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First record of the acanthurid fish Zebrasoma xanthurum (Blyth, 1852) in the Mediterranean Sea, with some considerations on the risk associated with aquarium trade

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The occurrence of a single individual of yellowtail tang Zebrasoma xanthurum (Acanthuridae) from Sardinia island (Italy), probably released from an aquarium, is reported. This observation represents the first record of this species in the Mediterranean Sea. General information on the Acanthurid fishes and other non-native species in the Mediterranean is discussed in the light of the ongoing ecological change taking place on rocky reef ecosystems with consideration of implications on the aquarium trade.
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Medit. Mar. Sci., 17/1, 2016, 147-151 147
Short Communication
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
DOI: http://dx.doi.org/10.12681/mms.1470
Abstract
The occurrence of a single individual of yellowtail tang Zebrasoma xanthurum (Acanthuridae) from Sardinia island (Italy),
probably released from an aquarium, is reported. This observation represents the rst record of this species in the Mediterranean
Sea. General information on the Acanthurid shes and other non-native species in the Mediterranean is discussed in the light of
the ongoing ecological change taking place on rocky reef ecosystems with consideration of implications on the aquarium trade.
Keywords: Non-native shes, surgeonsh, Acanthuridae, accidental introduction, aquarium trade, ecosystem shifts, Tyrrhenian
Sea, Italy.
First record of the acanthurid sh Zebrasoma xanthurum (Blyth, 1852) in the Mediterranean
Sea, with some considerations on the risk associated with the aquarium trade
P. GUIDETTI1, L. MAGNANI2 and A. NAVONE3
1 Université Nice Sophia Antipolis, CNRS, FRE 3729 ECOMERS, Parc Valrose 28, Avenue Valrose, 06108 Nice, France
2 Porto San Paolo Dive Center, Via Pietro Nenni, 14A, 07020 Porto San Paolo OT, Italy
3 Marine Protected Area of Tavolara-Punta Coda Cavallo, Via Dante 1, 07026 Olbia, Italy
Corresponding author: guidetti@unice.fr
Handling Editor: Murat Bilecenoglu
Received: 25 August 2015; Accepted: 16 December 2015; Published on line: 29 January 2016
Introduction
The Acanthuridae is a widespread teleost family,
comprising of 84 species, with tropical and subtropical
afnity (Eschmeyer, 2015). Within the acanthurids, the
yellowtail tang, Zebrasoma xanthurum (Blyth, 1852),
is distributed throughout the Western Indian Ocean, in-
cluding the Red Sea, the Persian Gulf and Maldives (see
Froese & Pauly, 2015). There have also been isolated,
individual recordings from the marine waters off Boca
Raton, Palm Beach County, Florida, US (Bartley, 2006)
and off Hoi Ha Wan Marine Park, Hong Kong (Myers et
al., 2012).
Z. xanthurum is reported to occur on coral- and
rocky-reefs (Sommer et al., 1996) within the 2-20 m
bathymetric range and between 24 and 28°C sea water
temperature (Baensch & Debelius, 1997). It is a typical
herbivorous grazer, generally feeding on benthic algae.
Natural predators are primarily large serranids (e.g. ge-
nus Cephalopholis).
Z. xanthurum has a reported maximum length of
37 cm, however it is commonly observed around 10-20
cm (Froese & Pauly, 2015 and references therein). The
body is blue in color with a yellow tail, the head displays
numerous black spots, and in some locations black hori-
zontal lines can be displayed along the sides of the body.
Similarly to other species belonging to the Zebrasoma
genus, the yellowtail tang is characterized by large dorsal
and anal ns accompanied by an extended snout used to
feed upon algae. The tips of the pectoral ns are often
yellowish (Carpenter et al., 1997).
There are no specic conservation measures in place
for this species. The yellowtail tang is not commercially
important for sheries and is considered a minor species
in the aquarium trade. Consequently, the IUCN has clas-
sied this sh as ‘least concerned’ (Myers et al., 2012).
In this work we report the rst known occurrence of
Z. xanthurum (Blyth, 1852) in the Mediterranean Sea and
discuss the ongoing changes in rocky reef ecosystems
throughout the basin and implications of the aquarium
trade.
Materials and Methods
On the 3rd of August, 2015, a single individual of
Zebrasoma xanthurum was observed (L. Magnani) at
Tavolara Island, in a site located within the borders (spe-
cically in the buffer zone) of the Tavolara-Punta Coda
Cavallo Marine Protected Area (Sardinia, Italy; Medi-
terranean Sea; Fig. 1; 40.8847220 N; 9.7097220 E). The
specimen occurred on a rocky bottom covered by mac-
roalgae interspersed with Posidonia oceanica patches at
about 16-17 m depth. Identication was based on photo-
graphs performed while on SCUBA.
Subsequent to the rst sighting, 33 dives (15 in Au-
gust, 10 in September and 8 in October) at the same site
were made (during daytime by the three authors of this
ms) to identify behavioral traits (e.g. feeding and interac-
tions with other shes) via in situ observations, and by
analyzing video footage and pictures. Three dives were
made by the authors in August 2015 with HD video to
148 Medit. Mar. Sci., 17/1, 2016, 147-151
help with ne-scale observations of behavior. The main
behavioral features observed were: 1) location of the sh
(where it was observed more frequently) and general pat-
terns of movement; 2) events of interaction with other
shes; 3) events of feeding.
Results
The individual acanthurid observed at Tavolara Is-
land had a total length (TL) of 11-12 cm, and the typical
blue livery with yellow tail, yellowish tips of the pectoral
ns, numerous black spots on the head, and some black
horizontal lines on the body. The caudal n had a linear
margin and the soft portion of the dorsal n was higher
than the spiny portion (specic to the Zebrasoma). This
combination of characteristics allowed for its univocal
identication as a subadult Zebrasoma xanthurum. This
result was further conrmed thanks to in situ observa-
tions, by analyzing pictures and videos, and with two
experts of acanthurids (see Acknowledgements). Dur-
ing all observations, the specimen appeared to be in a
good state of health. The individual actively moved over
rocky bottoms covered by macroalgae, rich in boulders
and crevices, and over patches of the seagrass Posidonia
oceanica. Preference for these habitats suggest suitable
refuge and food. The sh was always observed at one of
two locations and each location was roughly ten square
meters. The individual regularly moved between the two
locations found at 12-14 and 16-18 m depth. Movement
patterns were ‘stop-and-go’, typical of many herbivorous
shes picking at (roughly every 10-15 sec.), and feeding
from, benthic algae that settled on rocks and boulders.
Furthermore, it also fed on epiphytic algae growing on
the leaves of P. oceanica and on other large-sized mac-
roalgae (e.g. Codium bursa).
Other shes observed in the same locations included
typical Mediterranean sh fauna associated with rocky
reefs and P. oceanica. Fish communities of the Tavolara-
Punta Coda Cavallo MPA has been surveyed annually
since 2005 for which a more detailed description can be
found at Di Franco et al. (2009). Based on our eld ob-
servations, the specimen of yellowtail tang at Tavolara
did not interact with other shes except for pairs of the
pomacentrid Chromis chromis, a species well known to
actively defend their nests during the reproduction phase.
Multiple observations (n=11 events observed) of defense
behavior of individual C. chromis against approaches
of the yellowtail tang resulted in the yellowtail tang to
move elsewhere. Relatively large individuals of the ser-
ranid, Epinephelus marginatus, were present in the area
with some observed within close range of the yellowtail
tang. Although representing a potential predator, we did
not observe any predatorial behavior, attraction, or in-
terest towards the yellowtail tang. At times (n=6 events
observed), the yellowtail tang would swim a few meters
into the water column and angle its body at about 45°.
This was assumed to be behavior aimed at attracting
cleaning shes. Nonetheless, this behavior never resulted
in cleaning from Symphodus melanocercus, the only spe-
cie present known to perform the function. With regard
to interactions with divers, generally, the yellowtail tang
at Tavolara was unaffected by diver presence allowing us
to approach the sh for optimal observations.
Fig. 1. Location of Tavolara Island (Sardinia, Italy; central Tyr-
rhenian Sea); the site where the specimen of Zebrasoma xan-
thurum was recorded.
Fig. 2. Photograph of the individual Zebrasoma xanthurum (~11-
12 cm total length) that was observed swimming on rocky reefs
and Posidonia oceanica patches at Tavolara (photo: L. Magnani).
Medit. Mar. Sci., 17/1, 2016, 147-151 149
The sh was last observed in the Tavolara-Punta
Coda Cavallo MPA on September 21st, 2015. At that time
water temperatures at the observation depth (15-20 m)
was 23-24 °C.
Discussion and Conclusion
This observation represents the rst record of the yel-
lowtail tang in the Mediterranean and further conrmed by
the species absence from a recent report of acanthurids by
Langeneck et al. (2015). Including this this observation of
the yellowtail tang, ve species belonging to the Acanthu-
ridae have, to date, been reported from the Mediterranean
Sea. These species include: Acanthurus monroviae (Stein-
dachner, 1876), A. chirurgus (Bloch, 1787), A. coeruleus
(Bloch & Schneider, 1801), Zebrasoma avescens (Ben-
nett, 1828) and Z. xanthurum (Blyth, 1852). As noted by
Langeneck et al. (2015), Acanthurus monroviae was, un-
til recently, the only surgeonsh species reported from the
Mediterranean Sea. However, in the last years, the list of
acanthurid shes recorded from the basin has increased sig-
nicantly from one to ve species (see above).
The increasing number of non-native shes in the
Mediterranean (Zenetos et al., 2012) demands considera-
tion about pathways of introduction during climate change
(thermophilous species). This will help to identify future
scenarios and trajectories of Mediterranean marine eco-
systems, and to eventually adopt appropriate measures for
management or adaptation (Thresher & Kuris, 2004; Zene-
tos et al., 2012; Katsanevakis et al. 2014).
Of the ve acanthurids presently reported from the
Mediterranean, A. monroviae (usually occurring from An-
gola to southern Morocco, Atlantic Ocean, and probably
entered via Gibraltar), observations are sporadic and this
species if considered as a ‘vagrant’ in the areas where it has
been recorded (i.e. Algeria, Israel and NW Mediterranean
; Langeneck et al., 2015 and references therein). Observa-
tions of the other four acanthurids (A. coeruleus, A. chirur-
gus, Z. avescens and Z. xanthurum) have been sporadic, or
from only a single record, indicating these to be related to
intentional/accidental releases from tropical aquaria.
As a global and generally unregulated business, the
aquarium trade is emerging as an important pathway of in-
troduction of non-native marine species (Padilla & Williams,
2004). Padilla & Williams (2004) suggested that releases
may take place intentionally or accidentally, via dumping of
unwanted organisms, the deliberate release from captivity
or by the draining of water containing adult organisms or
their sexual (eggs, larvae) or asexual propagules.
The consequences of invasion (sometimes happening
after introductions) of non-native species to marine ecosys-
tems can result in serious ecological impacts and dramatic
socio-economic costs. Some authors have stated that the
probability for aquarium species to be released is higher in
close geographical distance to large coastal cities (Johnston
& Purkis, 2014). We suggest that in some regions, where
mega-yachts (often equipped with tropical aquaria) are fre-
quent, releases from aquaria can also be frequent especially
during high tourism seasons. From our best knowledge,
there is has been no precedent in the scientic literature con-
cerning introductions from mega yachts, however this is the
avenue that we hypothesize for our recorded individual of Z.
xanthurum in NE Sardinia.
Prevention of releases and possible invasions will re-
quire education and outreach, but also adequate legisla-
tion along with appropriate enforcement efforts to address
aquarium amateurs, shops and industry (Padilla & Williams,
2004; Cô et al., 2013). However, once an introduction has
occurred, eradication or efcient population control through
active removal may be considered the most effective ac-
tions, as natural ecosystems generally do not have the ca-
pacity to limit the expansion of non-native species (Cô et
al., 2013; Hackerott et al., 2013). For instance, the example
of the lionsh (Pterois volitans and P. miles) remains para-
digmatic. The dramatic invasion of the Indo-Pacic lionsh
to the western Atlantic and Caribbean has been attributed to
the aquarium trade. Inter-specic ecological processes such
as predation and competition with native shes has not limit
the lionsh expansion (Hackerott et al., 2013). The success
of the lionsh seems to be due to a combination of life his-
tory traits (e.g. early maturation/reproduction, ecological
plasticity) and the characteristics of the recipient ecosystem
(e.g. favorable climatic conditions, overshing of native
large predators; Côté et al., 2013). Likewise, this successful
invasion has had detrimental and rapid ecological impacts
on native communities (see e.g. Côté et al., 2013). Lionsh
(P. miles) have recently been reported in the eastern Medi-
terranean. However, given the geographical proximity and
connection with the Red Sea via the Suez Canal (where the
lionsh is present), these records from the Levantine basin
are attributed to lessepsian migration (Oray et al., 2015 and
references therein). Despite modelling studies that sug-
gested invasion by the lionsh to the Mediterranean to be
unlikely (Johnston & Purkis, 2014), new records of lionsh
continue to occur (Oray et al., 2015 and references therein)
perhaps providing a warning signal that should be recog-
nized before potential catastrophic damages occur to native
Mediterranean species and ecosystems.
The yellowtail tang, Z. xanthurum, is not a predator
like the lionsh, but rather a herbivorous sh. Until now,
the accidental/deliberate introduction in herbivorous tropi-
cal shes to the Mediterranean via the aquarium trade has
not caused signicant ecological impacts. Nevertheless, the
possible consequences of the increasing number of observa-
tions, should be considered. Non-native herbivorous shes
(notwithstanding the pathway of arrival) have the potential
to dramatically alter native Mediterranean communities. For
instance, the invasion of rabbitsh (Siganus spp.) from the
Red Sea to the eastern Mediterranean resulted in barrens; a
phenomenon that generally arises from urchin over-graving
(Sala et al., 2011). Tropical shes like acanthurids may nd
the Mediterranean temperatures during summer to be ap-
150 Medit. Mar. Sci., 17/1, 2016, 147-151
propriate for survival. Surface waters in Sardinia during Au-
gust 2015 were 26-28°C at surface, and 24-26°C at 16 m
depth. These temperatures, unusual in the past but becom-
ing more frequent in recent years, are probably related to
climatic changes resulting in the warming of marine waters
(Bianchi, 2007). This trend is likely to make Mediterranean
waters increasingly suitable to receive thermophilous spe-
cies (Raitsos et al., 2010).
Previous reports (Baensch & Debelius, 1997) have sug-
gested that the optimal temperatures for Z. xanthurum range
between 24 and 28°C. Thus, we believed that our observed
individual at Tavolara would thrive during the summer, but
mortality would ensue during winter’s 12-14°C. Unfortu-
nately we were unable to conrm this because the specimen
disappeared from the study area at the end of September
2015, while the water temperature was still tolerable. The
absence of the sh suggests that it moved elsewhere or that
it had been successfully attacked by a predator.
Langeneck et al. (2015) stated that the absence of
lessepsian acanthurids in the Mediterranean Sea was due
to their close ecological association with coral reefs; a fea-
ture absent in the Mediterranean Sea (Goren et al., 2011).
Based on the preliminary observations from this study,
the absence of coral reefs, per se, does not seem to pre-
vent Z. xanthurum from surviving (at least temporarily)
in the Mediterranean. Other coral-reef associated shes
have also displayed short-term survival in the Mediterra-
nean (e.g. Chaetodon austriacus and C. larvatus; Goren
et al., 2011, Salameh et al., 2011). Thus, it would seem
that thermal barriers or local predators limit the expan-
sion of many thermophilic shes accidentally released in
Mediterranean waters rather than the absence of coral-
reefs. This is in agreement with Golani et al. (2013) who
stated that Lessepsian migrants and thermophilic Atlantic
species may display a signicant rate of establishment
and invasion success, while tropical species accidentally
introduced (seldom become invasive.
Despite pathway or mechanism, more thermophilous
shes are entering the Mediterranean Sea and they are
increasingly nding conditions conducive for their sur-
vival. They often establish in the warmer southern and
eastern sectors of the Mediterranean basin, and occasion-
ally expand north- and westwards (Azzurro, 2008). This
phenomenon of geographical expansion encompasses a
variety of thermophilic organisms including macroalgae,
plankton, invertebrates and shes (Bianchi, 2007; Galil
et al., 2014). Furthermore, these expansions are con-
sidered one of the most detectable indicators of climate
change in the Northern hemisphere (Perry et al., 2005
and references therein included).
In the last two decades the number of non-native shes
recorded in the Mediterranean has increased signicantly
(Azzurro, 2008; Golani et al., 2013). Most are typically
herbivorous, like Siganus spp. and the ve Acanthuridae.
In the areas where species of Siganus become established,
rocky reef habitats have been dramatically and rapidly
degraded. Furthermore, profound ecosystem shifts occur
where rocky reefs covered in macroalgae are converted to
coralline barrens, a trajectory that is hardly reversible (Sala
et al., 2011; Guidetti et al., 2014). In a recent study carried
out at the Kos Island (Aegean Sea, Greece), Bianchi et al.
(2014) has noted a dramatic regime shift occurring over
the last 30 years. At this site they recorded a rise in sea sur-
face temperatures 1-2°C, human pressures have increased
signicantly and multiple invasions by non-native species
has occured. These changes are further seen in the benthos
where once ourishing macroalgal forests have been re-
placed by sponges and wide barrens. The authors (Bianchi
et al., 2014) attributed these profound changes chiey to
the overgrazing by non-native herbivorous shes (Siganus
luridus and S. rivulatus), whose establishment and spread
have been probably favored by sea warming in combina-
tion with local human impacts (Bianchi et al., 2014; Giak-
oumi, 2014). From this perspective, given that Acanthurid
shes are also herbivores, their potential introduction and
spread across the Mediterranean coastal waters could in-
crease the degradation of Mediterranean rocky reefs. The
shift from macroalgal beds to barrens implies signicant
changes in biodiversity, 3-D architecture of habitats, and
a number of ecosystem functions (including several goods
and services provided to society) (Guidetti, 2006). This
ecosystem shift is attributable to overshing and other hu-
man impacts, climate change and the introduction of non-
native herbivorous species (also including some inverte-
brates like the crab Percnon gibbesii; Evans et al., 2015).
In the worst case scenario, the increase of temperatures
and continued biological introductions combined with
human resource usage, will interact resulting in irrevers-
ible, negative consequences, especially for Mediterranean
rocky reefs.
Acknowledgements
Many thanks are expressed to J. Langeneck and P.
Louisy, who conrmed the identication and provided
valuable information about the species object of this
study, and to Bianchi C.N., who provided interesting ele-
ments for discussion. Special thanks to J. Plass-Johnson
for his useful comments and the revision of the English
language, to the two referees and the handling editor, for
their helpful criticism and suggestions.
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contribution to the application of European Union’s Ma-
rine Strategy Framework Directive (MSFD). Part 2. Intro-
duction trends and pathways. Mediterranean Marine Sci-
ence, 13, 328-352.
... Even though only one introduction, of C. taxifolia, can be ascribed with certainty to aquarium trade (Jousson et al. 1998;Wiedenmann et al. 2001), several other species, including the lionfish Pterois volitans, are suspected to have been introduced by accidental releases from aquaria (Whitfield et al. 2002;Zenetos et al. 2012). Some introductions of marine species (Zebrasoma xanthurum and C. taxifolia) are even assumed to be caused by accidental release from aquaria on board mega yachts that travel the world (Guidetti et al. 2015;Meinesz and Simberloff 2001;Verlaque et al. 2015). Aquarium trade as a pathway for the introduction of marine alien species is, however, still largely unexplored. ...
... It has been previously stated that the probability of introduction of aquarium species is higher in regions close to large coastal cities and in regions where mega yachts with on-board marine aquaria are common due to a higher chance of transfer of seaweed material to the sea (Guidetti et al. 2015;Johnston and Purkis 2014). Personal communication with aquarists revealed that many aquarists dispose aquarium waste in ways that should prevent future introductions; i.e. putting waste in solid waste for landfill or solid waste for compost, indoor plumbing, which is encouraging. ...
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Aquaculture and maritime traffic have been identified as the main vectors for introductions of alien marine species. Except for one notorious case of Caulerpa taxifolia, the role of aquarium trade towards the introduction of alien seaweeds has been largely unassessed. Here, we address the risk of accidental release of seaweed species from the aquarium trade market in European waters. We assessed the importance and diversity of seaweed species in the European online aquarium retail circuit. Our web survey revealed more than 30 genera available for online sale into Europe, including known introduced and invasive species. A second aspect of the study consisted in sampling algal diversity found in aquaria. While allowing direct and accurate identification of the specimens, this approach was targeting not only ornamental species, but also seaweeds that may be accidentally present in the aquarium circuit. By DNA-barcoding we identified no less than 134 taxa, 7 of which are flagged as introduced in Europe and 5 reported as invasive. Climate envelope models show that at least 23 aquarium species have the potential to thrive in European waters. As expected by the tropical conditions in most aquaria, southern Atlantic regions of Europe and the Mediterranean are the most vulnerable towards new introductions. Further predictions show that this risk will increase and shift northwards as global warming proceeds. Overall our data indicate that aquarium trade poses a potential risk of new seaweed introductions, and calls for a cautious approach.
... Even though only one introduction, of Caulerpa taxifolia, can be ascribed with certainty to aquarium trade (Jousson et al., 1998;Wiedenmann et al., 2001), several other species, including the lionfish Pterois volitans, are suspected to have been introduced by accidental releases from aquaria (Whitfield et al., 2002;Zenetos et al., 2012). Some introductions of marine species (Zebrasoma xanthurum & Caulerpa taxifolia) are even assumed to be caused by accidental release from aquaria on board mega yachts that travel the world (Meinesz, 1999;Guidetti et al., 2015;Verlaque et al., 2015). Aquarium trade as a pathway for the introduction of marine alien species is, however, still largely unexplored. ...
... It has been previously stated that the probability of introduction of aquarium species is higher in regions close to large coastal cities and in regions where mega yachts with on-board marine aquaria are common due to a higher chance of transfer of seaweed material to the sea (Johnston & Purkis, 2014;Guidetti et al., 2015). Personal communication with aquarists revealed that many aquarists dispose their waste in ways that should prevent future introductions; i.e. putting waste in solid waste for landfill or solid waste for compost, which is encouraging. ...
... The Monrovia surgeonfish, Acanthurus monroviae Steindachner, 1876, was first recorded in 1981 from Spain (Crespo et al. 1987), and has since been reported from several other Mediterranean countries (see Batjakas et al. 2015 and references therein). The other five species are much more recent additions to the Mediterranean ichthyofauna: Zebrasoma flavescens (Bennett, 1828) was reported from the Balearic Sea, near Sitges (Spain), in 2008 (Weitzmann et al. 2015); Acanthurus coeruleus Bloch and Schneider, 1801, was first sighted in 2011 in Cyprus (Langeneck et al. 2012); Acanthurus chirurgus (Bloch, 1787), was recorded from off Elba Island, Tyrrhenian Sea in 2012 (Langeneck et al. 2015); Zebrasoma xanthurum (Blyth, 1852) was sighted in Sardinia in 2015 (Guidetti et al. 2016); while Paracanthurus hepatus (Linnaeus, 1766) was observed off Bat Yam, Israel in 2015 (Marcelli et al. 2016). Apart from A. monroviae, only A. coeruleus has managed to establish itself in the Mediterranean (Golani et al. 2015;Langeneck et al. 2015); the other four species are only known from single observations. ...
... Indeed, the aquarium trade was considered to be the most likely introduction pathway for the specimen recorded from Elba Island (Langeneck et al. 2015). An aquarium release has also been considered as the most likely mode of introduction for most of the Acanthuridae reported from the Mediterranean: A. coeruleus (Langeneck et al. 2012), P. hepatus (Marcelli et al. 2016), Z. flavescens (Weitzmann et al. 2015), and Z. xanthurum (Guidetti et al. 2016). However, for A. coeruleus, a natural range expansion may be a better explanation (Golani et al. 2015, but see Marcelli et al. 2016). ...
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The doctorfish Acanthurus chirurgus (Bloch, 1787) is reported for the first time from the central Mediterranean, based on a specimen caught in Maltese waters during August 2016. Since the only previous Mediterranean record of this species was based on a single individual observed in the Tyrrhenian Sea, the present record likely represents an independent introduction that may have occurred through the aquarium trade or via shipping. Two other surgeonfish species, Acanthurus coeruleus Bloch and Schneider, 1801 and Acanthurus monroviae Steindachner, 1876, were previously recorded from the central Mediterranean. While A. coeruleus may have established a population in the Levantine Sea, like A. chirurgus it has only been reported once from Malta (and from the central Mediterranean in general); both A. coeruleus and A. chirurgus are, therefore, considered to be casual species in Maltese waters. In contrast, A. monroviae was reported from several Mediterranean countries including Tunisia and Malta in the central Mediterranean. Here we present several authenticated reports of this species from Maltese waters, which strongly suggest that it has managed to establish a population in this region, although the possibility of multiple introductions cannot be excluded.
... Fishes belonging to this order are typically from tropical and subtropical coral reef ecosystems [67], suggesting their introduction from the Red Sea through the Suez Canal, since there are no native species from the order Acanthuriformes in the Mediterranean Sea. To date, eight acanthurid species, mostly with Red Sea and Indo-Pacific Ocean origins, have been observed in the Mediterranean Sea for the first time in the 2000s [68][69][70][71][72][73], although our data suggest they could have arrived earlier, sometime between the year 1960 and 1980. The strongest wave of exotic species arrivals in the eastern Mediterranean Sea occurred in 1998 due to an abrupt shift in the increasing eastern Mediterranean SST [74], although the arrivals of exotic species are expected to continue increasing due to further global trade [75]. ...
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Anthropogenic impacts on marine ecosystems have led to a decline of biodiversity across the oceans, threatening invaluable ecosystem services on which we depend. Ecological temporal data to track changes in diversity are relatively rare, and the few long-term datasets that exist often only date back a few decades or less. Here, we use eDNA taken from dated sediment cores to investigate changes over approximately the last 100 years of metazoan communities in native (Cymodocea nodosa and Posidonia oceanica) and exotic (Halophila stipulacea) seagrass meadows within the eastern Mediterranean Sea, at two locations in Greece and two in Cyprus. Overall, metazoan communities showed a high turnover of taxa during the past century, where losses of individual taxa in a seagrass meadow were compensated by the arrival of new taxa, probably due to the arrival of exotic species introduced in the Mediterranean Sea from the Suez Canal or the Gibraltar Strait. Specifically, bony fishes (Class Actinopteri) and soft corals (Class Anthozoa) presented significantly higher richness in the past (before the 1980s) than in the most recent time periods (from 1980–2017) and some Cnidarian orders were solely found in the past, whereas sponges and Calanoids (Class Hexanauplia), an order of copepods, showed an increase in richness since the 1980s. Moreover, the Phyla Porifera, Nematoda and the Classes Staurozoa, Hydrozoa and Ophiuroidea were detected in P. oceanica meadows but not in C. nodosa and H. stipulacea, which led to P. oceanica meadows having twice the richness of other seagrasses. The greater richness resulted from the more complex habitat provided by P. oceanica. The combination of eDNA and sediment cores allowed us to reconstruct temporal patterns of metazoan community diversity and provides a novel approach to follow natural communities back in time in the absence of time series and baseline data. The ongoing loss of P. oceanica meadows, likely to be compounded with future warming, might lead to a major loss of biodiversity and the replacement by other seagrass species, whether native or exotic, does not compensate for the loss.
... Tyrrhenian records of these Fishes also represent first sightings for Italy. In particular, A. chirurgus was found in Isola d'Elba (Langeneck et al., 2015b), C. auriga in Cape Miseno (Tiralongo et al., 2018), while Z. xanthurum in Isola di Tavolara (Sardinia) (Guidetti et al., 2016). Lutjanus sebae was recorded in 2016 off Palermo and its potential pathway is still unknown (Deidun & Piraino, 2017). ...
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The re-examination of marine alien species or Non-indigenous species (NIS) reported in Italian Seas by December 2018, is here provided, particularly focusing on establishment success, year of first record, origin, potential invasiveness, and likely pathways. Furthermore, their distribution is assessed according to marine subregions outlined by the European Union (EU) Marine Strategy Framework Directive: Adriatic Sea (ADRIA), Ionian Sea and Central Mediterranean Sea (CMED), and Western Mediterranean Sea (WMED). In Italy, 265 NIS have been detected with the highest number of species being recorded in the CMED (154 species) and the WMED (151 species), followed by the ADRIA (143). Most of these species were recorded in more than one subregion. The NIS that have established stable populations in Italian Seas are 180 (68%), among which 26 have exhibited invasive traits.Among taxa involved, Macrophyta rank first with 65 taxa. Fifty-five of them are established in at least one subregion, mostly in the ADRIA and the CMED. Crustacea rank second with 48 taxa, followed by Polychaeta with 43 taxa, Mollusca with 29 taxa, and Pisces with 28 taxa, which were mainly reported from the CMED. In the period 2012-2017, 44 new alien species were recorded, resulting in approximately one new entry every two months. Approximately half of the NIS (~52%) recorded in Italy have most likely arrived through the transport-stowaway pathway related to shipping traffic (~28% as biofoulers, ~22% in ballast waters, and ~2% as hitchhikers). The second most common pathway is the unaided movement with currents (~19%), followed by the transport-contaminant on farmed shellfishes pathway (~18%). Unaided is the most common pathway for alien Fisshes, especially in CMED. Escapes from confinement account for ~3% and release in nature for ~2% of the NIS. The present NIS distribution hotspots for new introductions were defined on the first recipient area/location in Italy. In ADRIA the hotspot is Venice which accounts for the highest number of alien taxa introduced in Italy, with 50 newly recorded taxa. In the CMED, hotspots of introduction are the Taranto and Catania Gulfs, hosting 21 first records each. The Strait of Sicily represents a crossroad between the alien taxa from the Atlantic Ocean and the Indo-Pacific area. In the WMED, hotspots of bioinvasions include the Gulfs of Naples, Genoa and Livorno.This review can serve as an updated baseline for future coordination and harmonization of monitoring initiatives under international, EU and regional policies, for the compilation of new data from established monitoring programs, and for rapid assessment surveys.
... This new record of alien species, follows others from areas that are characterized by intensive marine activity in Malta, such as the first Mediterranean records of Stegastes variabilis, Lutjanus fulviflamma and Abudefduf hoefleri (Vella et al., 2015a(Vella et al., , b & 2016a. Nonetheless, one cannot exclude the possibility that C. nigri was an aquarium release given that members of the genus Cephalopholis are exported as ornamental fish (Monteiro-Neto et al., 2003) and in recent years this industry has led to an increase in alien species within the Mediterranean Sea (Guidetti et al., 2016;Zenetos et al., 2016). ...
Article
Background: Non-native marine species, including tropical eastern Atlantic fish species are on the increase in Malta, with shipping activities being the main vector for the movement of these alien species from the Atlantic into the Mediterranean Sea. This calls for cooperation and collaboration between various sea-users and researchers to ensure continuous monitoring of the coastal biodiversity. Methods: Research methods involving local fishermen cooperation in monitoring efforts to identify and track populations of alien species in the Central Mediterranean has led to new records for the genus Cephalopholis (Perciformes: Serranidae) in Malta Morphological characteristics, meristic counts and mitochondrial DNA sequences from specimens of both species sampled from Maltese waters were analysed to confirm their species identify accurately, essential for tracking their respective population expansions in the Mediterranean. Results and conclusion: Results from this study have led to confirmation of the first record of the Niger Hind, C. nigri (Günther, 1859), in the Mediterranean Sea and of the establishment of the African Hind, C. taeniops (Valenciennes, 1828) in Maltese waters.
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Environmental conditions are shaping the spatial distribution of marine species worldwide. However, climate change may alter their future distribution, impacting marine resources exploitation and ecosystems balance. In this context, this PhD identifies climate induced impacts in species and geographical areas, by focusing on some species, indigenous or non-indigenous, of commercial interest in the Mediterranean.Based on the ecological niche concept, that defines the potential distribution of a species according to the environmental conditions in which it is observed, we developed a contemporary and future distribution modelling procedure for marine species. This procedure includes an ensemble of statistical algorithms, future climate models and scenarios while accounting for common ecological niche modelling limitations. Applied to small pelagic fish and cephalopods, we projected major climate induced impacts in the Mediterranean Sea by 2100, including local extinctions in its south-eastern basin. Conversely, we projected a distributional range expansion of most of the studied species towards the North, Norwegian and Baltic seas. In the Gulf of Lion, the small pelagic fish distributional range shifts may indirectly impact their harvesting capacity as well as the productivity of low trophic levels. The combined effects of climate warming and the opening of the Suez Canal induced biological invasions, especially in the South-East Mediterranean. These non-indigenous Mediterranean species may be of commercial interest subject to future harvesting. After quantifying the invasive potential of several non-native Mediterranean marine species, according to their functional and ecological traits, we applied our modelling procedure to estimate their future distributional range expansion. We projected a major distributional range expansion of non-native species in the whole Mediterranean Sea by 2100, especially for warming exceeding 2°C.This work highlights the sensitivity of the Mediterranean Sea to climate change while proposing adaptation and conservation perspective of species and ecosystems facing the upcoming climate trends of the 21st century.
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The human-mediated introduction of marine non-indigenous species is a centuries-if not millennia-old phenomenon, but was only recently acknowledged as a potent driver of change in the sea. We provide a synopsis of key historical milestones for marine bioinva-sions, including timelines of (a) discovery and understanding of the invasion process, focus-ing on transfer mechanisms and outcomes, (b) methodologies used for detection and monitoring, (c) approaches to ecological impacts research, and (d) management and policy responses. Early (until the mid-1900s) marine bioinvasions were given little attention, and in a number of cases actively and routinely facilitated. Beginning in the second half of the 20 th century, several conspicuous non-indigenous species outbreaks with strong environmental, economic, and public health impacts raised widespread concerns and initiated shifts in public and scientific perceptions. These high-profile invasions led to policy documents and strategies to reduce the introduction and spread of non-indigenous species, although with significant time lags and limited success and focused on only a subset of transfer mechanisms. Integrated, multi-vector management within an ecosystem-based marine management context is urgently needed to address the complex interactions of natural and human pressures that drive invasions in marine ecosystems.
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The possibility that the recent expansion of the Suez Canal could trigger an entirely new twenty first century wave of invasions was investigated. Results showed that only 19 new alien species were detected after August 2015 (date of the last Suez Canal enlargement). Five of the newcomers have already established viable populations. Between August 2015 and August 2017 approximately 9,5 new species (mostly fish) entered the Mediterranean annually, 7 of them via the Suez Canal unaided. The next most important pathway is Transport - Stowaway: Shipping, while intentional releases from aquaria appear to play an important role. Our results confirm previous findings on the decreasing rate of introductions, which is not affected by the recent expansion of the Suez Canal. Conclusively, the rate of bio invasions via the Suez Canal has not “doubled” as anticipated but rather decreased in relation to previous years. © 2017, Institute of Oceanography and Fisheries. All rights reserved.
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The occurrence of the doctorfish Acanthurus chirurgus is reported for the first time in the Mediterranean Sea, off Elba Island, Tyrrhenian Sea (42.726667° N, 10.434444° E). This record is tentatively related to aquarium release. The occurrence of Acanthuridae in the Mediterranean Sea is briefly reviewed, and some distributional notes on Acanthurus coeruleus and Acanthurus monroviae in the Mediterranean are provided.
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The Red Sea species, the Orangeface Butterflyfish, Chaetodon larvatus, is recorded for the first time from the Mediterranean. Its occurrence there is evidentially the result of entering the Mediterranean via the Suez Canal.
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A single specimen of the blacktail butterflyfish, Chaetodon austriacus, one of the most common butterflyfishes in the Red Sea, was collected in the port of Ashdod, on the Mediterranean coast of Israel in August 2011. The present record demonstrates a greater than expected plasticity in habitat choice and feeding habits in a species considered an obligate corallivore. Recent records of Eritrean coral-reef associating species in the Mediterranean serve as a warning that life-history based bioinvasion risk assessment has limited predictability in cases where species have broader environmental tolerances than their native range would seem to indicate.
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An updated review of marine alien species and other ‘newcomers’ recorded from the Maltese Islands is presented on account of new records and amendments to a previous review in 2007. Species were classified according to their establishment status (‘Questionable’, ‘Casual’, ‘Established’, ‘Invasive’) and origin (‘Alien’, ‘Range expansion’, ‘Cryptogenic’). A total of 31 species were added to the inventory, while 6 species have been removed, bringing the total number of species to 73. Of these, 66 are considered to be aliens (or putative aliens but with uncertain origin) with the remaining 7 resulting from range expansion. Six records are considered to be questionable and hence unverified. For verified records, the dominant taxonomic groups are Mollusca (represented by 21 species) and Actinopterygii (15 species), followed by Crustacea (8 species) and Rhodophyta (7 species). Eight of these species (aliens: Caulerpa cylindracea, Lophocladia lallemandi, Womersleyella setacea, Brachidontes pharaonis, Percnon gibbesi, Fistularia commersonii, Siganus luridus; range extender: Sphoeroides pachygaster) are considered to be invasive. The introduction pathway for 30 species is unknown. Amongst the alien species, ‘Shipping’ is the most common introduction pathway, followed by ‘Secondary dispersal’ from elsewhere in the Mediterranean Sea. An increasing trend in the number of alien marine species reported from the Maltese Islands is evident, with a peak of 22 species recorded during the last decade (2001–2010). A discussion on the rationale for including range-expanding species in national inventories of recent arrivals, and in the analysis of trends in records from the Maltese Islands, is included. In particular, the general warming trend of Mediterranean surface waters appears to be facilitating the westward spread of thermophilic alien species from the Eastern to the Central Mediterranean, and the eastward range expansion of tropical and subtropical Eastern Atlantic species.
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