First records of the Red Sea alien mollusc Haminoea cyanomarginata (Gastropoda: Heterobranchia: Cephalaspidea) in the Western Mediterranean

Abstract

The colonization of foreign species into the Mediterranean Sea has increased in number and geographic coverage over the past decades. For instance, the marine mollusc Haminoea cyanomargi-nata has scattered across the Central and Eastern Mediterranean since its description in the Red Sea by Heller and Thompson in 1983. In this study, we add the first records of the species in the Western Mediterranean basin and review the progression of its colonization from the Red Sea. The new records were obtained through the online database of the NGO called Catalan Opisthobranch Research Group (Spain), thus highlighting how citizen science platforms can provide an early warning for marine scientists and managers in relation to exogenous species. ARTICLE HISTORY

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First records of the Red Sea alien mollusc
Haminoea cyanomarginata (Gastropoda:
Heterobranchia: Cephalaspidea) in the Western
Mediterranean
Robert Fernández-Vilert, Joan Giménez, Guillem Mas, Irene Figueroa & Juan
Moles
To cite this article: Robert Fernández-Vilert, Joan Giménez, Guillem Mas, Irene Figueroa & Juan
Moles (2018) First records of the Red Sea alien mollusc Haminoea�cyanomarginata (Gastropoda:
Heterobranchia: Cephalaspidea) in the Western Mediterranean, Journal of Natural History,
52:27-28, 1817-1823
To link to this article: https://doi.org/10.1080/00222933.2018.1497212
Published online: 23 Jul 2018.
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First records of the Red Sea alien mollusc Haminoea
cyanomarginata (Gastropoda: Heterobranchia:
Cephalaspidea) in the Western Mediterranean
Robert Fernández-Vilert
a
, Joan Giménez
a,b
, Guillem Mas
a
, Irene Figueroa
a
and Juan Moles
a,c
a
Catalan Opisthobranch Research Group (GROC), Pontós, Spain;
b
Department of Conservation Biology,
Estación Biológica de Doñana (EBD-CSIC), Seville, Spain;
c
Museum of Comparative Zoology & Department
of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA
The colonization of foreign species into the Mediterranean Sea has
increased in number and geographic coverage over the past
decades. For instance, the marine mollusc Haminoea cyanomargi-
nata has scattered across the Central and Eastern Mediterranean
since its description in the Red Sea by Heller and Thompson in
1983. In this study, we add the first records of the species in the
Western Mediterranean basin and review the progression of its
colonization from the Red Sea. The new records were obtained
through the online database of the NGO called Catalan
Opisthobranch Research Group (Spain), thus highlighting how
citizen science platforms can provide an early warning for marine
scientists and managers in relation to exogenous species.
ARTICLE HISTORY
Received 25 January 2018
Accepted 25 June 2018
KEYWORDS
Bubble snail; non-native
species; marine ecosystems;
citizen science
Introduction
Haminoeid cephalaspidean molluscs are herbivorous snails with a bubble shell that
inhabit shallow waters from tropical and temperate seas worldwide (Rudman 1971;
Malaquias and Cervera 2006). A total of eight species of Haminoea are recognized as
naturally occurring within the European coasts (Malaquias and Cervera 2006), among
which seven species are recognized in the Iberian Peninsula, including the Atlantic
coastline (Cervera et al. 2004), and four have been found in the Catalan coast (NE
Spain), namely H. exigua Schaefer, 1992, H. hydatis (Linnaeus, 1758), H. navicula (da
Costa, 1778), and H. orbignyana (de Férussac) (Ballesteros et al. 2016). Two alien
Haminoea species have been recognized in the Mediterranean, H. japonica Pilsbry,
1895 found in the Adriatic and Tyrrhenian seas and the eastern Atlantic (Hanson et al.
2013), and H. cyanomarginata Heller & Thompson, 1983 found in the Central and Eastern
Mediterranean (Zenetos et al. 2010). The latter species was originally described from a
single specimen, found in the Sudanese Red Sea coast in between coral rubble (Heller
and Thompson 1983). This specimen measured 5.5 mm long × 2.5 mm wide, but
specimens can reach lengths of 15 mm and present a white and purple conspicuous
coloration (Zenetos et al. 2004).
CONTACT Juan Moles moles.sanchez@gmail.com
JOURNAL OF NATURAL HISTORY
2018, VOL. 52, NOS. 27–28, 1817–1823
https://doi.org/10.1080/00222933.2018.1497212
© 2018 Informa UK Limited, trading as Taylor & Francis Group
Published online 23 Jul 2018

The first record of H. cyanomarginata in the Mediterranean Sea was in Greece in 2001 where
it has now established a viable population (Rudman 2003; Zenetos et al. 2004,2008;Pontes
et al. 2012–2018;GBIF.org2016;Köhler2018). Later on, in 2002 H. cyanomarginata settled in
Turkey (Rudman 2003;Çinaretal.2011;Kodiat2018), in 2006 it was found in Malta (Rudman
2003;Mifsud2007; Sciberras and Schembri 2007;Kodiat2018;Köhler2018), and a year after in
Italy (Crocetta et al. 2009; Crocetta and Vazzana 2009; Crocetta 2012;Pontesetal.2012–2018;
Stasolla et al. 2014). Also, a population of 100 specimens was recently discovered in Croatia in
2016 (Pontes et al. 2012–2018) and represents the first record in the Adriatic Sea. Since its
description, the species has spread in the Central and Eastern Mediterranean Sea. Despite the
absence of records from the far eastern Mediterranean, it is now considered one of the most
recent immigrants entering from the Red Sea through the Suez Canal (Zenetos et al. 2004,
2005;Mifsud2007). Here, we report new records and extend the distribution range of the
species into the Western Mediterranean Sea. Also, we demonstrate that citizen science is a
valuable tool for the early awareness of new colonizations as well as for monitoring the
advance and settlement of new populations of alien species (Moles et al. 2017).
Material and methods
Fifteen new records of H. cyanomarginata were gathered from the online database of
the Catalan Opisthobranch Research Group (GROC 2018; see http://www.opistobranquis.
org/ca/guia/329). Two specimens were photographed underwater with a Canon
Powershot S120 at Mallorca in the Balearic Islands by the certified divers Rubén
Castrillo and Rosa Taberner from the GROC Association. Twelve and one additional
specimens were also found in Mallorca by Sèbastien Scala and Javier Atero Cano,
respectively.
Results
Systematics
Class GASTROPODA Cuvier
Subclass HETEROBRANCHIA Burmeister
Order CEPHALASPIDEA Fischer
Family HAMINOEIDAE Pilsbry
Haminoea cyanomarginata Heller & Thompson, 1983
(Figure 1(a),1(b))
Material examined
Two specimens of 10 and 15 mm in length were found in Illa del Toro, Calvià, Mallorca,
Balearic Islands, Spain (39°27ʹ41.75″N, 2°28ʹ17.48″E; Figure 1), on 6 December 2017. The
individuals were found at 27.5 m depth, the water temperature was 17°C. Divers were
only able to photograph the largest individual. Twelve individuals from Cala d’Or (39°
21ʹ55.05″N; 3°14ʹ9.6″E), also in Mallorca, were recorded on 20 December 2017. Finally,
another specimen of 4 mm in length was recorded near Illa del Toro in Ses Penyes
Roges, Mallorca, on 21 January 2018 at 21 m depth. All individuals were casual observa-
tions found by different divers without scientific purposes.
1818 R. FERNÁNDEZ-VILERT ET AL.

Morphological description (Figure 1(a), 1(b))
Body white, purple line delimiting cephalic shield, parapodial and infrapallial lobes, and foot;
with scattered purple patches especially concentred in anterior cephalic shield and parapodial
lobes. Cephalic shield divided posteriorly, forming two well-developed lobes. Eyes present,
slightly delimited by an unpigmented area, two pairs of purple spots found in between them.
Shell external, globose, hyaline, partially covered by cephalic, parapodial, and infrapallial lobes.
Parapodial lobes covering shell, not overlapping. Metapodium oval.
Ecology
A single individual was found crawling on coral rubble in the Red Sea (Heller and Thompson
1983). In the Mediterranean Sea, the species has been spotted both in the daytime and at
night, from 3 to 30 m depth on rocky surfaces covered by a thin algal film and the brown alga
Cystoseira sp., other undetermined algae, and sessile organisms (Rudman 2003; Zenetos et al.
2004; Crocetta et al. 2009; Crocetta and Vazzana 2009; Stasolla et al. 2014). Here, the species
was found in daytime on a clear and well-lit slope, crawling among pebbles partially covered
by Corallinaceae algae.
Distribution (Figure 2(a–c))
Sudan, the Red Sea (type locality; Heller and Thompson 1983), Egypt (Kodiat 2018;Köhler
2018), Oman (Köhler 2018), Saudi Arabia (GBIF.org 2016), Greece (Rudman 2003; Zenetos et al.
2004,2008;Pontesetal.2012–2018;GBIF.org2016;Köhler2018), Turkey (Rudman 2003;Çinar
et al. 2011;Kodiat2018), Israel (Rudman 2003;Köhler2018), Malta (Rudman 2003;Mifsud2007;
Sciberras and Schembri 2007;Kodiat2018;Köhler2018), Italy (Crocetta et al. 2009; Crocetta and
Vazzana 2009; Crocetta 2012;Pontesetal.2012–2018; Stasolla et al. 2014), Croatia (Pontes et al.
2012–2018), and Balearic Islands, Spain (this study).
Discussion
The new records of H. cyanomarginata reported here are the first for the Western
Mediterranean Sea. The morphological description of the specimens analysed in this
study clearly ascribed them to H. cyanomarginata (Heller and Thompson 1983). Since its
Figure 1. Underwater pictures of Haminoea cyanomarginata taken at 27 m depth in Illa del Toro,
Calvià, Mallorca, Balearic Islands. (a) Dorsal view; (b) lateral view.
JOURNAL OF NATURAL HISTORY 1819

description, the species has only been recently recorded a few times around the Red Sea
while it appears frequently in the Mediterranean (see Figure 2). An anti-Lessepsian
migration (i.e. from the Mediterranean to the Red Sea) is very unlikely since the species
was never recorded in the Mediterranean before 2001 (Zenetos et al. 2004), and its
conspicuous and likely aposematic coloration tends to be more frequent in species from
rich and stable environments, such as the Red Sea (Mollo et al. 2008). Although the
means of colonization of H. cyanomarginata into the Mediterranean is still uncertain, it
has progressively colonized from the eastern to the north and west of the Mediterranean
until 2018 (Sciberras and Schembri 2007; Zenetos et al. 2008; Çinar et al. 2011; Stasolla
et al. 2014; Pontes et al. 2012–2018, this study). Similarly, species from warmer waters
seem to easily cope with the Mediterranean environmental conditions, likely favoured
by climate change and anthropogenic activities (Streftaris and Zenetos 2006; Moles et al.
2017). Mollo et al. (2008) suggested that the colonization of H. cyanomarginata could be
related to the ability of biosynthesizing metabolites that were originally obtained from
food de novo, in contrast to other species that depend on its diet to be chemically
defended (see Avila et al. Forthcoming). Emancipating this dietary specialist from the
dependency on its original food may have provided a variety of ecological opportunities
for H. cyanomarginata to further colonize the Mediterranean nearshore basin (Mollo
et al. 2008).
Similarly to H. cyanomarginata, the invasive H. japonica also has great environmen-
tal tolerance and the ability to establish dominant populations in the Mediterranean
(Hanson et al. 2013). Nonetheless, H. japonica has been introduced to the Pacificcoast
of North America and to Europe through the introduction of Japanese oysters and
clams for maricultural purposes (Gosliner and Behrens 2006). The distribution patterns
of some alien heterobranch species belonging from the Red Sea and recorded for the
first time in the Central Mediterranean (e.g. the nudibranchs Melibe viridis and Polycera
hedgpethi) have been frequently explained through shipping transport via ballast
waters (Zenetos et al. 2004) and ship hulls (Giacobbe and De Matteo 2013). Mifsud
(2007) proposed that since the locality where H. cyanomarginata was first observed is
sheltered from strong easterly winds, it may act as an active ship bunkering site during
such weather conditions and, thus, reinforce the hypothesis that H. cyanomarginata
entered the Mediterranean by shipping transport instead of being a true Lessepsian
immigrant. Once established in Greece, the free-living larval stage of H. cyanomargi-
nata may have dispersed around the Mediterranean following the main oceanographic
currents, as proposed for Aplysia dactylomela (Valdés et al. 2013;Moles et al. 2017).
Non-native migrations seem to be common in the Mediterranean Sea, especially
nowadays, due to the rising sea-water temperatures during the last decades
(Francour et al. 1994)andthe‘tropicalization’of its fauna (Bianchi and Morri 2003)
that led to a day-by-day increase in the list of exotic organisms in the Mediterranean
(Zenetos et al. 2010). In this sense, an early awareness of these intruders is vital for
understanding further biogeographic advancements. We want to encourage other
researchers to establish and use platforms such as the Catalan Opisthobranch
Research Group (GROC 2018). This website achieves rapid detection of colonization
events of heterobranch sea slugs through citizen science monitoring, thus becoming
an early warning for marine scientists and managers.
1820 R. FERNÁNDEZ-VILERT ET AL.

Acknowledgements
We would like to thank R Castrillo, R Taberner, S Scala, and JA Cano for providing the records to
the website. Especial thanks are given to three anonymous reviewers for their valuable comments.
We are indebted to the nearly 200 citizen collaborators of GROC that regularly monitor the Catalan
coast and adjacent waters. J Moles was supported by a postdoctoral fellowship from the
Fundación Ramón Areces. This is study #4 of the GROC Association.
Figure 2. Distribution of Haminoea cyanomarginata based on bibliographic data and this study. (a)
General view of the Red and Mediterranean seas showing all documented occurrences including the
type location (red star) and the time periods of 2001–2006 (orange dots), 2007–2012 (green dots),
and 2013–2017 (purple dots). (b) Close-up of the Arabian Peninsula showing the occurrences in the
Red Sea and Oman. (c) Close-up showing the new records from Mallorca in the Balearic Islands.
JOURNAL OF NATURAL HISTORY 1821

Disclosure statement
No potential conflict of interest was reported by the authors.
ORCID
Joan Giménez http://orcid.org/0000-0001-9207-4792
Juan Moles http://orcid.org/0000-0003-4511-4055
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