema antillarum in Jamai-
ca: Hillis-Colinvaux, 1974; for the bucktooth parrotsh
Sparisoma radians in Virgin Islands: Lobel & Ogden,
1981 and for the pinsh Lagodon rhomboides in the Flor-
ida Keys: Ribble, 2019), shelter to other species (Heck &
Wetstone 1977) and an ideal surface for the development
of epifaunal organisms (Mateo-Ramírez et al., 2022).
Although H. incrassata is not a signicant competitor of
the native phanerogam Posidonia oceanica, it is known
to compete with other macrophytes including Dasycladus
vermicularis (Sureda et al., 2017) and Thalassia testudi-
num (Davis & Fourqurean, 2001). The species could be
favoured by the increasing temperature of the Mediterra-
nean Sea, regardless of acidication, as demonstrated in
aquarium experiments (Campbell et al., 2016).
Herein, the presence of the species in the Eastern
Mediterranean Sea is reported for the rst time from
Rhodian Levantine waters, identied by morphological
observations and DNA barcoding. Possible pathways of
introduction and future challenges are discussed.
Material and Methods
Several thalli of Halimeda incrassata (Fig. 2) were
found in the stomach content of a silver-cheeked toad-
sh Lagocephalus sceleratus individual (TL 59.5 cm,
weight 2350.2 g) caught o Plimmiri beach, SE Rhodes
(35.917203°N, 27.860926°E) with bottom long lines
(length 600 m, 100 hooks size No 10-12) during experi-
mental shing with the most commonly used shing gear,
including static nets, longlines, jigs and bottom traps,
from April 2021 to March 2022. The shing gear was de-
ployed by a commercial 106.5 KW shing vessel at 11-14
m depth, over a sandy-muddy substrate early in the morn-
ing of 6 October 2021 and was retrieved one hour later.
Along with six more individuals of the species, caught
with the same bottom longline, specimens were trans-
ported to the Hydrobiological Station of Rhodes (HSR),
measured and photographed, while their stomach was
removed and analysed for contents. Apart from the chlo-
rophyte, viewing under a stereoscope revealed pieces of
a freshly preyed Atlantic horse mackerel Trachurus tra-
churus, an unidentied decapod and a small unidentied
pelagic crustacean in the stomach of the aforementioned
specimen. Some of the thalli of H. incrassata were placed
in absolute ethanol for DNA extraction, whereas the re-
maining were preserved in 70% ethanol and deposited at
the HSR collection (catalogue number HSR560).
A Nikon SMZ800 stereoscope and a Nikon AW111
camera were used for morphological observations and
photographs of the H. incrassata samples.
For the molecular identication of the specimen,
the plastid gene tufA was used, following Cremen et al.
(2016). Total genomic DNA was extracted from a sample
of tissue (50mg) using the DNeasy Plant Pro kit (QIA-
GEN), according to the manufacturer’s instructions.
The plant tissue was homogenized using TissueLyzer II
(two rounds of shaking at 25 Hz). Extracted DNA was
PCR-amplied using the primers tufAF and tufAR from
Fama et al. (2002) and tufGF4 (5’-GGNGCNGCN-
Fig. 1: Distribution of Halimeda incrassata in the proximity of the invaded areas. The green line indicates the approximate natural
range according to Guiry and Guiry (2021); the red dots indicate the invaded areas.

635
Medit. Mar. Sci., 24/3 2023, 633-638
CAAATGGAYGG-3’) from Saunders & Kucera (2010),
in two dierent PCR combinations (tufAF-tufAR and
tufGF4-tufAR). PCR reactions were performed in a total
volume of 12.5μl and consisted of 1μl (~20ng) template
DNA, 7.75μL of ddH2O, 2.5μL of MyTaq Red Reaction
Buer (5x), 0.25μl of MyTaq™ Red DNA Polymerase
(meridian BIOSCIENCE) and 0.5μL of each primer
(10μM). PCR conditions were as in Cremen et al. (2016).
Sanger sequencing reactions (both forward and reverse)
were performed using the BigDye™ Terminator v3.1
Cycle Sequencing Kit and were electrophoresed on an
ABI 3730xl DNA Analyzer (Applied Biosystems™). The
produced sequence was compared to existing GenBank
sequences using BLAST and was deposited in GenBank
under accession number OQ871581.
Results
Thalli light-green to dark green, calcied, erect,
sparsely branched, composed of segments; segments rath-
er at, becoming barrel-shaped towards the base; they are
unlobed or trilobed, obovate–cuneate, broadest at or near
their tip rather than at or near their base; segment dimen-
sions ranged between 4.16-5.88 mm in height, 2.19-3.55
mm in width, and 0.67-1.57 mm in thickness; holdfasts
were missing.
Anatomical observation revealed a cortex composed
of 2-3 (rarely 4) layers of utricles; utricles not inated, but
rather cylindrical; peripheral utricles adhere to one anoth-
er at their distal end; they measure 70-90 μm in height
and 40-60 μm in width; sub-peripheral utricles measure
100-130 μm in height and 50-70 μm in width; peripheral
utricles in surface view are polygons with slightly round-
ed corners, 40-55 μm in diameter. Our specimens are in
good match with previous descriptions of the species
(Verbruggen et al., 2006; Alos et al., 2016).
The molecular analysis of the specimen produced a
sequence of 813 bp in length, which presented 100% sim-
ilarity with H. incrassata sequences deposited in Gen-
Bank (accession numbers: FJ624534.1, AM049958.1,
KT781884.1), thus conrming the morphological iden-
tication. Moreover, the resulting sequence presents less
than 98% similarity with all the other deposited sequenc-
es of Halimeda species. More specically, our speci-
men presents 98% similarity with Halimeda simulans
M.A.Howe, 1907 (accession number: AM049963.1),
97% with Halimeda monile (J.Ellis & Solander) J.V.Lam-
ouroux, 1816 (accession number: AM049962.1) and Hal-
imeda cylindracea Decaisne, 1842 (accession number:
KM820164.1).
Phylogenetic analysis further shows that our spec-
imen (GenBank: OQ871581) is grouped together in a
separate clade with Halimeda incrassata sequences from
GenBank (accession numbers: FJ624534.1, AM049958.1
and KT781884.1). GenBank sequences AM049957.1 and
AM049959.1 are deposited in GenBank under species
name Halimeda incrassata. However, after revision of
the paper (Verbruggen et al., 2006), they are identied
as Halimeda heteromorpha and Halimeda kanaloana,
respectively, and are represented as such in the phyloge-
netic tree (Fig. 3).
Discussion
The L. sceleratus individual containing the thalli of
H. incrassata was collected from shallow, 11-14m deep,
coastal waters, a depth range where H. incrassata can
proliferate (Wirtz & Kaufmann, 2005; Alós et al., 2016;
Sangil et al., 2018). This information is rather signicant
because it provides an indicative depth zone where initial
underwater observations can begin for the investigation
of the current status of H. incrassata and its spread in
Rhodian waters.
The presence of thalli of H. incrassata in the stomach
content of the strictly carnivorous L. sceleratus is consid-
ered a collateral prey item. However, this is a very impor-
Fig. 2: Thalli of Halimeda incrassata from Rhodes, Greece. (Photo credit: G. Kondylatos).

636 Medit. Mar. Sci., 24/3 2023, 633-638
tant nding not only because this is the rst record of H.
incrassata in the Eastern Mediterranean Sea, but also be-
cause it reveals another possible pathway for the spread
of the species. When the undigested thalli are expelled
through the faeces in an area far from the praying site, it
is likely that H. incrassata will have the opportunity to
germinate and start developing a new population.
It is worth mentioning that during the study period
(April 2021 – March 2022), a total of 724 individuals of
L. sceleratus were collected, mainly with longlines and
jigs. Analysis of their stomach contents revealed the pres-
ence of six specimens of another macrophyte NIS, Hal-
ophila stipulacea (Forsskål) Ascherson. The species is
considered as an established NIS in the south Aegean Sea
(Zenetos et al., 2020). The nding of H. incrassata in the
stomach contents of only one out of the 724 examined L.
sceleratus individuals, suggests the possibility of an early
stage of the colonization process of the species.
Halimeda incrassata is native to the western Atlan-
tic, the Indo-West Pacic and Red Sea waters (Guiry &
Guiry, 2021). Two scenarios regarding the pathways of
introduction of the species to the Rhodian marine wa-
ters are considered as most probable. The rst possible
scenario is that H. incrassata reached the island through
shipping, when fragments mixed with soft bottom mate-
rial were caught on anchors and transported to Rhodes
either from the western Mediterranean or the Atlantic via
the Strait of Gibraltar or the Red Sea via the Suez Ca-
Fig. 3: The phylogenetic position of the Halimeda incrassata specimen in relation to other Halimeda species with available tufA
sequences in GenBank (Neighbour-joining tree using Kimura-2P distances and 1000 bootstrap replicates).

637
Medit. Mar. Sci., 24/3 2023, 633-638
nal. Shipping is a very common vector of introduction
of NIS macroalgae in the Mediterranean Sea (Zenetos
et al., 2018, 2020) and Rhodes is a favourite destination
for cruise ships sailing around the Mediterranean and
adjacent Atlantic. During the tourism seasons of 2020
and 2021, more than 200 cruise ships docked at the tour-
ist harbour (36.445572°N, 28.233499°E) of the island
(ELIME, 2023). Since our nding comes from coastal
water, the anchors of western Mediterranean trawlers
shing in international waters, six nautical miles from the
coasts of Rhodes, are unlikely to have been involved. Ad-
ditionally, ballast waters might also have been involved
in the transportation of the species because H. incrassata
does not have planktonic spores, while its gametes and
zygotes are short-lived. The second scenario involves an
accidental/intentional release from home/private aquaria,
which is a known pathway of NIS introduction (Zenetos
et al., 2018), since this macroalga is used for aquarium
decoration.
In any case, visual inspection of the soft-bottoms near
the ports of the town of Rhodes and along the coastal wa-
ters of southern Rhodes is necessary for drawing safer
conclusions. Furthermore, relevant underwater observa-
tions in the major tourist ports of the Eastern Mediterra-
nean, will further assist in revealing the degree of impli-
cation of shipping, mainly cruising, in the dispersion of
H. incrassata within the basin.
Despite the uncertainty surrounding the pathway of
introduction, the colonization of H. incrassata in the
Western Mediterranean Sea has profound and document-
ed eects on the invaded ecosystem (Tsirintanis et al.,
2022). These include the modication of the synthesis of
the substrate and of sh communities (Nadal Nebot, 2017)
and can be either positive, neutral or negative (Vivó-Pons
et al., 2020). For herbivorous organisms, such as herbiv-
orous sh and sea urchins, the presence of H. incrassata
entails the availability of a new food source. However,
Halimeda species possess physical and chemical defenc-
es in order to avoid predation (Multer & Clavijo, 2004
and references within; Mateo Ramirez et al., 2022 and
references within). In that sense, the incorporation of H.
incrassata in the diet of indigenous and NIS Mediterrane-
an fauna needs further investigation.
Halimeda incrassata is a habitat-engineer (Granier,
2012) and the colonization of the vast sandy and mud-
dy bottoms of the coastal waters of Rhodes could work
in two ways. On the one hand, the formation of elds
of calcareous algae could signicantly contribute to the
reduction of the niches of many sh species and other
organisms that have been using the substrate for preying,
burial and camouage as pointed out by Vivó-Pons et al.
(2020), but on the other hand this substitution could cre-
ate a new niche and favour other species.
Although H. incrassata is known to bear epiphytes
(Nadal Nebot, 2017), no epiphytes were found on the
examined thali of this work, either because of the early
colonization phase or the digestion process. Furthermore,
the possibility of introduction of exotic epiphytes and al-
teration of the diversity of epifaunal organisms (Naim,
1988) should be further investigated.
Acknowledgements
The present work was undertaken within the frame-
work of the project EXPLIAS (“Design and piloting
methods of commercial exploitation of invasive alien
species with a view to contributing to their population
control”; https://explias.gr/, accessed on 24 July 2023),
which was coordinated by the National Technical Univer-
sity of Athens (NTUA) with the collaboration of the Hel-
lenic Centre for Marine Research (HCMR) and the Uni-
versity of the Aegean (UoA) and funded by the Fisheries
and Maritime Operational Program 2014–2020 of the
Greek Ministry of Agricultural Development and Food,
and the European Maritime and Fisheries Fund (MIS No:
5049912) and also by the project “DRESSAGE” (MIS
5045792), funded by the Operational Programme “Com-
petitiveness, Entrepreneurship and Innovation” (NSRF
2014-2020), coordinated by the HSR and co-nanced by
Greek and the European Union. The authors would like
to thank the sherman Mr. Osman Karaosman for his co-
operation throughout the project and the two reviewers
for their valuable contribution to the revision of the man-
uscript.
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