ANNAtES • Ser. hist. nat. • 13 • 2003 ■ 2
review article	IJDK 597.5:591.9(262.3-12!
received: 2003-10-01
LESSEPSIAN FISH MIGRANTS REPORTED IN THE EASTERN ADRIATIC SEA:
AN ANNOTATED IJST
Jakov DULČIČ & Armin PALLAORO institute of Oceanography and Fisheries, HR 21000 Split, P.O.BOX S00 E-mail: dulcic@(20r.hr
Lovrenc UPEJ
National institute of Biology, Marine Biology Station, Sl-6330 Piran, Fornacc 41
ABSTRACT
At least nine Lessepsian fish migrants have been so far recorded in the eastern part of the Adriatic: Pampus ar-genteus, Hemirsmphus far, Paraexocoetus mento, Saurida undosquamis, Sphyraena chrysotaenia, Epinephelus coioides, Leiognathus kkinzingeri, Stephanolepis diaspros and Siganus rivuiatus. The Adriatic Sea is becoming an area of the Lessepsian migrants' westward distribution path, which has provided us with some important information on their westward spreading.
Key words: fchthyoiauna, Lessepsian migration, eastern Adriatic, Mediterranean, Red Sea
PESCI MiGRANTI LESSEPSIAN1 RITROVATI IN ADRIATICO ORIENTALE:
LISTA INT EG RATA
siNiis i
!! ritrovamcnto di almeno nove specie ittic.he lessepsiane é stato fin'ora segnalato nella parte orientate del mare Adriático: Pampus argenieus, Hemiramphus far, Paraexocoetus mento, Saurida undosquamis, Sphyraena chrysolae-nia, Epinephelus coioides, Leiognathus kkinzingeri, Stephanolepis diaspros e Siganus rivulatus. 11 mare Adriático sta diventando una delle aree di espansione verso occidente dei migrant! iessepsiani e sono state fornite alcune importanti annotazioni e studi ¡ ¡guardo ¡'espansione verso occidente di nove specie.
Parole chiave: ittiofauna, migrazione lessepsiana, Adriático orientate, Mediterráneo, Mar Rosso
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latov DUlClC tni.; ICSSEPSIAN FISH MIGR ANTS REPORTED IN THE CASTtRN ADRIATIC it'A: AN ANNOTATED UST. 137-144
INTRODUCTION
According to various marine biological surveys, at least 60 exotic fish species of Indo-Pacific origin have been recorded for the Mediterranean after the opening of the Suez Canal (Orsi Reiini, 2001; Golani et at., 2002). Fish and decapod crustaceans as well as molluscs have advanced beyond the limits of the Levant basins. The term "Lessepsian migrant" was coined by for (1969) to characterize the Red Sea species that have passed through the Suez Canal and settled in the Eastern Mediterranean. The spreading of lessepsian fish migrants has already been recorded for the Aegean and Ionian Seas and considerable numbers have reached the Greek, Turkish and Cyprus coasts (Papaconstantinou, 1990; Goiani, 1998, 2000; Corsini & Economidis, 1999; Taskavak etal., 2000; Basusta et al., 2002), while only a few species have been recorded further west and north (Tortonese, 19G7; 1970; Papaconstantinou, 1988; also in Goiani, 1998; Goiani et al., 2002).
Certain changes have been recorded in the Adriatic ichthyofauna, and some Lessepsian fish species were recently reported (in Duicic et a!., 1999; DulCic & Grbec, 2000; Duicic et al., 2002; Lipej & DulCiii, in press). Owing to the several studies recently carried out in the Adriatic, we now have a fairly accurate overview of the exotic species in this basin. On the basis of the above considerations, the purpose of this paper was to examine the distribution and abundance of l essepsian migrants (immigrants) in the Adriatic Sea, especially along the eastern coast (Albanian, Montenegrin, Croatian, Slovenian and Italian waters), taking into account some data on their presence and abundance and on the variation of some abiotic parameters in recent years.
MATERIAL AND METHODS
This study was based mainly on scientific literature and material collected within the framework of research projects conducted by various national research institutions. Other data sources were sports and professional fishermen who have supplied specimens for identification. During this study, data from literature concerning the spreading of lessepsian migrants in the Mediterranean were also analysed. The greater pari of the material is being kept by different Adriatic institutions.
AN ANNOTATED LIST OF LESSEPSIAN MIGRANTS IN THE ADRIATIC SEA
Pampus argenteus (Euphrasen. 1788)
A specimen of butterfish (Stromateidae) was caught off Rijefca (northern Adriatic) in 1896 and was initially identified as Stromateus fiatola (Fig. 1). This specimen {Fig. 2), which is kept in the collection of the Zoological
Museum in Zagreb, v/as identified as Pampus argenteus by Soljan (1948); however, he was doubtful about his identification because P. argenteus is an Indo-Pacific species, occurring mainly in South-east Asia and in the East China Sea. Also, Soljan did not provide any description of the specimen to justify his identification, which remained doubtful until a recent examination of the specimen allowing to confirm Soijan's provisional identification, It is suggested that the specimen could have entered the Mediterranean Sea by following slow-moving vessels or with pelagic medusae, floating wreckages or drifting seaweed. This record, which dates from 1896, represents the first Lessepsian migrant in the Mediterranean Sea (Dulcii et al., in press).
Hemiramphus far (Forsskal, 1775)
Hemiramphus far is widely distributed in the Indo-Pacific from the Red Sea and east Africa to the Philippines and Samoa (Goiani, 2002). In the Mediterranean, it was recorded first in the Eastern Levantine Basin as H. margimtus {Steinitz, 1927), and then successively off Syria, Rhodes and Egypt (in Goiani et al., 2002), A specimen of this species was also recorded along the Albanian coast {Colette & Parin, 1986).
Paraexocoetus mentn (Valenciennes, 1846)
Paraexocoetus mento is widely distributed in the indo-Pacific from the Red Sea to Fiji (Goiani et al., 2002). In the Mediterranean, it was first recorded in the Eastern Levantine Basin (Bruun, 1935) and then successively in the waters of Rhodes and Libya (in Goiani et al.r 2002). This species, too, was recorded in Albanian coastal waters (Parin, 1986).
Saurida mdosquamis (Richardson, 1848)
Saurida undosquamis is widely distributed in the Indo-Pacific from the Red Sea and eastern Africa to Australia and southern japan (Goiani et al., 2002). In the Mediterranean, it was first of all recorded in Israel (Ben-Tuvla, 1953) and then successively in the waters of Cyprus, Turkey, Greece, Libya, Dodecanese?, Crete and Egypt (in Goiani et al., 2002). It is very important commercial fish, caught by trawl in large quantities in the eastern Basin. A single specimen (28 cm total length) has been recorded off the Albanian coast by Rakaj (1995).
Sphyraena chrysotacnia Klunzinger, 1884
The obtuse barracuda Sphyraena chrysotaenia lias a wide distribution and is found in the eastern Mediterranean (Israel, Lebanon and Egypt), in the Indo-Pacific, from the Red Sea, Persian Guif and East Africa through-
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WswtHAOt« a!.: LtSSEPSIAN HSU MIGRANTS RiPOF.UD It-IE EASTERN ADRIATIC SEA- AN aNNOTATCD LIST. 137-144
t|) Pampas argenteus Hem iramphus far Paraexocoetus mento Saurida undosquamis Sphyvaena chrysotaenia Epinephelus coioides Leiognathus klunzirigeri Stephan o I ep is diaspros Siganus rivtdatus
DUBROVNIK ^..KOTOR
o TIRANA
cv? VLORE
V ^
Fig. 1: Records of nine Lessepsian migrants found in the Adriatic Sea. St. 1: Podatki o devetih /esepskth migrantih, ugotovljenih v fadranskem morju.
out Indian Ocean to Australia and japan (Ben-Ttjvia, 1966). it has also been observed in Turkish waters, from Malta, Eastern Aegean Sea, Western Aegean Sea, Ionian Sea and in the Italian and Tunisian coastlines (Golani, 1998). On 10 August 2000, a 123 mm total length specimen of this species was captured with a small beach seine in the Ray of Gornji Mofunat (southern
Adriatic) at a depth of 6 m together with several specimens of 5, sphyraena (Pallaoro & DultiO, 2001). The specimen was preserved in formalin and deposited in the collection of the Institute of Oceanography and Fisheries in Split. This is the northernmost record of this species in the Mediterranean area.
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Epinephelus coioides (Hamilton, J822)
The orange-spoiled grouper Epinephelus coioides occurs in the Red Sea, southwards to (at (east) Durban, and eastwards to Ryukyu islands, Paiau, and Fiji (Golani et a!., 2002). The first specimen recorded in the Mediterranean Sea was misidentjfied by Ben-Tuvia & Lourie [1969) as Epinephelus tauvina. Another specimen was also caught in Haifa Bay; the local fishermen claimed that this species was caught only on rare occasions (Golani, 1996). It is very rare and only few specimens have been collected in the Mediterranean (Golani el a/., 2002). An orange-spotted grouper specimen of 12 cm total length was caught by fishing net on 16 May 1998 about 0.9 km from Trieste, northern Italy, and then maintained at the Civic Marine Aquarium of Trieste (presently the specimen measures 52 cm total length) (Parenti & Bressi, 2001). This is the northernmost record of this species in the Mediterranean Sea.
Leiognathus klunziitgeri (Steindachner, 1R98)
The ponyfish Leiognathus ktun/ingeri has been reported only from the Red Sea, but as Leiognathus badly needs taxonomic revision, the distribution range might change (Golani <?f a/., 2002). In the Mediterranean, it was first recorded in Syria (Gruvel, 1931); successively in the waters of Israel, Rhodes, Turkey, Lampedusa island, NE Greece and Egypt (in Golani et a!., 2002). It is very common in the Eastern Mediterranean and caught in large numbers as bycatch in trawl. On 29 June 2000,
an 85 mm total length specimen of ponyfish was captured by beach seine in Saplunara Bay (Mljet Island, southern Adriatic) at a depth of 4 m on sandy bottom (Dliicic & Pallaoro, 2002). It has been deposited in the ichthyoiogicai collection of the Institute of Oceanography and Fisheries in Split. This is (he northernmost record of this species in the Mediterranean Sea.
Stephanolepis diaspros Fraser-B runner, 1940
The filefish Stephanolepis diaspros has been reported from the Red Sea to the Arabian Gulf (Golani et al„ 2002). In the Mediterranean Sea, it was first recorded in the Eastern Levantine Basin (Steinitz, 1927); successive in the waters of Syria, Cyprus, Rhodes, Gulf of Gabes (Tunisia), Gulf of Taranto (Italy), Crete, Saronikos Gulf and Gulf of Palermo (Sicily) (in Golani et a/., 2002). It is very common in the Mediterranean Sea. On 23 August 2.002, a 77.3 mm total length specimen of 5. diaspros was found at Ulcinj fish market (southern Adriatic, Montenegro) (DuiCid & Pallaoro, in press, a). According to the Ulcinj fishermen, it had been captured with a beach seine in the area of Hrid Oeran, at a depth of about 20 m on the rocky-sandy bottom. The specimen was preserved in formalin and deposited in the ichthyoiogical collection of the Institute of Oceanography and Fisheries in Split (Fig. 3). This is the northernmost record of this species in the Mediterranean area and the first record of a species from the family Monacanthidae for the Adriatic Sea.
Fig. 2: A specimen of Pampas argenteus (Euphrasen, 1788) kept in the Natural History Musem in Zagreb. (Photo: I. jardas) SI. 2: Primerek vrste Pampus argenteus (Euphrasen, 1788), shranjene v zbirki Hrvatskega prirodoslovnega muzeja v Zagrebu. (Foto: t. jar da s)
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Siganus rivulatus Forsskài, 1775
The rabbitfish .Siganus rivulatus has been reported from tlit: Red Sea and the Gulf of Aden (Colani et ai, 2002). In the Mediterranean, it was first recorded in the Eastern Levantine Basin (Steinitz, 1927); successively in the waters of Syria, Cyprus, Aegean Sea, L ibya, Tunisia and Ionian Sea (in Golani ef ai., 2002). It is very common in the eastern Mediterranean and caught in large quantities by trammel net and purse seine. On S October 2000, two specimens of S/ganus rivulatus {111-149 rum total length) were captured by the beach seine between 07:00 to 09:00 near the islet of Bobara, southern Adriatic (Croatian coast, near Cavtat) at a depth of 15 m on sandy bottom covered by algae and seagrass (DuiCc & Pallaoro, in press, b). They were deposited in the Ichthyologies I Collection of the Institute of Oceanography and Fisheries in Split. This is the northernmost record of this species in the Mediterranean area.
DISCUSSION
Up to date, nine Lessepsian migrants (Tab. 1) have readied the Adriatic Sea. The importance of consecutive records in determining the rate of establishment of Lessepsian fish migrant populations cannot be overemphasized. It is natural for first records lo be published immediately upon discovery and to receive a great deal of attention. But second and subsequent records can certainly add to our knowledge of a migrant species' establishment. There are seven Lessepsian migrant fish species that have been recorded only as single specimens: P. argentëu.% H. far, S. undosquamis, 5. chryso-
taenia, E. coioides, L. khtnzingeri and 5. draspros. There have been no data on the number of recorded specimens for the species P. memo, while two specimens were observed for S. rivulatus. In order to" understand whether these records constitute an abortive episode or rather the founder trailblazers of a sustainable population, it is necessary to report consecutive records. In those cases, where subsequent reports include an extension of the species' distribution, it is clear that there will be second and third records as well. There are still no such cases for the Lessepsian fish species found in the Adriatic Sea. However, second and subsequent records that do not extend the distribution often receive less attention and may not necessarily be published (Colani, 2002). lessepsian fish migrant species may be characterized according to several traits, namely abundance, habitat, feeding habits and size (Golani, 2002).
Nine Lessepsian fish migrants have brought up (together witli previous mentioned species in Dulčič e! al., 2002) the number of species recorded for the Adriatic to 432 and 122 families. The record of P. aigenteus dated from 1896 represents the first Lessepsian migrant in the Mediterranean Sea. The occurrence of tine orarige-spotted grouper L coioides in the Gulf of Trieste (Parent! & Bressi, 2001) is very interesting indeed, since it had been previously recorded only from the coastal waters of Israel and is considered a rare and recent: invader (Golani, 1998). Other seven species were amongst the first Erithrean invaders of the Eastern Mediterranean more than thirty years ago, when recorded as common or very common fish species in the Aegean coastal waters and off Anatolian coast (Ben-Tuvia, 1966). Temperature is the most important abiotic factor in deter-
Tab. i: List of Lessepsian migrants fished in the Adriatic Sea.
Legend: 1 - occurrence: VR - very rare; 2 - habitat: P - pelagic, IP ■ inshore pelagic, BP - bentho-pelagic, B - ben-thic, R - rocky; 3 - feeding habits: Fl - feeders of fish and benthic invertebrates, PL - planktivores, Bt ■ bentbic invertebrates, H - herbivores; 4 - size: S - small, /VI - medium; 5 - area: CT - Gulf of Trieste, NA - northern Adriatic, MA • middle Adriatic, SA ■ southern Adriatic; 6 - first record; 7 - source. Tab. 1: Seznam lesepskih selivk; ugotovljenih v Jadranskem morju.
Legenda: T - pojavljanje: VR - zelo redko; 2 - habitat: P - pelaški, IP - obalno pelaški, BP - bento-pelaski, B - bentoški, R - skalnati; 3 - prehranjevalne navade: Fl - ribe in bentoški ne vretenčarji, PL - planktivoriBI - bentoški nevretenčarji, H - rastlinojedi; 4 ~ velikost: S - majhne, M - srednje velike; 5 - območje: GT - Tržaški zaliv, NA -severni Jadran, MA - srednji Jadran, SA - južni Jadran; G ~ prvi zapis; 7 - vir.
Species	1	2	3	4	5	6	7 !
Pampas aigenteus (Euphrasen, 1788)	VR	P	?	M	NA	1896	Duičid et al. (in press) :
Hemirampbus far (LorsskcU 1775)	VR	IP	PL	7	SA	?	Collette & Parin El 986)
Paraexocoetus mento (Valenciennes, 1846)	?	IP	PL	?	SA	?	Parin (1986)
Sauhda undosquamis (Richardson, 1848)	VR	B	Fl	i	SA	?	Rakaj (1995) lj
Sphvraena c.hrysotaenia Klunzinger, 1884	VR	BP	Fl	M	SA	2000	Pallaoro & Dulčič (2001)
Epinephelus coioides (Hamilton, 1822)	VR	B	Fl	M	GT	1998	Parenti & Bressi (2001)
Leicgnathus klunzingeri (Steindachner, 1898)	VR	B	Bl	S	SA	2000	Dulčič & Pallaoro (2002)
Stephannfepis diaspros Fraser-Brunner, 1940	VR	R	Bl	S	SA	2002	Dulčič & Pallaoro (in press, b)
Siganus rivulatus Forsskal, 1775	VR	B	H	M	SA	2000	Dulčič & Pallaoro (in press, a)
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tsfcov OULČIL et ni: LESSEPSIAN HSH MIGRANTS REPORTED IN THE EASTERN ADRIATIC SEA: AN ANNOTATED UST, 137-144
Fig. 3: A specimen of Stephanolepis diaspros Fraser-Brunner, 1940 caught in the waters off Uicinj (Montenegro). (Photo: A. Pallaoro)
SI. 3: Primerek vrste Stephanolepis diaspros Fraser-Brunncr, 1940, ujet v vodah blizu Ulcinja (Črna gora). (Foto: A. Pallaoro)
mining the dispersal of Lessepsian fish (Golani, 2002). It is not really known what is the impact of the lessepsian migrant in the Adriatic environment and at this stage it is very hard to perform any direct study to assess possible impact. According to Colani (1993), however, the impact of Lessepsian migration on the Levantine basin ecosystem lias been immense. Some authors reported that the diet of Lessepsian predators, such as the brush-tooth iizardfish S. undosquamis, consisted mainly of other Lessepsian fish species (L klunzingeri) and Lessepsian crustaceans (Golani, 1993). Goiarii & Galil (1991) compared the feeding habits of the two indigenous intillels Mulitis barbatm and M. surmuletus to that of the two confamilial Lessepsian migrant Upeneus mollucen-sis and U. pori. The authors found a high rate of similarity in the diet of all four species. Colani (1994) showed that niche partitioning of the eastern Mediterranean mullets is achieved on the bathymetrical axis; Lessepsian mullets occupy shallow waters (20-50 in), while indigenous species dominate at greater depths. However, due to lack of knowledge concerning bathymetric distribution of the indigenous mullets in the eastern Levant, prior to the Lessepsian invasion, it cannot be determined whether a habitat displacement has taken place in this region. An opposite trend has been observed regarding lizardfishes (Synodontidae); the indigenous species Synodus saurus occupies shallower water than the Lessepsian migrant S. undosquamis (Golani, 1993).
Changes in the Adriatic ichthyofauna have been associated with climatic and oceanographic changes (Dulčič et al., 1999; Dulčič & Grbec, 2000; Lipej & Dulčič, in press). Oceanographic changes in the Adriatic can be associated with the climate in the Mediterranean; this is a consequence of the changes in distribution of air pressure over the wider Mediterranean, which causes the horizontal air pressure to vary between the northern and southern Adriatic and hence influences the intensity of water exchange between the Adriatic and the eastern Mediterranean (Grbec et al., 1998). Because the incoming Mediterranean water in the Adriatic, carries nutrient-rich water that affects primary and secondary production, climate change, via its oceanographic influence, can play an important role in the Adriatic ecosystem. The incoming Ionian water (Adriatic ingression) is aiso warmer, and many fish species move towards higher latitudes. Therefore, the strong year-to-year changes in sea surface temperatures, which are closely related to climatic fluctuations, can well be responsible for such range extensions. A general summary of the occurrence of fish species in the Adriatic, over the last 25 years is that numbers of thermopbilous species have increased, that several species, fairly rare or very rare until now, are more abundant, while others are new to the zone (in Dulčič et al., 1999; Dulčič & Grbec, 2000; Lipe j & Dulčič, in press).
The last decade has witnessed an upsurge of comprehensive studies on the phenomenon of Lessepsian fish migration. The Adriatic Sea is obviously becoming an area of the Lessepsian migrants' westward distribution path, which has provided us with some important information on their westward spreading. We are looking forward to the continuation of this scientific effort and hope for further cooperation amongst ichthyologists of the Levant and Adriatic Sea in the study of Lessepsian migration.
ACKNOWLEDGEMENTS
The authors wish to thank Mr. Tihomir Makovec and Mr. Alen Soldo for their help in preparing photographs and figures. This contribution originated on the basis of the results of a bilateral Slovenian-Croatian "Climate change and Adriatic ichthyofauna" research project.
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id sov OUIČIC « aL- lESSt'PSIAN FISH MIGRANTS RCPORTtO IN THF EASTERN ADRIATIC SEA: AN ANNOTATED UST. 1371«
LES EPS K F RIBJE SELIVKE., UGOTOVLJENE V VZHODNEM JADRANU: DOPOLNJFN SEZNAM VRST
Jakov DULČIČ & Armin PALLAORO
Inštitut za oceatiogtafijo i» ribištvo, HR-2100G Split, P.O.BOX 500 E-mail: dulcic@izor.lir
Lovrenc UPE)
Nacionalni inštitut za biologija, Morska biološka postaja, $1-6330 Piran, Fornače 41
POVZETEK
Na podlagi številnih bioloških raziskav so v Sredozemskem morju ugotovili vsaj 60 vrst ribjih lesepskih selivk po odprtju Sueškega prekopa leta 1869. Doslej je bih v vzhodnem Jadranskem morju ugotovljenih devet vrst lesepskih selivk: Pampas argenteus, Henniramphus far, Paraexocoetus mento, Saurida undosquamis, Sphyraena chrysotaenia, Eplnephelus coioides, Leiognathus kluiuingeri, Stephanolepis diaspros in Siganus rivulatus. Vrsfa Pa m pus argenteus je bila šele pred kratkim potrjena kot lesepska selivka, čeprav je bila ujeta v vodah blizu Reke Že davnega 1896. leta. Druge vrsle so bile najdene v obdobju zadnjih dvajsetih le!, večina med njimi pa v zadnjih nekaj letih. Vse vrste lesepskih rib so bile ujete posamič ali kvečjemu v dveh primerkih. Trenutno še nimamo nobenih podatkov o možnem vplivu lesepskih selivk na avtohtono ihtio favno.
Upoštevaje devet novih vrst za jadransko morje, šteje jadranska ribja favna 432 vrst, ki pripadajo 122 družinam. Pojavljanje lesepskih selivk v jadranskem morju je bržkone treba pripisati istim dejavnikom, to je oceanografskim in klimatskim spremembam, zaradi katerih smo v zadnjih desetletjih v Jadranu zabeležili večje število termofilnih južnih vrst.
Ključne besede: ihtiofauna, selitev lesepskih vrst, vzhodni Jadran, Sredozemsko morje, Rdeče morje
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