Anali za istrske in mediteranske študije Annaii di Studi istriani e mediterranei Annais for Istrian and Mediterranean Studies
UDK 5	Annales, Ser. hist. nat., 29, 2019, 1, pp. 1-158, Koper 2019	ISSN1408-533X
UDK 5
ISSN 1408-533X (Print) ISSN 2591-1783 (Online)
AnnaleS
Anali za istrske in mediteranske študije Annali di Studi istriani e mediterranei Annals for Istrian and Mediterranean Studies
Series Historia Naturalis, 29, 2019, 1
KOPER 2019
ANNALES ■ Ser. hist. nat. ■ 29 ■ 2019 ■ 1
Anali za istrske in mediteranske študije - Annali di Studi istriani e mediterranei - Annals for Istrian and Mediterranean Studies
UDK 5	Letnik 29, leto 2019, številka 1
ISSN 1408-533X (Tiskana izd. ISSN 2591-1783 (Spletna izd.;
UREDNIŠKI ODBOR/ COMITATO DI REDAZIONE/ BOARD OF EDITORS:
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ANNALES ■ Ser. hist. nat. ■ 29 ■ 2019 ■ 1
Anali za istrske in mediteranske študije - Annali di Studi istriani e mediterranei - Annals for Istrian and Mediterranean Studies
UDK 5	Letnik 29, Koper 2019, številka 1	ISSN 1408-533X (Print)
ISSN 2591-1783 (Online)
VSEBINA / INDICE GENERALE / CONTENTS 2019(1)
SREDOZEMSKI MORSKI PSI SQUALI MEDITERRANEI MEDITERRANEAN SHARKS
Hakan KABASAKAL
A Review of Shark Research in Turkish Waters...... 1
Pregled raziskav o morskih psih v turških vodah
Hakan KABASAKAL
Finally Under Protection! Status of the Angel Shark, Squatina squatina (Linnaeus, 1758) in Turkish Seas, with Notes on a Recent
Sighting and Incidental Captures........................... 17
Končno zavarovan! Status navadnega sklata, Squatina squatina (Linnaeus, 1758) v turških morjih s posebnim poudarkom na novejša opazovanja in naključne ulove
Sihem RAFRAFI-NOUIRA, Youssouph DIATTA, Almamy DIABY & Christian CAPAPČ
Additional Records of Rare Sharks from
Northern Tunisia (Central Mediterranean Sea)....... 25
Dodatni zapisi o pojavljanju redkih morskih psov iz severne Tunizije (osrednje Sredozemsko morje)
RECENTNE SPREMEMBE V SREDOZEMSKI BIODIVERZITETI
CAMBIAMENTI RECENTI NELLA BIODIVERSITÀ MEDITERRANEA
RECENT CHANGES IN MEDITERRANEAN BIODIVERSITY
Thodoros E. KAMPOURIS, Costas CONSTANTINOU & loannis E. BATJAKAS
Establishment of the Non-Indigenous Prawn Penaeus pulchricaudatus Stebbing, 1914
in the Marine Area of Cyprus................................ 37
Tujerodna kozica Penaeus pulchricaudatus Stebbing, 1914, ustaljena vrsta v vodah Cipra
Ayta? OZGUL & Okan AKYOL
Occurrence of a Lessepsian Swimming Crab, Portunus segnis (Crustacea: Decapoda),
in Southern Aegean Sea, Turkey............................ 43
Pojavljanje lesepske plavajoče rakovice, Portunus segnis (Crustacea: Decapoda), v južnem Egejskem morju, Turčija
Moez SHAIEK, Sihem RAFRAFI-NOUIRA & Christian CAPAPČ
Occurrence and Unusual Abundance of Reticulated Leatherjack Stephanolepis diaspros (Osteichthyes: Monacanthidae) from the Lagoon of Bizerte (Northern Tunisia,
Central Mediterranean Sea).................................. 49
Pojavljanje in nenavadna številčnost afriškega kostoroga, Stephanolepis diaspros (Osteichthyes: Monacanthidae) iz lagune pri Bizerti (severna Tunizija, osrednje Sredozemsko morje)
IHTIOLOGIJA
ITTIOLOGIA
ICHTHYOLOGY
Domen TRKOV, Borut MAVRIČ,
Martina ORLANDO-BONACA & Lovrenc LIPEJ
Marine Cryptobenthic Fish Fauna
of Slovenia (Northern Adriatic Sea)....................... 59
Morska kriptobentoška ribja favna Slovenije (severni Jadran)
Polona PENGAL, Eva HORVAT & Mihael J. TOMAN
Spatial and Temporal Distribution of Anchovy (Engraulis encrasicolus) and Sardine (Sardina pilchardus) Eggs in Slovenian
Territorial Waters (Northern Adriatic).................... 73
Prostorsko in časovno pojavljanje iker sardele in sardona v slovenskem teritorialnem morju
ANNALES ■ Ser. hist. nat. ■ 29 ■ 2019 ■ 1
Sihem RAFRAFI-NOUIRA, Youssouph DIATTA & Christian CAPAPČ
Overview of Trophic Levels Recorded in Teleost Species from Northern Tunisian
Waters (Central Mediterranean Sea)...................... 85
Pregled trofičnih nivojev pri ribah kostnicah vzdolž severnotunizijskih voda (osrednje Sredozemsko morje)
FLORA FLORA FLORA
Nenad JASPRICA, Marija PANDŽA & Milenko MILOVIC
Spontaneous Vegetation on Slag Heaps
in Southern Croatia.............................................. 93
Spontana vegetacija na jalovinah v južni Hrvaški
Amelio PEZZETTA
Le Lamiaceae della Flora Italiana: Distribuzione
Regionale e Considerazioni Fitogeografiche.......... 103
Ustnatice (Lamiaceae) v italijanski flori: regionalna razširjenost in fitogeografski pomisleki
FAVNA FAUNA FAUNA
Manja ROGELJA & Lovrenc LIPEJ
Occurrence of Giant Tun, Tonna galea (Linnaeus, 1758) (Gastropoda: Tonnidae) in the Marine
Waters Off Slovenia (Northern Adriatic Sea).......... 121
Pojavljanje velikega sodca, Tonna galea (Linnaeus, 1758) (Gastropoda: Tonnidae) v morskih vodah Slovenije (severni Jadran)
Jure JUGOVIC & Živa MUHIČ
Spatial Distribution of Three Species of Palaemon Shrimp (Crustacea: Decapoda:
Caridea) in Badaševica River (SW Slovenia).......... 125
Prostorska razporeditev treh vrst kozic iz rodu Palaemon (Crustacea: Decapoda: Caridea) v Badaševici (JZ Slovenija)
MISCELLANEA
Khadija OUNIFI BEN AMOR, Mohamed Mourad BEN AMOR & Jamila BEN SOUISSI
Abiotic Parameters in Tunis Southern Lagoon After an Environmental Restoration and Status of Macrobenthic Biocenosis
(Northern Tunisia, Central Mediterranean Sea)...... 135
Abiotski parametri v tuniški južni laguni po okoljski obnovi in status makrobentoških biocenoz (severna Tunizija, osrednje Sredozemsko morje)
DELO NAŠIH ZAVODOV IN DRUŠTEV ATTIVITA DEI NOSTRIISTITUTI E SOCIETA ACTIVITIES BY OUR INSTITUTIONS AND ASSOCIATIONS
Ana FORTIČ
Protecting Adriatic Biodiversity in Kotor:
The Congress AdriBioPro 2019............................. 143
IN MEMORIAM
In Memoriam of Fabio Perco (1946-2019)
(Lovrenc Lipej)..................................................... 147
Navodila avtorjem................................................ 149
Istruzioni per gli autori.......................................... 151
Instruction to Authors............................................ 153
Kazalo k slikam na ovitku..................................... 156
Index to images on the cover................................ 156
SREDOZEMSKI MORSKI PSI
SQUALIMEDITERRANEI MEDITERRANEAN SHARKS
ANNALES ■ Ser. hist. nat. ■ 28 ■ 2018 ■ 2
received: 2018-11-05	DOI 10.19233/ASHN.2019.01
A REVIEW OF SHARK RESEARCH IN TURKISH WATERS
Hakan KABASAKAL
Ichthyological Research Society, Tantavi mahallesi, Mente§oglu caddesi, Idil apt., No: 30, D: 4, Umraniye, 34764 Istanbul, Turkey
e-mail: kabasakal.hakan@gmail.com
ABSTRACT
Until the last quarter of the 20th century, most of our knowledge on the sharks of the Turkish waters was based on elasmobranch-specific chapters in general ichthyological inventory studies and on a limited number of anecdotal studies. Since the mid-1990s, however, there has been a remarkable rise in the number and quality of shark-specific studies and publications, resulting in a gradual filling of the gaps in our understanding of the sharks of the Turkish waters. Based on the publication dates, there were only 2 shark-specific articles published before 1990, 8 scientific articles about the sharks of the Turkish waters between 1990 and 2000, and as many as 88 papers dealing with several aspects of the sharks of Turkey since, for a total of 96 articles on the sharks of the Turkish waters published between 1968 and 2018. Hopefully, future studies by new generations of researchers will provide new data on several aspects of the sharks of the Turkish waters, which can deepen our understanding of them and complete their life stories.
Key words: shark research, publications, Turkish waters, eastern Mediterranean
REVISIONE DELLA RICERCA SUGLI SQUALI IN ACQUE DELLA TURCHIA
SINTESI
Fino all'ultimo quarto del XX secolo, la maggior parte delle nostre conoscenze sugli squali delle acque della Turchia si basava su capitoli specifici dedicati agli elasmobranchi pubblicati in studi generali di inventario ittologico e su un numero limitato di studi aneddotici. Dalla metà degli anni 90, tuttavia, c'è stato un notevole aumento del numero e della qualità degli studi e delle pubblicazioni specifici sugli squali, con un risultante riempimento graduale delle lacune nella comprensione degli squali delle acque turche. Sulla base delle date di pubblicazione, !'autore riscontra che solo due articoli specifici sugli squali sono stati pubblicati prima del 1990, 8 articoli scientifici sugli squali delle acque turche tra il 1990 e il 2000, e ben 88 articoli riguardanti diversi aspetti degli squali della Turchia da allora, per un totale di 96 articoli sugli squali delle acque turche pubblicati tra il 1968 e il 2018. L'autore spera che studi futuri di nuove generazioni di ricercatori possano fornire nuovi dati su diversi aspetti riguardanti gli squali delle acque turche, al fine di approfondirne la comprensione e completare le loro storie di vita.
Parole chiave: ricerca sugli squali, pubblicazioni, acque turche, Mediterráneo orientale
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Hakan KABASAKAL: A REVIEW OF SHARK RESEARCH IN TURKISH WATERS, 1-16
INTRODUCTION
Despite an anecdotal note on a great white shark, Carcharodon carcharias (Linnaeus, 1758), off the coast of izmir (western Turkey) from the 16th century (Bellonii, 1553), the story of shark research in the seas of Turkey started in the early 1920s. Regardless of their remarkable ecological value, sharks have always been a short chapter in the general ichthyological inventory studies of Turkish marine waters (e.g., Ninni, 1923; Deveciyan, 1926; Ayagli, 1937; Ak§iray, 1987). The first accounts of sharks in the seas of Turkey were by Ninni (1923) and Deveciyan (1926). Besides being two of the most wanted items among collectors of antique books on Turkey's ichthyofauna, these pioneering monumental studies also contain the first scientific inventories of the sharks of the Turkish waters. The chronology of shark research in the mentioned waters can be divided into two distinct eras, with the first reaching up to the last quarter of 20th century, and the second beginning in almost mid-1990s and still continuing. They each have peculiar characteristics that outline the general trends of shark research in the seas of Turkey. While the first era was dominated by a clear disregard of sharks in the general ichthyological studies and a lack of shark-specific research, the second has witnessed a boom in the study of the sharks of the seas of Turkey. In the present article, the author reviews the contemporary status of shark research in Turkish waters in the light of available data.
MATERIAL AND METHODS
The data of the present review were obtained from published journals and electronic sources. To extract data from electronic sources, a structured Boolean search was performed on search engines such as Google Scholar, ScienceDirect, etc., with the following keywords: "sharks", "elasmobranchii", "Turkey", "Levantine", "Black, Marmara, Aegean OR Mediterranean Seas", "distribution", "hexanchiformes", "lamniformes", "squaliformes", "carcharhiniformes". To extract data published in journals before 2000 and not accessible via internet, a manual search was performed. The collected data were arbitrarily grouped under the following headings: 'distribution, occurrence and first record; feeding biology; population dynamics, including studies on age, growth and length-weight relationship; reproduction, including studies on neonates, gravid females and nurseries; morphometry; underwater observations and behaviour; miscellaneous, including studies on conservation, fishery economy, anthropogenic injuries and newspaper portrayals; and general chondrichthyan studies including sharks'; and their contents were reviewed under the respective shark species. Since some of the articles dealt with more than one topic, each of these multi-topic articles was considered as a single article to prevent the overestimation of the total
number of publications. The taxonomic nomenclature of the shark species follows Serena (2005). The distribution of sharks in Turkish waters was based on Ak§iray (1987), Bilecenoglu et al. (2014), Kabasakal (2011b) or Kabasakal et al. (2017). The tabulated results of the data search are available upon request to the author, for further investigation.
RESULTS AND DISCUSSION Overview of the studies
The data search for the present review revealed a remarkable difference between the numbers of shark-specific articles published in each of the two eras of research on the sharks of the Turkish waters (Fig. 1). In the first era, the historical data about sharks in Turkish waters were comprised in general ichthyological inventories (Ninni, 1923; Deveciyan, 1926; Aya§li, 1937) and rare anecdotal notes (e.g., Erazi, 1942; Geldiay & Mater, 1968), which, however, provided occurrence data of some rare (e.g., Oxynotus centrina, Echinorhinus bru-cus) or questionable (e.g., Lamna nasus) or threatened sharks (e.g., Hexanchus griseus, Squatina squatina) in the mentioned marine region. These references also represent some of the earliest occurrence records of sharks in the Levantine Basin, and therefore, provide an understanding of the historical distribution of sharks in the eastern Mediterranean.
Based on publication dates, there were only 2 shark-specific articles published before 1990, 8 scientif-
iiPl	FtTl	jöl	iöT"
Fig. 1: Geographical location of Turkish waters in the Mediterranean ecosystem. The shaded areas indicate the approximate locations of the three possible sharks breeding grounds: (1) in the northern Aegean Sea, from Gokqeada to Foqa, (2) Boncuk Bay in the southern Aegean Sea, and (3) in the Bay of Iskenderun in the eastern Levant.
Sl. 1.: Geografska lega turških voda v Sredozemskem morju. Osenčeni predeli označujejo približne lokalitete treh možnih območij razmnoževanja morskih psov:
(1)	severno Egejsko morje, v predelu Gokqeada - Foqa,
(2)	zaliv Boncuk v južnem Egejskem morju, in (3) zaliv Iskenderun v vzhodnem Levantu.
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Hakan KABASAKAL: A REVIEW OF SHARK RESEARCH IN TURKISH WATERS, 1-16
ic articles about the sharks of the Turkish waters between 1990 and 2000, and as many as 88 papers dealing with several aspects of the sharks of Turkey since, for a total of 96 articles on the sharks of the Turkish waters published between 1968 and 2018.
With regard to the topics of the publications, the largest number of articles (n = 60) dealt with the occurrence, distribution and first records of sharks in Turkish waters, followed by articles about stomach contents and feeding bioecology of sharks (n = 13), reproduction and nurseries (n = 13), morphometrics (n = 13), population dynamics (n = 11), underwater observations and behaviour studies (n = 5), and miscellaneous topics (n = 5) (Fig. 2). The sharks of the Turkish waters were also discussed in general chondrichthyan studies, including those about the batoids of the mentioned marine region (n = 9) (Fig. 2).
Species accounts
HEXANCHIFORMES
HEXANCHIDAE
Heptranchias perlo (Bonnaterre, 1788)
Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Hexanchus griseus (Bonnaterre, 1788)
Distribution in Turkish waters: Black, Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on H. perlo and H. griseus in Turkish waters
The earliest records of the hexanchid sharks, H. griseus and Heptranchias perlo, in Turkish waters were reported in general ichthyological inventories by Ninni (1923), Deveciyan (1926) and Ak§ira§ (1987); their contemporary occurrences in the mentioned marine region were confirmed by Kabasakal (1998a, 2004a, 2005, 2009b, 2013a), Kabasakal and ince (2008), and Ba§usta (2015). Among these, studies by Kabasakal (2005) and Ba§usta (2015) are particularly worth mentioning. On 19 November 2004, one male specimen of H. griseus of 300 cm TL and weighing 250 kg was captured by a commercial gill-netter nearly 3 miles off the coast of Amasra. This single capture extends the Mediterranean distribution of H. griseus to the Black Sea (Kabasakal, 2005). Occurrence of neonates of H. perlo in iskenderun Bay (north-eastern Mediterranean Sea) was recorded for the first time by Ba§usta (2015). In a recent review of large sharks caught by commercial fisheries in Turkish waters, H. griseus was the predominant species accounting for 169 specimens and 43.2% of total captures between 1990 and August 2015 (Kabasakal et al., 2017).
Following the capture of newborns of sevengill sharks in iskenderun Bay, Ba§usta (2015) suggested the possibility of a breeding ground of H. perlo in the north-eastern Mediterranean Sea. In Turkish waters, bony fish constitute the main prey of H. griseus (Kabasakal,
■	Sludiin CndiMHbuliOn, «IJifUo a id fafl ffCOfti	■ V.-Jr'. i irM flg biology
■	suidmon reofodueiion biology	■ si udies on oöimi.mon (Vin (3 p studil» on mi iiv	* Studies Dn miscellaneous moles
■	Liener, tl chofirtnrhHiMin tludlSl	■ udii^i on ..ri!vi-i-l»i Obarva I i fro and bduymui
Fig. 2: Numerical distribution of the topics of articles on the sharks of the Turkish waters, published between 1968 and 2018.
Sl. 2: Številčna porazdelitev tematik prispevkov o morskih psih turških voda, objavljenih med leti 1968 in 2018.
2004a). Available information suggests that H. griseus gives birth between October and late February in the northern Aegean and Marmara Seas (Kabasakal, 2004a). Morphometric measurements of the H. griseus caught in the Sea of Marmara were reported by Kabasakal (1998a). Based on the specimens captured by commercial fishermen in Turkish waters, the length-weight relationship for the bluntnose sixgill shark, H. griseus, was calculated as logTW=2.76xlogTL-4.6 (r=0.92; n=34; sexes combined; Kabasakal, 2006). Analysis of 81 articles related to H. griseus and published in major Turkish newspaper and internet media between 1974 and 2009 revealed that the tenor of the coverage was neutral in 49.3% of the articles, 45.6% were negative and only 4.9% were positive (Kabasakal, 2010c). The effect of anthropogenic and fishing-gear induced injuries on the survival and cryptic mortality of sharks were examined in two recent studies (Kabasakal 2010d, 2017a). Post-release behaviour of H. griseus in Saros Bay (north-eastern Aegean Sea) was also recorded via underwater videography (Kabasakal, 2010d).
SQUALIFORMES ECHINORHINIDAE
Echinorhinus brucus (Bonnaterre, 1788) Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on E. brucus in Turkish waters
In October 2002, a bramble shark E. brucus was imaged by means of a ROV camera at a depth of 1,214 m in the northern Sea of Marmara (Kabasakal et al., 2005). This single recording of the bramble shark shows that E. brucus, once thought extinct in Turkish seas, still occurs
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Hakan KABASAKAL: A REVIEW OF SHARK RESEARCH IN TURKISH WATERS, 1-16
in this area. Recent studies provide further records confirming the contemporary existence of E. brucus in Turkish waters (Kabasakal & Dalyan, 2011; Kabasakal & Bilecenoglu, 2014; Kabasakal, 2017a).
SQUALIDAE
Squalus acanthias Linnaeus, 1758
Distribution in Turkish waters: Black, Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Squalus blainvillei (Risso, 1826)
Distribution in Turkish waters: Black, Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on S. acanthias and S. blainvillei in Turkish waters
Subsequently to the pioneering study of Geldiay and Mater (1968), Kutaygil and Bilecik (1977) reported on the distribution and abundance of the spurdog, S. acanthias, which ranked the second and/or third among the demersal fish along the western and central Black Sea coasts of Turkey. Contemporary occurrence of the congeneric S. blainvillei in Turkish waters was confirmed by Kabasakal and Kabasakal (2004), and Ba§usta et al. (2016).
The main prey of S. acanthias and S. blainvillei is composed of decapod crustaceans and bony fish (Ka-basakal 2002d; Demirhan et al., 2007; Ozutemiz et al., 2009). Decapod crustaceans Liocarcinus sp. and the commercially important deep-water prawn, P. longiro-stris, constituted the main prey items recorded in the stomach contents of S. blainvillei (Kabasakal, 2002d). According to Demirhan et al. (2007), the availability of prey is the main criterion for the feeding strategy of S. acanthias; thus in winter, the main prey item of the spiny dogfish is anchovy (Engraulis encrasicolus). In the eastern Mediterranean population of S. acanthias, the length at 50% maturity was 87.57 cm for males and 102.97 cm for females (Demirhan & Seyhan, 2007). On the other hand, Yigin and i§men (2013) estimated the mean length at 50% maturity for females and males of S. acanthias at 56.4 cm and 52.8 cm, respectively. The structural problems of using spines for determining the age of the spiny dogfish (S. acanthias) were examined by Demirhan et al. (2006), and the authors concluded that the percentage of age reading failure was 70% and 37% on the first and second spines, respectively. One of the previous studies investigated the population structure of S. acanthias along the south-eastern Black Sea coast of Turkey (Duzgune§ et al., 2006). In this study, a total of 267 specimens (85 male and 182 female) were collected and the mean (±se) length and weight were 88.25±2.157 cm and 3319±204 g for males, and 92.55±1.73 cm and 4387±217.6 g for females. The length-weight relationship for the stock was derived as W=0.009*L3.3423 (r2=0.9607) (Duzgune§ et al., 2006). In a previous study carried out in the south-eastern region of the Black Sea, Av§ar (1996) reported that male specimens of S. acanthi-
as dominated the population, the age of this species in the region ranged between 1 and 14 years, and the mean annual growth rate was 7.2 cm. The growth parameters of S. blainvillei were examined based on the specimens captured in Sigacik Bay (Aegean Sea), and the mean size for the examined specimens of S. blainvillei was 21.46+2.21 cm, respectively (Ozutemiz et al., 2009).
CENTROPHORIDAE
Centrophorus granulosus (Bloch & Schneider, 1801) Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014). Centrophorus uyato (Rafinesque, 1810) Distribution in Turkish waters: Marmara Sea (Bilecenoglu et al., 2014).
Review of studies on C. granulosus and C. uyato in Turkish waters
In the early 1990s, the first record of the gulper shark, Centrophorus granulosus, in the Sea of Marmara was reported by Benli et al. (1993), based on specimens caught at a depth of 400 m. Although the congeneric C. uyato was also recorded in the Sea of Marmara in the mid-1990s (Merig, 1995), White et al. (2013) suggested that C. uyato was not a valid species and that further research was necessary to clarify the taxonomic status of this species in Turkish waters (Kabasakal & Karhan, 2015).
ETMOPTERIDAE
Etmopterus spinax (Linnaeus, 1758) Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on E. spinax in Turkish waters
Kabasakal and Unsal (1999) reported rare occurrences of E. spinax caught in deep-water bottom-trawl fishery in the northern Aegean Sea, together with the morphometric measurements of the examined specimens. In a previous study, 116 velvet belly lantern sharks, E. spinax, were caught at depths between 200 and 600 m, in Sigacik Bay (Aegean Sea), and the population was composed of more females than males, at 53.4% and 46.6%, respectively; the maximum total lengths for females and males were 20.5 cm and 18.9 cm, respectively (Bilge et al., 2010).
OXYNOTIDAE
Oxynotus centrina (Linnaeus, 1758) Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on O. centrina in Turkish waters
Based on the chronological order, the first shark-specific article on the distribution and occurrence of sharks in Turkish waters was published in late 1960s. It provided anecdotal data on an angular rough shark (O. centrina) caught in the Bay of izmir (Geldiay & Mater,
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1968). Studies on O. centrina, which is now considered a rare and threatened shark in the entire Mediterranean Sea, continued in the following decades and provided further understanding about the life story, occurrence and status of the angular rough shark in Turkish waters (Kabasakal, 2009a, 2010a, 2015a; Ba§usta et al., 2015; Yigin et al., 2016). A recent review on the occurrence and status of O. centrina in the eastern Mediterranean (Kabasakal, 2015a) revealed that between the late 1800s and 2012, the highest number of O. centrina specimens (72%) was recorded in the Aegean Sea, followed by the Sea of Marmara (21.5%). Contemporary occurrence of O. centrina in Turkish waters was also confirmed by two recent studies (Ba§usta et al., 2015; Yigin et al., 2016). Locomotory and feeding behaviour of the rare angular rough shark, O. centrina, were recorded by means of diver-operated camera in the northern Sea of Marmara (Kabasakal, 2009a). Measurements of O. centrina were reported by Yigin et al. (2016), based on a specimen caught in Saros Bay (north-eastern Aegean Sea). Based on the occurrence of a gravid female in iskenderun Bay, Ba§usta et al. (2015) suggested a possible breeding ground of O. centrina in the region.
DALATIIDAE
Dalatias licha (Bonnaterre, 1788) Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on D. licha in Turkish waters
Kabasakal and Kabasakal (2002) reported rare occurrences of D. licha caught in deep-water bottom-trawl fishery in the northern Aegean Sea. Although the main prey of D. licha is comprised of decapod crustaceans (Lio-carcinus sp. and P. longirostris), remains of the sympatric blackmouth dogfish (G. melastomus) were also found in the stomach contents of the kitefin shark (Kabasakal & Kabasakal, 2002). Based on the occurrence of newborn specimens of D. licha, Kabasakal and Kabasakal (2002) suggested a possible breeding area of the kitefin shark over the bathyal grounds of the north-eastern Aegean Sea. Morphometric measurements of 5 newborn D. licha from the north-eastern Aegean Sea were reported by Kabasakal and Kabasakal (2002). Recently, an adult female of D. licha, 118 cm TL, got entangled in a trammel net set at a depth of 40 m in Iskenderun Bay (NE Mediterranean sea) (Erguden et al., 2017)
SQUATINIFORMES SQUATINIDAE
Squatina aculeata Dumeril, in Cuvier, 1817 Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014). Squatina oculata Bonaparte, 1840 Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Squatina squatina (Linnaeus, 1758) Distribution in Turkish waters: Black, Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on S. aculeata, S. oculata and S. squatina in Turkish waters
In Turkish waters, the angel shark family Squatinidae is represented by 3 species: Squatina aculeata, S. oculata and S. squatina, and their contemporary occurrences have been confirmed by a number of studies (Ba§usta, 2002; Ba§usta et al., 1998; Kabasakal & Kabasakal, 2004, 2014; Yaglioglu et al., 2015). S. squatina is considered one of the largest sharks in Turkish waters, and, historically, it was one of the commercially important shark species in Turkish demersal fishery. However, the remarkable decrease that has been recorded in angel shark populations is alarming, as the survival of the species may be threatened. As recent surveys show, S. squatina accounts for less than 2 percent of the total shark biomass incidentally caught by Turkish fishermen (Yagliglu et al., 2015; Kabasakal et al., 2017 ).
LAMNIFORMES ODONTASPIDIDAE Carcharias taurus Rafinesque, 1810 Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014). Odontaspis ferox (Risso, 1810) Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on C. taurus and O. ferox in Turkish waters
There is no specific study available on odontaspidid sharks in Turkish waters.
ALOPIIDAE
Alopias superciliosus (Lowe, 1839) Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014). Alopias vulpinus (Bonnaterre, 1788) Distribution in Turkish waters: Black, Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on A. superciliosus and A. vulpinus in Turkish waters
Kabasakal (1998b) reported on the incidental capture of a female thresher shark, A. vulpinus, 453 cm TL, by a commercial purse-seiner off §ile coast (south-western Black Sea), on 8 November 1996, and this anecdotal note was followed by further records. Contrary to the species' open water habits, Kabasakal (2007) reported on the coastal occurrences of 19 common thresher sharks (A. vulpinus) that were incidentally captured by coastal stationary netters. Recently, Erguden et al. (2015) reported on a single male thresher shark, 392 cm TL and weighing ca. 180 kg, captured incidentally in purse-
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-seine fishery in iskenderun Bay; this was the first record of A. vulpinus from the north-eastern Mediterranean coast of Turkey. The first record of the congeneric bigeye thresher shark, A. superciliosus, in Turkish waters dates back to the early 2000s (Mater, 2005; Bay of Gokova, south-eastern Aegean Sea); a few years later it was recorded in the Sea of Marmara (Kabasakal & Karhan, 2008). The female bigeye thresher shark, 450 cm TL, caught on 28 February 2011 off Fethiye coast, is one of the largest specimens of A. superciliosus ever recorded in the Mediterranean Sea and worldwide (Kabasakal et al., 2011). Based on the total number (n = 392) of large sharks caught by commercial fishermen between 1990 and August 2015 in Turkish waters, A. superciliosus and A. vulpinus accounted for 2.5% and 9.9% of the total catch, respectively (Kabasakal et al., 2017).
CETORHINIDAE
Cetorhinus maximus (Gunnerus, 1765) Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on C. maximus in Turkish waters
Early writings on the occurrence of basking sharks in Turkish waters date back to the 1990s, when an anecdotal record of basking shark, Cetorhinus maximus, was reported from north-eastern Levantine waters (Kidey§, 1997). It was followed by further records off the Turkish coasts, particularly in the Bay of Antalya (Kabasakal, 2002a, 2004b, 2013b). In January of 2009, an adult male basking shark was accidentally caught in a stationary net in the waters some 2 nautical miles off Kugukkuyu (north Aegean Sea); its total length measured ca. 1,000 cm (Kabasakal, 2009c). According to Kabasakal (2009c), this specimen is the largest well-documented basking shark recorded in the Mediterranean to date. In a recent review of the status of basking sharks in the eastern Mediterranean, Kabasakal (2013c), based on the extremely low number of records off Turkish coast since the 1950s, emphasized the rarity of C. maximus in Turkish waters and the need for a specific monitoring program accompanied by zooplankton surveys that would determine the seasonal movements of basking sharks in the mentioned region and answer the questions whether the occurrence of this species in Turkish waters exhibits seasonality and site fidelity or not.
LAMNIDAE
Carcharodon carcharias (Linnaeus, 1758) Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on C. carcharias in Turkish waters
In a 16th century record, Bellonii (1553) reported on the occurrence of C. carcharias off izmir coast. Following this historical note, this top predator was listed in the general ichthyological inventories of Turkish waters
(Ninni,1923; Deveciyan, 1926; Ayagli, 1937; Ak§iray, 1987) When talking about the sharks of the Mediterranean Sea, the great white shark, C. carcharias, has always been the "top star" of research efforts and incidental captures of this predator have always found room in newspaper reports as well. Therefore, a detailed search in newspaper archives covering the period between the early 1900s and the late 1960s yielded several articles about specimens of C. carcharias incidentally captured by tuna hand-liners in the Bosphorus Strait during that time (Kabasakal, 2003a, b). Further research revealed the presence of C. carcharias in Marmara and Turkish Aegean waters between the 1960s and the 1990s (Kaba-sakal 2008, 2011a; Kabasakal & Kabasakal, 2004). Following the capture of two newborns of the great white in Edremit Bay (northern Aegean Sea) in the summer of 2008, contemporary occurrence of C. carcharias in Turkish waters was confirmed (Kabasakal & Gedikoglu, 2008) and this incidence was followed by the captures of additional specimens (4 newborns and 3 juveniles) in the north-eastern Aegean Sea, in the coastal zone extending from Foga (central Aegean Sea) to Gokgeada (north-eastern Aegean Sea) (Kabasakal, 2014; Kabasakal & Kabasakal, 2015; Kabasakal et al., 2009). Among the captured newborns, a north Aegean Sea specimen (85 cm TL) caught by a coastal trammel netter in Edremit Bay on 6 July 2011, is possibly the smallest neonate great white shark reported from Mediterranean waters to date (Kabasakal, 2014). The capture of neonate, young-of-the-year and juvenile white sharks suggested the presence of a breeding ground of C. carcharias in the central and northern coasts of the Turkish Aegean Sea (Kabasakal, 2014; Kabasakal & Kabasakal, 2015; Kabasakal et al., 2009). In light of the available data, C. carcharias is an extant lamnoid shark in the Aegean waters off the Turkish coast, but presently not occurring in the Sea of Marmara (Kabasakal, 2016a, Kabasakal et al., 2018), contrary to the assertions in Bilecenoglu et al. (2014), which are based on historical occurrence data of the species.
Isurus oxyrinchus Rafinesque, 1810
Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on I. oxyrinchus in Turkish waters
A huge female shortfin mako shark, Isurus oxyrinchus, was caught in the late 1950s off Marmaris (south-eastern Aegean Sea; Kabasakal & De Maddalena, 2011). Photographic documentation was used by the authors to estimate the total length of this specimen at 585 cm, which greatly exceeded the previous maximum size recorded for the species (445 cm). Although recent studies have confirmed the contemporary occurrence of I. oxyrinchus in Turkish Aegean and Mediterranean waters (Erguden et al., 2013; Kabasakal 2015b, 2017b; Kabasakal & Kabasakal, 2013; Tunger & Kabasakal,
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2016), this is a rare lamnoid shark in Turkish waters. Therefore, the seasonal occurrence of both young and adult shortfin mako sharks off Turkey's Aegean and Mediterranean coasts should be monitored to clarify whether the shortfin mako shark is a resident or a vagrant species along the aforementioned coastline. According to Kabasakal et al. (2017), I. oxyrinchus accounted for 5.3% of the total number of large sharks captured by commercial fishermen in the 1990-2015 period in Turkish waters. Occurrences of I. oxyrinchus newborns and youngs-of-the-year off Foga and in iskenderun Bay suggest the possibility of a mating region in the northern Aegean and north-eastern Mediterranean Seas (Ergüden et al., 2013; Kabasakal, 2015b).
Lamna nasus (Bonnaterre, 1788) Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on L. nasus in Turkish waters
Occurrence of the porbeagle shark, Lamna nasus, in Turkish waters was reported by Deveciyan (1926), Ak§iray (1987) and Kabasakal (2002b). Kabasakal and Kabasakal (2004) reported on a porbeagle shark, 250 cm TL, caught off Bozcaada (northern Aegean Sea), on 11 April 2004. L. nasus is a rare shark in Turkish waters and its questionable presence in Marmaric waters requires confirmation (Kabasakal & Karhan, 2015).
CARCHARHINIFORMES SCYLIORHINIDAE
Galeus melastomus Rafinesque, 1810 Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014). Scyliorhinus canicula (Linnaeus, 1758) Distribution in Turkish waters: Black, Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014). Scyliorhinus stellaris (Linnaeus, 1758) Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on G. melastomus, S. canicula and S. stellaris in Turkish waters
Contemporary occurrences of cat sharks (family Scyliorhinidae), Galeus melastomus, Scyliorhinus canicula and S. stellaris, in Turkish waters were confirmed by Ba§usta et al. (2016), Kabasakal (2002b), Kabasakal and Kabasakal (2004), Kabasakal and Karhan (2015), Keskin and Karakulak (2006), i§men et al. (2013), and Yaglioglu et al. (2015). S. canicula is the most abundant cartilaginous fish species caught in demersal fishery in Turkish waters (Cihangir et al., 1997; Kabasakal, 2002b; Keskin & Karakulak, 2006; i§men et al., 2013; Yaglioglu et al., 2015).
Investigations carried out since 1997 have revealed that, in Turkish waters, the main prey items of S. canicula are decapod crustaceans (Parapenaeus longirostris, Lio-
carcinus sp., Goneplax rhomboides, Xantho sp. and Munida sp.) and teleostean fish, while secondary food items comprise polychaetes (e.g., Sipinculida) and cephalo-pods (Cihangir et al., 1997; Kabasakal, 2001, 2002c; Filiz & Ta§kavak, 2006; Turker ^akir 2006). A previous study on the stomach contents and feeding ecologies of the S. canicula and thornback ray, Raja clavata, caught in the northern Aegean Sea, revealed a clear niche overlap between S. canicula (all sizes) and R. clavata (>50 cm TL), and competition for similar prey items (Kabasakal, 2001). In a broader perspective, in Turkish waters, G. melastomus preys mainly on crustaceans, teleosteans and cephalopods (Kabasakal, 2002c; Ozutemiz et al., 2009), while in the deep zones (>1000 m depth) of the Sea of Marmara, the blackmouth catshark feeds mainly on crustaceans, Calocaris macandreae and Sergestes robustus (Oral, 2010).
In a previous study on the distribution and determinate biological aspects of the lesser spotted dogfish in the north-eastern Aegean Sea, Cihangir et al. (1997) reported that the reproduction of S. canicula occurs year-round, with a relatively low rate of oogenesis in winter and early spring. Demersal trawl surveys carried out in the northern Aegean Sea showed that seasonal biomass of S. canicula in shallow waters (<100 m depth) varied from 576 to 2,958 tonnes (Cihangir et al., 1997). Filiz and Mater (2002) examined the length-weight relationships of seven elasmobranch species sampled from the north Aegean Sea, and calculated the length-weight equations for S. canicula, M. mustelus and S. acanthias as follows: WT= 0.0016TL x 3.1804 (r2 = 0.9795), WT= 0.0008TL x 3.3259 (r2 = 0.9745) and WT= 0.0031TL x 3.1056 (r2 = 0.9814), respectively. According to Turker-^akir et al. (2006), the weight increased allometrically in the both sexes of the S. canicula sampled in the northern Aegean Sea (b = 2.93). Sexual dimorphism, dentition and morphometry of the S. canicula caught in Turkish waters were studied by Erdogan et al. (2004) and Filiz and Ta§kavak (2006).
Growth parameters of G. melastomus were examined based on specimens captured in Sigacik Bay (Aegean Sea), and the mean size for the examined specimens was 14.01+1.96 cm (Ozutemiz et al., 2009). The length-weight relationship parameters of 16 out of the 30 cartilaginous fish species (11 sharks, 18 batoids and 1 chimaera) caught in the central Aegean Sea were examined; the values of the slope b in the length-weight relationship parameters ranged from 2.79 (Torpedo marmorata) to 3.78 (Scyliorhinus stellaris), a values from 0.0002 (Scyliorhinus stellaris) to 0.9713 (Dasyatis pastinaca) (Eronat and Ozaydin, 2014).
TRIAKIDAE
Galeorhinus galeus (Linnaeus, 1758)
Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Mustelus asterias Cloquet, 1821
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Distribution in Turkish waters: Black, Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014). Mustelus mustelus (Linnaeus, 1758) Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014). Mustelus punctulatus Risso, 1826 Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on G. galeus, M. asterias, M. mustelus and M. punctulatus in Turkish waters
Contemporary occurrences of triakid sharks (family Triakidae), Galeorhinus galeus, Mustelus asterias, M. mustelus and M. punctulatus, in Turkish waters have been confirmed by a number of studies (Filiz and Mater, 2002; Kabasakal, 2002b; Kabasakal & Kabasakal, 2004; Ba§usta et al., 1998, 2016; Yaglioglu et al., 2015). Two specimens of the starry smoothhound, M. asterias, were captured three miles off the coast of §ile (south-western Black Sea) on 19 November 2000 at a depth of ca. 90 m, and this previous record extended the Mediterranean distribution of M. asterias to the Black Sea (Eryilmaz et al., 2011). The tope shark, G. galeus, is one of the largest shark species occurring in Turkish waters, and the recent remarkable decrease in its populations is alarming. Between 1990 and 2015, G. galeus accounted for less than 2 percent of the total shark biomass recorded in the Turkish commercial fisheries (Kabasakal et al., 2017). The diet of M. mustelus is heterogeneous and generalized, and the main prey item found in the stomach contents is decapod crustaceans, with teleosteans and cephalopods featuring as secondary important food items (Kabasakal, 2002c; Filiz, 2009; Özcan & Ba§usta, 2016).
CARCHARHINIDAE Carcharhinus altimus (Springer, 1950) Distribution in Turkish waters: Mediterranean Sea (Bilecenoglu et al., 2014).
Carcharhinus brevipinna (Müller & Henle, 1839) Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Carcharhinus limbatus (Müller & Henle, 1839) Distribution in Turkish waters: Mediterranean Sea (Bilecenoglu et al., 2014).
Carcharhinus melanopterus (Quoy & Gaimard, 1824) Distribution in Turkish waters: Mediterranean Sea (Ak§iray, 1987; Kabasakal, 2011b).
Carcharhinus obscurus (Lesueur, 1818) Distribution in Turkish waters: Mediterranean Sea (Ak§iray, 1987; Kabasakal, 2011b).
Carcharhinus plumbeus (Nardo, 1827) Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014). Prionace glauca (Linnaeus, 1758) Distribution in Turkish waters: Marmara, Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on Carcharhinus species and P. glauca in Turkish waters
Despite historical and contemporary occurrences of carcharhinid sharks (family Carcharhinidae) in Turkish waters have been noted in general ichthyological or chondrichthyan inventories of the mentioned region (e.g., Ninni, 1923; Ak§iray, 1987; Ba§usta et al., 1998; Kabasakal, 2002b, 2003b; Kabasakal & Kabasakal, 2004; Kabasakal et al., 2017; Yaglioglu et al., 2015), the paucity of species specific studies is obvious. In a previous report on the status of the blue shark, Prionace glauca, in the northern Aegean Sea, Kabasakal (2010b) emphasized that coastal trammel- and gill-netting is a serious threat to the survival of the young populations of the species in Edre-mit Bay. In an extensive survey on the chondrichthyan fish of iskenderun Bay (north-eastern Mediterranean Sea), Ba§usta et al. (1998) recorded the bignose shark, Carcharhinus altimus, for the first time in Turkish waters and confirmed the contemporary presence of the sandbar shark, C. plumbeus, as well. Underwater observations carried out in Boncuk Bay (south-eastern Aegean Sea) and the knowledge gathered from these surveys played a critical role in declaring C. plumbeus a protected species in Turkish seas (Akga, 2010; Ozturk, 2006). Recent surveys have confirmed the occurrence of the dusky shark, C. obscurus, in the Bay of iskenderun (Kabasakal et al., 2017). The spinner shark, C. brevipinna, is considered a rare shark and has only been listed in the general ichthyological and chondrichthyan inventories of Turkish waters (Ak§iray, 1987; Kabasakal, 2002b); recently, Filiz and Kabasakal (2015) reported on a specimen of this species photographed in the Bay of Gokova. The recently discovered photographic evidence suggests that Carcharhinus spp. were present in the Sea of Marmara in the 1950s (Kabasakal, 2015c), and this evidence also extends the known historical distributional range of Carcharhinus spp. into Marmaric waters, a northern extension of the Mediterranean Basin.
In a pioneering study in which the length-weight relationship (LWR) of the sandbar shark, C. plumbeus, from the northeastern Mediterranean Sea population was examined for the first time, the LWR estimated for combined sexes, females and males, were W= 0.01*TL (r=0.915, SE =0.174), W= 0.0034*TL (r =0.912, SE =0.278) and W= 0.0039*TL (r =0.915, SE =0.231), respectively (Ba§usta, 2016). According to Ba§usta (2016), the type of allometric growth in the examined population of C. plumbeus was negative (b < 3) for all sexes and for males, and positive (b > 3) for females. Seeing that Boncuk Bay (south-eastern Aegean Sea) is of critical importance for the reproduction of C. plumbeus, Ozturk (2006) suggested that the bay should be declared a protected area and all fishery should be banned in its waters. Underwater observations to record the bioecological characteristics of the sandbar shark, C. plumbeus, were also carried out in Boncuk Bay (south-eastern Aegean Sea) during a 39-day expedition
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in 2009 (Akga, 2010). A study has also been carried out which confirmed the year-round aggregations of sandbar sharks in the area and provided new and solid evidence for banning all fishing activities in this marine protected area (Filiz, 2018).
SPHYRNIDAE
Sphyrna (Sphyrna) zygaena (Linnaeus, 1758)
Distribution in Turkish waters: Aegean and Mediterranean Seas (Bilecenoglu et al., 2014).
Review of studies on S. zygaena in Turkish waters
Our knowledge on hammerhead sharks (family Sphyrnidae) in Turkish waters consists of rudimentary data. Uluturk (1987) and Kabasakal and Kabasakal (2004) reported rare occurrences of the smooth hammerhead shark, Sphyrna zygaena, off Gokgeada coasts (northern Aegean Sea), and the species was observed off the Ka§ Peninsula (western Levantine Basin) in August 2015 (Kabasakal et al., 2017). Although its occurrence was confirmed, S. zygaena is a rare shark in Turkish waters (Kabasakal et al., 2017).
Review of general studies on chondrichthyan fish in Turkish waters
In an extensive survey of the chondrichthyan fish of iskenderun Bay, the bignose shark, C. altimus, was recorded for the first time in Turkish waters and the presence of C. plumbeus, O. centrina and S. oculata in the bay waters were confirmed as well (Ba§usta et al., 1998). Based on the results of field surveys and a review of available data, Kabasakal (2002b) reported on the presence of 39 shark species in Turkish waters, defining the occurrence of 8 of them questionable and requiring confirmation. The results of an extensive trawl survey carried out in the northern Aegean Sea determined S. canicula as the most abundant cartilaginous fish species, with a total mass estimated at 2,850.6 kg/nm2 (Keskin & Karakulak, 2006). Between March 2005 and June 2008, in Saros Bay, Turkey, ten shark species were sampled from depths ranging from 5 to 500 m for length-weight relationship using a commercial trawl vessel. The values of the exponent b of the length-weight relationships ranged from 2.6816 to 3.6060 (i§men et al., 2009). In rare occasions, selected measurements of lamniform sharks (C. maximus, A. superciliosus, A. vulpinus, C. carcharias and I. oxyrin-chus) were also reported by Kabasakal (2002a, 2017b), Kabasakal and Gedikoglu (2008), Kabasakal and Karhan (2008), Kabasakal and Kabasakal (2013), Erguden et al. (2013, 2015) and Tunger and Kabasakal (2016).
Between October 2011 and February 2013, the composition of by-catch in the beam trawls used in the pink shrimp (Parapenaeus longirostris) fishery was surveyed seasonally and S. canicula, S. stellaris, S. acanthias and O. centrina were recorded (i§men et al., 2013). Between 2009 and 2010, the total biomass, species composition, depth distribution, seasonal distribution and abundance
of elasmobranchs caught by commercial bottom-trawlers in iskenderun Bay (north-eastern Levantine Sea) were also examined (Yaglioglu et al., 2015). In this study, M. mustelus, S. canicula, S. stellaris, G. melastomus and S. squatina represented between 0.45% and 1.7% of the total biomass of the examined cartilaginous fish. Single or sporadic captures were also recorded for I. oxyrinchus, C. altimus, C. plumbeus and O. centrina (Yaglioglu et al., 2015). In a recent review on cartilaginous fish and fisheries along the Mediterranean coast of Turkey, Ba§usta et al. (2016) recorded 32 species from 16 families, and concluded that the landings of elasmobranchs were reduced from 3,980 tonnes in 2000 to 246.2 tonnes in 2015. The production and economic values of sharks and their relatives in Turkey have been analysed for the last 34 years, and according to Dogan (2006), the maximum catch level was recorded in 1979 (11,125 t), followed by a significant decrease after 1989 and reaching the minimum level of 400 t in 2003. The current status of sharks and shark fisheries in the waters of the Sea of Marmara has been of late extensively reviewed (Kabasakal, 2016b; Yigin et al., 2016). Last but not least, in a recent survey of shark attacks against humans and boats, 13 shark attacks were recorded in Turkey's waters between 1931 and 1983, 2 of which fatal (Kabasakal & Gedikoglu, 2015).
CONCLUSIONS
Until the last quarter of the 20th century, most of our knowledge on the sharks of the Turkish waters was based on elasmobranch-specific chapters in general ich-thyological inventory studies and on a limited number of anecdotal studies. Since the mid-1990s, however, there has been a remarkable rise in the number and quality of shark-specific studies and publications, resulting in a gradual filling of the gaps in our understanding of the sharks of the Turkish waters. The reference list of the present article also serves as a bibliographical archive of the shark- and elasmobranch-specific studies related to Turkish waters that were published between 1968 and 2018. The next step in shark- and elasmobranch-spe-cific studies should involve designing a master plan for the management of sharks and their relatives in Turkish waters, and implementing the conservatory acts that would be based on the available data.
Currently, 36 species of sharks with confirmed occurrence are present in Turkish waters (Ak§iray, 1987; Kabasakal, 2011b; Bilecenoglu et al., 2014; Kabasakal et al., 2017): Hexanchus griseus, Heptranchias perlo, Echinorhinus brucus, Squalus acanthias, S. blainvillei, Centrophorus granulosus, C. uyato, Etmopterus spinax, Oxynotus centrina, Dalatias licha, Squatina aculeata, S. oculata, S. squatina, Carcharias taurus, Odontaspis ferox, Alopias superciliosus, A. vulpinus, Cetorhinus maximus, Carcharodon carcharias, Isurus oxyrinchus, Lamna nasus, Galeus melastomus, Scyliorhinus canicula, S. stellaris, Galeorhinus galeus, Mustelus asterias,
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M. mustelus, M. punctulatus, Carcharhinus altimus, C. brevipinna, C. limbatus, C. melanopterus, C. obscurus, C. plumbeus, Prionace glauca, and Sphyrna zygaena. There are also species of questionable occurrence, which are included in one of the noteworthy ichthyological inventories of Turkish waters (Ak§iray, 1987), but require confirmation, namely: C. longimanus, S. lewini, S. tudes and Somniosus rostratus.
The continuous rise in the number of articles and chapters on the sharks of the Turkish waters published annually is promising. The seasonal occurrence of neonate and young-of-the-year specimens of several shark species in Turkish waters, as well as the presence of documented breeding and nursery grounds in the region form a solid basis for the implementation of seasonal restrictions of commercial fisheries in these grounds. Based on the by-catch records of neonates and juvenile specimens of some rare sharks, such as D. licha and O. centrina, or some large sharks, for example, H. grise-us, C. carcharias, I. oxyrinchus and C. plumbeus, it is possible to speculate that sharks, at least the mentioned species, could reproduce in Turkish waters throughout the vast coastal zone spreading from the north Aegean Sea to the eastern Levant. In light of available and confirmed data, there are three possible breeding grounds; (1) in the northern Aegean Sea, between Gokgeada and Foga, (2) in Boncuk Bay in the southern Aegean Sea, and (3) in the Bay of iskenderun, eastern Levant (Fig. 1). To allow the survival of shark species, these areas should be declared seasonally protected or at least restricted zones for commercial fisheries. Currently, Boncuk Bay is the only protected area.
Different geographical populations of the same shark species can exhibit different growth parameters, which
should be taken into account in their management. For instance, available data on the parameters of the Aegean Sea and Black Sea populations of S. acanthias present a clear difference in length at 50% maturity (Demirhan & Seyhan, 2007; Yigin & i§men, 2013) - a critical detail that should not be overlooked in the regional management of S. acanthias in Turkish waters.
Populations of many large shark species in Turkish waters have drastically declined; a recent review of the distribution of large sharks captured mostly by commercial fishermen in the 1990-2015 period in Turkish waters showed that large sharks accounted for less than 2 percent of the total captured biomass (Kabasakal et al., 2017). According to Kabasakal et al. (2017), large sharks in Turkish waters are threatened by multi-parameter fishing pressure of demersal and pelagic fisheries of artisanal to industrial scale that operate in coastal to open waters and in shallow to deep fishing grounds almost year-round. Last but not least, fishing-gear induced injuries and harsh handling are overlooked contributors to the cryptic mortality of sharks in Turkish waters. Hopefully, future studies by new generations of researchers will provide new data on several aspects of the sharks of the Turkish waters, which can deepen our understanding of them and fill in the blanks in their life stories.
ACKNOWLEDGMENTS
The author wishes to thank his colleagues, who shared their experiences and researches on sharks of Turkish waters, and two anonymous referees for their valuable comments, improving the content of the article. Author is grateful to his wife, Ozgür, and to his son, Derin, for their endless love and patience.
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PREGLED RAZISKAV O MORSKIH PSIH V TURŠKIH VODAH
Hakan KABASAKAL
Ichthyological Research Society, Tantavi mahallesi, Mente§oglu caddesi, Idil apt., No: 30, D: 4, Ümraniye, 34764 Istanbul, Turkey
e-mail: kabasakal.hakan@gmail.com
POVZETEK
Do zadnje četrtine 20. stoletja je bilo poznavanje o morskih psih v turških vodah omejeno na poglavja v specifičnih monografijah o morskih psih v splošnih ihtioloških pregledih in manjšem številu anekdotičnih raziskav. Od srede devetdesetih let pa je prišlo do občutnega povečanja v številu in kvaliteti specifičnih raziskav in publikacij o morskih psih, ki je počasi mašilo vrzel o poznavanju morskih psov v turških vodah. Pred letom 1990 sta bila objavljena le dva specifična prispevka o morskih psih, 8 prispevkov med leti 1990 in 2000 ter 88 prispevkov po letu 2000. Skupno je bilo objavljeno 96 prispevkov o morskih psih v turških vodah med leti 1968 in 2018. Smiselno je upati, da bodo nove generacije raziskovalcev odkrile nove podatke o morskih psih iz turških morij iz vseh vidikov, kar bo poglobilo in izpopolnilo znanje o njih in njihovem življenju.
Ključne besede: raziskave morskih psov, objave, turške vode, vzhodno Sredozemlje
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Kutaygil, N. & N. Bilecik (1977): Recherches sur le Squalus acanthias L. du littoral Anatolien de la Mer Noire. Rapp. Comm. int. Mer Médit., 24, 80-83.
Mater, S. (2005): Denizlerimizde yeni bir kopekbaligi, Alopias superciliosus (Lowe, 1841). Aquaculture, 1, 10.
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Ninni, E. (1923): Primo contributo allo studio dei pesci e della pesca nelle acque dell'Impero Ottomano. Venezia: Premiate Officine Grafiche Carlo Ferrari.
Oral, M. (2010): A preliminary study on feeding habits of black-mouth catshark Galeus melastomus, Rafinesque, 1810 sampled from the Sea of Marmara. Marmara Denizi 2010 Sempozyumu, 25-26 Eylul 2010, istanbul, pp. 312-316.
Ozcan, E.l. & N. Basusta (2016): Digestive system contents of the Mustelus mustelus (Linnaeus, 1758) inhabiting northeastern Mediterranean. Firat Unv. Journal of Science, 28, 7-12.
Ozturk, B. (2006): Save the sandbar sharks of Bon-cuk Bay, Turkey. In: Ba§usta, N., Keskin, Serena, F., Seret, B. (Eds.), 2006. "The Proceedings of the Workshop on Mediterranean Cartilaginous Fish with Emphasis on Southern and Eastern Mediterranean" Turkish Marine Research Foundation. Istanbul- TURKEY. Publication Number 23, pp. 42-47.
Ozutemiz §., M. Kaya & O. Ozaydin (2009): Growth and feeding characteristics of two shark species [Galeus melastomus Rafinesque, 1810 and Squalus blainvillei (Risso, 1826)] from Sigacik Bay (Aegean Sea). E. U. Journal of Fisheries & Aquatic Sciences, 26, 211-217.
Serena F. (2005): Field identification guide to the sharks and rays of the Mediterranean and Black Sea. FAO Species Identification Guide for Fishery Purposes. Rome, FAO. 97 pp.
Tun?er, S. & H. Kabasakal (2016): Capture of a juvenile shortfin mako shark, Isurus oxyrinchus Rafinesque, 1810 (Chondrichthyes: Lamnidae) in the Bay of Edremit, northern Aegean Sea (Turkey). Annales ser. hist. nat., 26, 31-36.
Turker ^akir, D., H. Torcu Ko? & Z. Erdogan (2006):
Some biological aspects of the lesser spotted dogfish Scyliorhinus canicula (Linnaeus, 1758) in Edremit Bay (the northern Aegean Sea) Turkey. In: Ba§usta, N., Keskin,
Serena, F., Seret, B. (Eds.), 2006. "The Proceedings of the Workshop on Mediterranean Cartilaginous Fish with Emphasis on Southern and Eastern Mediterranean" Turkish Marine Research Foundation. Istanbul- TURKEY. Publication Number 23, pp. 17-27.
Uluturk T. (1987): Fish fauna, background radioactivity of the Gokgeada marine environment. Journal of Aquatic Products, University of Istanbul, 1, 95-119.
White W.T., D.A. Ebert, G.J.P. Naylor, H-C. Ho, P. Clerkin, A. Verissimo & Cotton C.F. (2013): Revision of the genus Centrophorus (Squaliformes: Centrophoridae) Part 1 - Redescription of Centrophorus granulosus (Blo-ch & Schneider), a senior synonym of C. acus Garman and C. niaukang Teng. Zootaxa, 3752, 035-072.
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Hakan KABASAKAL: A REVIEW OF SHARK RESEARCH IN TURKISH WATERS, 1-16
Yaglioglu, D., T. Deniz, M. Gurlek, D. Erguden & C. Turan (2015): Elasmobranch bycatch in a bottom trawl fishery in the Iskenderun Bay, northeastern Mediterranean. Cah. Biol. Mar., 56, 237-243.
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Yigin, C. A. l§men & U. Onal (2016): Occurrence of a rare shark, Oxynotus centrina (Chondrichthyes: Oxynotidae), from Saros Bay, North Aegean Sea, Turkey. J. Black Sea / Mediterranean Environment, 22, 103-109.
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received: 2019-03-08	DOI 10.19233/ASHN.2019.02
FINALLY UNDER PROTECTION! STATUS OF THE ANGEL SHARK, SQUATINA SQUATINA (LINNAEUS, 1758) IN TURKISH SEAS, WITH NOTES ON A RECENT SIGHTING AND INCIDENTAL CAPTURES
Hakan KABASAKAL
Ichthyological Research Society, Tantavi mahallesi, Mente§oglu caddesi, Idil apt., No: 30, D: 4, Umraniye, 34764 Istanbul, Turkey
e-mail: kabasakal.hakan@gmail.com
ABSTRACT
Nine angel sharks, Squatina squatina, were recorded in different regions of Turkish waters between 21 March 2009 and February 2019. Eight specimens were captured by different means of bottom fishing gear (e.g., gill or trammel net, or longline) or harpoon, and 1 specimen was sighted alive. Considering the fishery statistics of angel sharks in the last 10 years and biomass and numerical abundance data on the species in Turkish waters as baseline data, an alarming reduction in the populations of S. squatina in the mentioned regions has been observed. An extensive study providing baseline information on the current spatial distribution patterns, habitat use, abundance and population structure of S. squatina in Turkish waters is an urgent necessity.
Key words: Angelshark, Squatina, protection, baseline shift, rarity, eastern Mediterranean
FINALMENTE PROTETTO! STATO DELLO SQUALO ANGELO, SQUATINA SQUATINA (LINNAEUS, 1758) IN MARE TURCO, CON NOTE SU AVVISTAMENTI RECENTI E
CATTURE ACCIDENTALI
SINTESI
Nove squali angelo, Squatina squatina, sono stati registrati in diverse regioni delle acque turche tra il 21 marzo 2009 e il febbraio 2019. Otto esemplari sono stati catturati con diversi attrezzi da pesca a fondo o con l'arpione, mentre un esemplare è stato avvistato vivo. Considerando le statistiche sulla pesca degli squali angelo negli ultimi 10 anni e i dati di biomassa e abbondanza numerica delle specie presenti nelle acque turche come dati di riferimento, è stata osservata una riduzione allarmante delle popolazioni di S. squatina nelle regioni considerate. Uno studio approfondito che fornisca informazioni di base sugli attuali modelli di distribuzione spaziale, sull'uso dell'habitat, e sull'abbondanza e la struttura demografica di S. squatina nelle acque turche è una necessità urgente.
Parole chiave: squalo angelo, Squatina, protezione, deviazione dal riferimento, rarità, Mediterraneo orientale
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Hakan KABASAKAL: FINALLY UNDER PROTECTION! STATUS OF THE ANGEL SHARK, SQUATINA SQUATINA (LINNAEUS, 1758) IN TURKISH SEAS, WITH ..., 17-24
INTRODUCTION
In natural systems, rarity of a species is a common phenomenon and most often defined by two attributes: the species' distribution and its abundance (Flather & Sieg, 2007). According to Flather and Sieg (2007), a species is considered rare if its area of occupancy or its number is small when compared to the other species that are taxonomically or ecologically comparable. The angel shark, Squatina squatina (Linnaeus, 1758), used to be reported as abundant in the entire Mediterranean Sea (Serena, 2005). Nowadays, it is supposed to be absent or even extirpated from several areas in the region (Bradai et al., 2012).
Due to the low overall number of records or a complete absence of the species in scientific trawl surveys conducted since 1958 (Holcer & Lazar, 2017), S. squatina is today considered a rare shark species throughout the Mediterranean Sea and its rarity has been emphasized by several researchers from different parts of the region (e.g., Golani, 2006; Serena & Relini, 2006; Kabasakal & Kabasakal, 2014; Akyol et al., 2015; Cavallaro et al., 2015).
Although the occurrence of S. squatina in Turkish waters has been noted in historical inventory studies of Turkish marine fishes (e.g., Ninni, 1923; Deveci-yan, 1926; Ak§iray, 1987), all of which attributed an economic value to the species and mentioned mass captures, current statistics indicate a drastic decline in
annual landings of incidentally captured angel sharks in Turkish waters (TUIK, 2017). As in many parts of the Mediterranean, populations of S. squatina have been severely depleted in Turkish waters as well, which calls for the protection of the species.
The present article provides a summary of the captures and of the single sighting of S. squatina in Turkish waters in the last 10 years, and discusses the causes of the species' depletion. These events have eventually resulted in the implementation of effective protective measures for the species in the mentioned region.
MATERIAL AND METHODS
Data on captures and a single sighting of S. squatina in Turkish waters were obtained from the following sources: (1) scientific literature; (2) preserved samples in public or private collections; (3) newspaper accounts or internet news reporting on the capture of angel sharks in the studied area and (4) visits to fishing ports. As far as popular sources are concerned, the validity of the records was confirmed through direct contact with the fishermen cited by the sources, or else, based on a reliable photograph of the specimen accompanying such news. The following data were recorded for the examined specimens of angel shark: date, depth and locality of capture, total length (TL), weight (W), sex and fishing gear.
Commercial landings data on angel sharks from 2008 to 2017 were used to indicate the trend of annual
Fig. 1: Maps showing the approximate locations of recent captures and the single sighting of S. squatina, in Turkish waters. The numbers correspond to those in Table 1.
Sl. 1: Zemljevidi o recentnih ulovih in opazovanjih navadnega sklata v turških vodah. Številke ustrezajo tistim v Tabeli 1.
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Hakan KABASAKAL: FINALLY UNDER PROTECTION! STATUS OF THE ANGEL SHARK, SQUATINA SQUATINA (LINNAEUS, 1758) IN TURKISH SEAS, WITH ..., 17-24
Tab. 1: Old and recent captures or sightings of the angel shark, Squatina squatina, in Turkish waters since 2009. The numbers in the "No." column are same as those in Fig. 1 indicating the approximate localities of capture. Tab. 1: Stari in novejši zapisi o opazovanju navadnih sklatov, Squatina squatina, v turških vodah od leta 2009. Številke v stolpcih so enake kot v Sliki 1 in ponazarjajo približno lokaliteto ulova.
No	Date	Locality	Depth (m)	Sex	TL (cm)	W (kg)	Remarks
1	21 March 2009	Bodrum	-	9	160	ca. 60	Entangled in coastal stationary-nets
2	October 2013	^anakkale	1.5	-	ca. 100	-	Harpooned by a freediver in shallow water
3	4 January 2014	Mudanya	ca. 50	9	174	35	Entangled in a trammel-net, after the auction it was sold (Kabasakal & Kabasakal, 2014)
4	5 February 2015	Gokova Bay	20	9	156	32.6	Entangled in a trammel-net; it was a pregnant female carrying at least four developping embryos, which were expelled during the handling (Akyol et al., 2015)
5	5 March 2015	Gokova Bay	-	9	160	-	Found dead while entangled in a stationary-net (unpublished data)
6	December 2015	Dardanelles Strait	ca. 30	9	ca. 150	-	Sighted by Mr. Mert Gokalp during a SCUBA diving expedition in the vicinity of the northern entrance of the Dardanelles Strait (unpublished data) (Fig. 2)
7	21 March 2018	§arkoy	ca. 40	d	114	-	Captured by long-lining set for sea breams (Sparidae), displayed in Be§ikta§ fishmarket in istanbul (unpuplished data) (Fig. 3).
8	3 April 2018	Dardanelles Strait	ca. 30	d	90	-	Captured by stationary-netting, displayed in Be§ikta§ fishmarket in istanbul (unpublished data) (Fig. 4).
9	February 2019	Bosphorus Strait	20 m	9	ca. 140	30	Captured by gill-netting around the southern entrance of the Bosphorus Strait, transported to Edirne city and sold (unpublished data)
catches of Squatina species in Turkish waters (TUIK, 2017). To date, three species of angel shark, S. aculeata Dumeril, in Cuvier, 1817, S. oculata Bonaparte, 1840 and S. squatina have been recorded in Turkish waters (Bilecenoglu et al., 2014). Since no species-specific discrimination of angel shark catches is reported in TUIK statistics, the annual landings data represent the combined data on the landings of three congeneric angel sharks in Turkish waters. Raw data and individual records of angel sharks are kept in the archive of the Ichthyological Research Society.
RESULTS AND DISCUSSION
Nine angel sharks, S. squatina, were recorded in several regions of Turkish waters between 21 March 2009 and February 2019 (Tab. 1; Fig. 1). Eight specimens were
captured by different means of bottom fishing gear (e.g., gill or trammel net, or longline) or harpoon, and 1 specimen was sighted alive (see Tab. 1 for specimen-specific details). Six specimens were females, 2 were males and the sex of 1 angel shark was unknown. The total length of the specimens varied from 90 to 174 cm. Five angel sharks were captured in Aegean waters, three in the Sea of Marmara and 1 specimen was sighted in the southeastern part of the region near the northern entrance to the Dardanelles Strait (Fig. 1). The angel sharks were recorded in very shallow (specimen no. 2 at a depth of 1.5 m) to quite deep waters (specimen no. 3 at a depth of ca. 50 m) of the coastal zone (Tab. 1).
Based on the information obtained from available literature, the occurrence of the angel shark, S. squatina, in Turkish waters dates back to the early 20th century, when Deveciyan (1926) reported on angel sharks landed
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Fig. 2: A live specimen of S. squatina (specimen no. 6 in Table 1) sighted in the Dardanelles Strait at a depth of 30 m (Photo: Mert Gokalp).
Sl. 2: Opaženi primerek navadnega sklata (primerek št. 6 v Tabeli 1), opažen v prelivu Dardanel na globini 30 m (Foto: Mert Gokalp).
at the istanbul fish market. According to his report (De-veciyan, 1926), angel shark was a regularly captured, landed and consumed shark species; however, the author did not provide any specific information, such as annual catch data, etc., on the species. Kabasakal
(2002)	reported captures of 51 angel sharks in total off the coast of Turkey between 1995 and 1999. Kabasakal
(2003)	reported the capture of a female angel shark of 87 cm TL in the southern Sea of Marmara, in November 1995. According to Kabasakal and Kabasakal (2004), 5 males in total were captured off the coast of Gokgeada in the northeastern Aegean Sea in October 1996 (3 specimens) and July 1997 (2 specimens), all by means of bottom fishing gear. In the 1950s, S. squatina was a popular gamefish among spearfishermen in the Sea of Marmara (Kabasakal & Kabasakal, 2014).
According to Deveciyan (1926), Ak§iray (1987) and Kocata§ et al. (1993), S. squatina is a valuable commercial species of shark in Turkish marine fishery. Deveciyan (1926) and Ak§iray (1987) in particular pointed out the significant landings and high economical value of angel sharks captured in Turkish waters in the 20th century. However, like many other shark species, populations of S. squatina in Turkish waters have drastically declined and the rarity or the absence of angel shark from the general ichthyological inventory or shark specific studies provides alarming evidence that the survival of the species is threatened. In two recent surveys on the composition of bycatch in pink-shrimp (Parapenaeus longirostris) beam trawl fishery in southern and northern Sea of Marmara, Bayhan et al. (2006) and Bok et al. (2011) reported the absence of S. squatina from both marine regions. Karakulak et al. (2000) also reported the absence of S. squatina in surveys on demersal fish populations of the northern Sea of Marmara. Keskin and Eryilmaz (2010) reviewed the demersal fish populations
Fig. 3: A S. squatina incidentally captured off §arköy coast (southwestern Sea of Marmara; specimen no. 7 in Tab. 1), on display at the fishmonger's (Photo: Hakan Kabasakal).
Sl. 3: Naključno ujeti primerek navadnega sklata ob obali §arköy (jugozahodno Marmarsko morje; primerek št. 7 v Tabeli 1), razkazan na ribji tržnici (Foto: Hakan Kabasakal).
of the Sea of Marmara and found S. squatina to be rare in the mentioned region, which was further corroborated by Kabasakal (2016).
The rarity of S. squatina in Turkish waters was also emphasised by Kabasakal and Kabasakal (2014) and Akyol et al. (2015). According to Ba§usta et al. (2016), the paucity of publications on S. squatina (less than 5) is conspicuous among the studies on cartilaginous fishes occurring in Turkish Mediterranean waters. Recently, Filiz et al. (2018) estimated the biomass and numerical
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Fig. 4: A S. squatina incidentally captured in Dardanelles Strait (specimen no. 8 in Tab. 1), on display at the fishmonger's (Photo: Hakan Kabasakal). Sl. 4: Navadni sklat naključno ujet v prelivu Dardanel (primerek št. 8 v Tabeli 1), razkazan na ribji tržnici (Foto: Hakan Kabasakal).
abundance of S. squatina at 13 kg/km2 and 5 individuals/km2 based on the bycatch composition of bottom trawl fishery in southern Aegean Sea. Since no species-specific discrimination of angel shark catches is reported in TUIK statistics, the annual landings data represent the combined data on the landings of three congeneric angel sharks, S. aculeata, S. oculata and S. squatina, captured in Turkish waters. A dramatic decline in the annual landings of Squatina species is clear from the fishery statistics for the 2008-2017 period (TUIK, 2017; Fig. 5). While in 2008 the annual landings of Squatina species by commercial fishermen amounted to 34 tons,
200a 2009 IOI □ 2011 2012 ."o 1 :c:f 2015 201 e 2017 Year
Fig. 5: Annual landings of Squatina species by Turkish fishermen in the 2008-2017 period. The graph based on the annual landings data of Squatina species is extracted from fisheries statistics (TUIK, 2017). Sl. 5: Letni ulov različnih vrst iz rodu Squatina, ki so jih ujeli turški ribiči v obdobju 2008-2017. Graf temelji na letnih ulovih sklatov, pridobljenih iz statističnih ribiških podatkih (TUIK, 2017).
in 2017 they came nearly 1 ton (Fig. 5). Although the landings rose to 17 tons in 2013, the declining trend in the annual landings during the 2008-2017 period did not change (Fig. 5).
The first records of S. squatina in Turkish waters date back to the early 20th century (Ninni, 1923; Deveciyan, 1926). The occurrence of S. squatina in Turkish waters was also reported in later studies (e.g., Roux, 1984; Ak§iray, 1987). Both in the earliest and later studies, S. squatina was reported as an abundant shark population sustaining a fishery based on it (Deveciyan, 1926; Ak§iray, 1987). Furthermore, the maximum total lengths reported for the species ranged between 200 cm (Ak§iray, 1987) and 250 cm (Roux, 1984). Unfortunately, there are no studies reporting about the population dynamics and abundance of S. squatina in Turkish waters during the last century, however, recent data show drastic declines in terms of biomass, numerical abundance and annual landings (TUIK, 2017; Filiz et al., 2018; Fig. 5). Also, the maximum total length of angel sharks captured in recent years (174 cm TL in the present study; specimen no: 3, Tab. 1) is remarkably below the historically reported sizes (200 to 250 cm TL).
Based on the limited historical and contemporary data on biomass, numerical abundance, annual landings and maximum total length of the S. squatina observed in Turkish waters, the 'shifting baseline syndrome' outlined by Pauly (1995) is dramatically present among young generations of fishermen, a common phenomenon that was also highlighted by Holcer and Lazar (2017) for the angel sharks from the Adriatic Sea. Due to the absence of baseline data indicating the status of S. squatina in Turkish waters during the last century, we cannot carry
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out a reasonable comparison between the historical and contemporary statuses of the species. However, based on available data it is possible to speculate that the abundance of S. squatina in demersal catch composition significantly declined over time, with the maximum total length of the species decreasing (Deveciyan, 1926; Roux, 1984; Ak§iray, 1987; TUIK, 2017; Filiz et al., 2018). According to Meyers et al. (2017), in regions where baseline information on the current spatial distribution patterns, habitat use, abundance and population structure of the angel shark is lacking, urgent conservation policies should be implemented. Therefore, the inclusion of S. squatina, as well as the congeneric angel sharks, S. aculeata and S. oculata, in the list of marine protected species, which was declared in the Official Gazzette in 2018 (Resmi Gazete, 2018), was a correct decision with respect to the status of angel shark in Turkish seas, where the baseline data of squatinid sharks is inadequate.
Except for the single live sighting, the angel sharks examined in the present study were incidentally captured specimens (Tab. 1); however, bycatch pressure on this rare shark by untargeted fisheries can also become a serious threat to its future survival. In an extensive study on the reproductive biology of S. squatina in the Mediterranean Sea, Capape et al. (1990) reported that males and females mature between the total lengths of 80-132 cm and 128-169 cm, respectively. According to Capape et al. (1990), males and females of over 80 cm and 128 cm in TL, respectively, can be considered as reproducing adult angel sharks. Recently, a pregnant female angel shark of 156 cm TL got entangled in a trammel net in Gokova Bay (southern Aegean Sea) and expelled its developing embryos during handling (Akyol et al., 2015). Based on the sizes of the reproducing adults of angel sharks reported by Capape et al. (1990) and Akyol et al. (2015), it can be concluded that all of the specimens examined in the present study were mature males and females (Tab. 1). Incidental captures of reproducing adults create another threat to the survival of S. squatina. Fishing-gear induced injuries, keeping sharks on the deck in rough conditions and subjecting them to harsh handling before releasing them into the sea negatively impact the post-release survival rate of specimens (see Kabasakal, 2010 for relevant references), and cannot be ruled out as causes of mortality in the incidentally captured specimens of S. squatina in the present study.
CONCLUSIONS
Although the protective legislation concerning angel sharks applies to all 3 species, S. aculeata, S. oculata and
S. squatina (Resmi Gazete, 2018), it is still very early to observe any positive results of the recent enactment of this legal protection on the angel shark populations occurring in Turkish waters. Since a "shifting baseline" effect is possibly present among younger fishermen, as reported by Holcer & Lazar (2017), the latter can lack incentive to act upon catching angel sharks, not recognising that as important. Due to life history parameters of S. squatina, such as low fecundity, long reproductive cycle (2 year) and the large size at which females reach sexual maturity (128 cm, which equals 51.2% of the reported maximum total length, 250 cm) (Roux, 1984; Capape et al., 1990), the species is considered as highly vulnerable to targeted and untargeted fisheries alike. Taking the fishery statistics of Squatina species during the last 10 years (TUIK, 2017) and the biomass and numerical abundance data on the species in Turkish waters (Filiz et al., 2018) as baseline data, we should point out an alarming reduction in the populations of S. squatina in the mentioned region. An extensive study providing baseline information on the current spatial distribution patterns, habitat use, abundance and population structure of S. squatina in Turkish waters is therefore an urgent necessity. Given the Red List status of S. squatina (critically endangered; Cavanagh & Gibson, 2007) and its rarity (Golani, 2006; Serena & Relini, 2006; Kabasakal & Kabasakal, 2014; Akyol et al., 2015; Cavallaro et al., 2015), the proposed study should employ non-invasive methods, such as capture and release of live specimens after satellite tagging and underwater imaging, perhaps with the contribution of citizen scientist divers. Last but not least, although S. aculeata, S. oculata and S. squatina are currently under full protection in Turkish seas (Resmi Gazete, 2018), it would be reasonable to expect cryptic mortality of the released angel sharks due to fishing-gear induced injuries and harsh handling before release. To prevent this and insure the safety of both fishermen and captured sharks, training of fishermen on which species of sharks are endangered and under protection and how these species should be kept alive on deck and handled before release, is critical.
ACKNOWLEDGMENTS
The author wishes to thank his colleagues who share their information on angel sharks, and two anonymous referees for their valuable comments improving the content of the article. Very special thank goes to Mr. Mert Gokalp, an Istanbul based underwater videographer and photographer, for sharing the photo of the angelshark (specimens No. 6 in Tab. 1). Author is grateful to his wife, Ozgur, and to his son, Derin, for their endless love and patience.
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KONČNO ZAVAROVAN! STATUS NAVADNEGA SKLATA, SQUATINA SQUATINA (LINNAEUS, 1758) V TURŠKIH MORJIH S POSEBNIM POUDARKOM NA NOVEJŠA
OPAZOVANJA IN NAKLJUČNE ULOVE
Hakan KABASAKAL
Ichthyological Research Society, Tantavi mahallesi, Mente§oglu caddesi, Idil apt., No: 30, D: 4, Umraniye, 34764 Istanbul, Turkey
e-mail: kabasakal.hakan@gmail.com
POVZETEK
Devet navadnih sklatov, Squatina squatina, je bilo popisanih v različnih predelih turških voda med 21. marcem 2009 in februarjem 2019. Osem primerkov je bilo ujetih z različnimi ribiškimi orodji (npr. zabodne in trislojne mreže, ribolov s parangali) ali harpuno, en primerek pa je bil opažen. Upoštevaje ribiško statistiko v zvezi s sklati v zadnjih desetih letih in podatke o abundanci in biomasi o vrsti v turških morjih kot temeljne podatke, je razviden veliki upad populacij sklatov v omenjenih okoljih. Zato je potrebno čimprej pripraviti obsežno raziskavo o vzorcih prostorske razširjenosti, izbiri habitata, abundanci in populacijski strukturi navadnega sklata v turških morjih.
Ključne besede: sklat, Squatina, varovanje, bazični odmik, redkost, vzhodno Sredozemlje
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Hakan KABASAKAL: FINALLY UNDER PROTECTION! STATUS OF THE ANGEL SHARK, SQUATINA SQUATINA (LINNAEUS, 1758) IN TURKISH SEAS, WITH ..., 17-24
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Holcer, D. & B. Lazar (2017): New data on the occurrence of the critically endangered common angelshark, Squatina squatina, in the Croatian Adriatic Sea. Jadrana. Nat. Croat., 26, 313-320.
Kabasakal, H. (2002): Elasmobranch species of the seas of Turkey. Annales ser. hist. nat., 12, 15-22.
Kabasakal, H. (2003): Historical and contemporary records of sharks from the Sea of Marmara, Turkey. Annales Ser. Hist. Nat., 13, 1-12.
Kabasakal, H. (2010): Post-release behavior and anthropogenic injuries of the bluntnose sixgill shark, Hexanchus griseus (Bonnaterre, 1788) (Chondrichthyes: Hexanchidae) in Turkish waters. Annales Ser. Hist. Nat., 20, 39-46.
Kabasakal, H. (2016): Status of cartilaginous fishes in the Sea of Marmara. In: Ozsoy, E., Çagatay, M.N., Balkis, N., Balkis, N., Ozturk, B. (Eds.) (2016). The Sea of Marmara; Marine Biodiversity, Fisheries, Conservation and Governance. Turkish Marine Research Foundation (TUDAV), Publication No: 42, Istanbul, TURKEY, 903-918 pp.
Kabasakal, H. & E. Kabasakal (2004): Sharks captured by commercial fishing vessels off the coast of Turkey in the northern Aegean Sea. Annales Ser. Hist. Nat., 14, 171-180.
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Preliminary study on the demersal fish stocks in the northern Marmara Sea. In: Öztürk, B., M. Kadioglu & H. Öztürk (eds.): Marmara Denizi 2000 Sempozyumu Bildiriler Kitabi. 11-12 November 2000, Ataköy Marina, Istanbul, pp. 500-512.
Keskin, & L. Eryilmaz (2010): Fish fauna of the Sea of Marmara and Demersal Fish Assemblages. Proceedings of the Symposium of the Marmara Sea. 25-26 September 2010, Istanbul, Turkey, p. 289-311.
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Meyers, E.K.M., F. Tuya, J. Barker, D.J. Alvarado, J.J. Castro-Hernández, R. Haroun & D. Rödder (2017): Population structure, distribution and habitat use of the critically endangered angelshark, Squatina squatina, in the Canary Islands. Aquatic Conserv. Mar. Freshw. Ecosyst., 27, 1133-1144.
Ninni, E. (1923): Primo contributo allo studio dei pesci e della pesca nelle acque dell'impero Ottomano. Missione Italiana Per l'Esplorazione dei Mari di Levante, Venezia, 187 pp.
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Roux, C. (1984): Squatinidae. In: Whitehead, P. J. P., M. -L. Bauchot, J. C. Hureau, J. Nielsen & E. Tortonese (eds.). Check-list of the fishes of the north-eastern Atlantic and of the Mediterranean (CLOFNAM). UNESCO, París. Vol. 1, 148-150.
Serena, F. (2005): Field identification guide to the sharks and rays of the Mediterranean and Black Sea. FAO Species Identification Guide for Fishery Purposes. FAO, Rome, 97 pp.
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received: 2019-04-15	DOI 10.19233/ASHN.2019.03
ADDITIONAL RECORDS OF RARE SHARKS FROM NORTHERN TUNISIA
(CENTRAL MEDITERRANEAN SEA)
Sihem RAFRAFI-NOUIRA
Unité de Recherches Exploitation des Milieux aquatiques, Institut Supérieur de Pêche et d'Aquaculture de Bizerte, Université de
Carthage, BP 15, 7080 Menzel Jemil, Tunisia
Youssouph DIATTA & Almamy DIABY
Laboratoire de Biologie marine, Institut fondamental d'Afrique noire, (IFAN Ch. A. Diop), Université Cheikh Anta Diop de Dakar, BP
206, Dakar, Senegal.
Christian CAPAPÉ
Laboratoire d'Ichtyologie, Université de Montpellier, case 104, 34095 Montpellier cedex 5, France
e-mail: capape@univ-montp2.fr
ABSTRACT
Routine investigative monitoring conducted along the northern Tunisian coast allowed us to collect some specimens of large predatory sharks, such as the great white shark, Carcharodon carcharias (Linnaeus, 1758), the shortfin mako Isurus oxyrinchus Rafinesque, 1810, and the common thresher shark Alopias vulpinus (Bonnaterre, 1788). These captures indicate that these sharks occur in the Mediterranean Sea, however, further records are needed before declaring that viable populations may still be established in the region. On the other hand, the captured specimen of smoothback angelshark Squatina oculata Bonaparte, 1840 could probably be considered as one of the last ones recorded to date in the Mediterranean Sea. The status of the species remains undetermined between extinct and critically endangered.
Key words: Large predatory sharks, distribution, status, central Mediterranean, endangered species
NUOVI RITROVAMENTI DI SQUALI RARI NELLE ACQUE DELLA TUNISIA SETTENTRIONALE (MEDITERRANEO CENTRALE)
SINTESI
Il monitoraggio investigativo di routine condotto lungo la costa tunisina settentrionale ci ha permesso di racco-gliere alcuni esemplari di grandi squali predatori, come il grande squalo bianco, Carcharodon carcharias (Linnaeus, 1758), il mako Isurus oxyrinchus Rafinesque, 1810, e lo squalo volpe Alopias vulpinus (Bonnaterre, 1788). Queste catture indicano che tali squali sono presenti nel mare Mediterraneo; sono tuttavia necessari ulteriori ritrovamenti al fine di asserire che nella regione possano essersi stabilite popolazioni vitali. D'altra parte, l'esemplare catturato di squalo angelo Squatina oculata Bonaparte, 1840, potrebbe venir considerato come uno degli ultimi ritrovamenti nel mare Mediterraneo. Lo stato della specie rimane indeterminato, tra estinto e in pericolo critico.
Parole chiave: grandi squali predatori, distribuzione, stato, Mediterraneo centrale, specie in via di estinzione
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INTRODUCTION
Studies carried out during the last two decades showed migrations of elasmobranch species towards northern areas, including brackish lagoons (Mejri et al., 2004; El Kamel et al., 2009, 2010; Rafrafi-Nouira et al., 2015). The species identified among these were the blackchin guitarfish Glaucostegus cemiculus (E. Geoffroy Saint Hilaire, 1817), the spiny butterfly ray Gymnura altavela (Linnaeus, 1758), and the sandbar shark Carcharhinus plumbeus (Nardo, 1827). Several large specimens of the latter were recorded (Rafrafi-Nouira et al., 2015; Soufi-Kechaou et al., 2018; Capape et al., 2018a). Since the capture included male and female adults, it suggested that a viable population was established in an area where the species was formerly unknown (Capape, 1989).
Additionally, these studies enabled the finding of species considered to be highly threatened, such as the sharpnose sevengill shark Heptranchias perlo (Bonnaterre, 1788), a deep-sea species recorded in the Eskerkis Bank (El Kamel-Moutalibi et al., 2014), which migrated southward to lower than usual depths (Capape et al., 2018b), and a critically endangered species, the Maltese skate Leucoraja melitensis (Clark, 1926), which is the latest specimen recorded to date (Ben Amor et al., 2018).
In this paper, we report additional and unusual records of rare species from northern Tunisian waters, among them the smoothback angelshark Squatina oculata Bonaparte, 1840, which is affected by drastic population decline.
Fig. 1: Map of the northern coast of Tunisia indicating (circle) the capture sites of the elasmobranch species presented in the paper.
Sl. 1: Zemljevid severno tunizijske obale z označenimi (krogec) lokalitetami ulova vrst, ki jih avtorji obravnavajo v prispevku.
MATERIAL AND METHODS
The four studied species reported in the present article were caught in marine waters of northern Tunisia and directly landed at the fishing sites of Bizerte and Ras Jebel (Fig. 1), where they were examined, measured for total length (TL) and weighed for total body weight (TBW). They were identified in situ using field guides, such as Whitehead et al. (1984), Louisy (2002) and Quéro et al. (2003), then delivered to the laboratory for confirmation and a thorough scientific analysis. Some specimens were measured to the nearest mm (including the percentage of total length), and the total body mass was weighed to the nearest gram following Com-pagno (1984a) for sharks, and Capapé & Roux (1980) for Squatina oculata. For each specimen, all available data related to their capture were given, including fishing gear, depth, type of bottom and, wherever possible, associated ichthyofauna. After being carefully measured and analysed, each specimen was fixed in 10% buffered formaldehyde, preserved in ethanol and deposited in the Ichthyological Collection of the Institut Supérieur de Pêche et d'Aquaculture de Bizerte, where it was assigned a catalogue number.
RESULTS
Great white shark, Carcharodon carcharias (Linnaeus, 1758)
Carcharodon carcharias is a large shark with worldwide distribution, inhabiting temperate waters especially, but known to penetrate tropical marine areas, too. Its occurrence is well documented in the entire Mediterranean Sea (De Maddalena & Heim, 2012). However, most of these records occurred in the central Mediterranean, especially in the Strait of Sicily, where several juvenile and adult specimens were recorded. Some authors consider this area a nursery ground for the species (Saïdi et al., 2005; Maliet et al., 2013; Bradaï & Saïdi, 2013). Historical and contemporary occurrences of C. carcharias in eastern Mediterranean are also well documented (Kabasakal, 2014, 2016). Based on the recent captures of newborn, young-of-the-year and juvenile specimens, a possible nursery ground for the great white shark in the Aegean Sea was also suggested (Kabasakal & Gedikoglu, 2008; Kabasakal et al., 2018).
C. carcharias is known off the Tunisian coast, and Bradaï & Saïdi (2013) noted that 59 reliable captures had been reported in the region between 1953 and 2012, with most captures (56%) occurring in the Gulf of Gabès, which was considered as a probable nursery area for the species. On 12 April 2015, a male measuring 1.8 m approximately was caught by longline in the waters surrounding the Cani Rocks (37°25'35.90" N and 10°08'43.28" E), at a depth of approximately 100 m, on rocky bottom. More recently, on 26 December 2018, a female was captured by a benthic trawl at the same
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Fig. 2: Snout of Carcharodon carcharias (Ref. ISPB-Car-carch-01), scale bar = 200 mm.
Sl. 2: Gobec velikega belega morskega volka (Ref. ISPB-Car-carch-01), merilo = 200 mm.
depth on sandy-muddy bottom (37° 25' 50.08" N and 10°02' 50. 96 E). It reached 2.80 m in total length and weighed 400 kg. As soon as it was landed on deck, the specimen was cut into slices to be sold, but it was still identified as a great white shark by experienced fishermen. Only the head of the specimen was preserved, which was more conical, sharper and pointier than it usually appears in this species. It was also slightly curved, but since no injuries or scars were observed in this atypical formation (Fig. 2), this could be considered an abnormality that had not been recorded before in any shark species. The teeth of both upper and lower jaws were huge, triangular, bladelike and serrated, confirming the identification made by the fishermen. The head was deposited in the ichthyological collection of the Institut Supérieur de Pêche et d'Aquaculture de Bizerte (Tunisia) under catalogue number ISPB-Car-carch -01.
In addition, on 11 April 2019, a second female of C. carcharias was captured by a bottom trawler in the very same area, measuring 2 m in TL and weighing 250 kg according to the information given by fishermen. It was sold immediately, but the fishermen provided us with a photograph, based on which we could confirm the identification of the species (Fig. 3).
Shortfin mako Isurus oxyrinchus Rafinesque, 1810
Isurus oxyrinchus is a pelagic, coastal and oceanic shark that can be found in tropical and temperate waters worldwide ranging from the surface to depths of
Fig. 3: The Carcharodon carcharias specimen captured on 11 April 2019, scale bar = 200 mm. Sl. 3: Primerek velikega belega morskega volka, ujet 11. aprila 2019, merilo = 200 mm.
400 m. It is well known in the eastern Atlantic and throughout the Mediterranean Sea (Quero, 1984). The species was first recorded in the northern Tunisian area
Fig. 4: Isurus oxyrinchus (Ref. FSB-lsu-oxy-01). A. General morphology, scale bar: 150 mm. B. Snout lateral view, scale bar = 40 mm. Snout ventral view, scale bar = 30 mm.
Sl. 4: Isurus oxyrinchus (Ref. FSB-lsu-oxy-01). A. Morfologija, merilo: 150 mm. B. stranski pogled na gobec, merilo = 40 mm. Pogled na gobec od spodaj, merilo = 30 mm.
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Tab. 1: Morphometric measurements (mm and %TL) of the specimen of Isurus oxyrinchus (Ref. FSB-lsu-oxy-01). Tab. 1: Morfometrične meritve (mm in %TL) primerka vrste Isurus oxyrinchus (Ref. FSB-lsu-oxy-01).
by Vinciguerra (1884). The shortfin shark is sporadically captured throughout the Tunisian coast. (Capape, 1989; Bradai et al, 2002). Additionally, Capape (1980)
noted that I. oxyrinchus is caught off the northern Cape Bon Peninsula in spring and early summer, and following Bradaï et al. (2002), it rarely occurs in southern regions.
Recently, investigations conducted in the same study area have allowed us to record the capture of several mako specimens. On 15 May 2015 and 7 July 2015, two males were caught by longline at a depth of approximately 150 m. They measured 1300 mm and 800 mm and weighed 24 kg and 4.2 kg, respectively. Several other specimens were collected during June 2018 by bottom trawlers according to the information provided by fishermen. The smallest specimen was delivered to our laboratory for examination and measurements (Fig. 4, Tab. 1).
All specimens were identified as Isurus oxyrinchus based on the combination of the following characters: body fusiform, snout very pointed; first dorsal with apex acutely pointed, pectoral fins shorter than head fins and falcate, origin of anal fin below the middle of second dorsal fin base, teeth very slender, alike in both jaws. Such description is in total accordance with Cadenat & Blache (1981), Compagno (1984b) and Quéro (1984). Isurus oxyrinchus' congeneric species, the longfin mako I. paucus Guitart Manday, 1966, occurs off the Algerian coast (Hemida & Capapé, 2008). It differs from I. oxyrinchus in pectoral fins being as long as the head, anal fin originating below the posterior end of the second dorsal fin base, and teeth widening towards the base.
The smallest specimen was deposited in the Ichthyo-logical Collection of the Faculté des Sciences de Bizerte (Tunisia) under catalogue number FSB-Isu-oxy-01 (see Tab. 1). All these captures suggest that the species is not extinct in this area and that the presence of a viable population remains a hypothesis that cannot be totally ruled out.
Common thresher shark Alopias vulpinus (Bonnaterre, 1788)
Alopias vulpinus is a large global coastal and pelagic shark occurring in depths up to 650 m (Compagno, 1984b). The species is present in the entire Mediterranean, but commoner in the western basin (Capapé, 1989). The species seems to be rather abundant off the Algerian coast, where it is caught as target or bycatch in pelagic and coastal commercial and small-scale longline, purse seine and gillnet fisheries. It is locally used for human consumption, especially the meat and fins, despite the fact that international regulations prohibit retention. Observations were carried out from 1999 to 2002 in the great fish market of Algiers, where all captures occurring throughout the Algerian coast are landed. A total of 194 specimens were examined. Conversely, recent observations carried out in the area and information provided by fishermen indicated a drastic decline of captures of the species (Hemida et al., in press).
Quignard & Capapé (1971) noted that A. vulpinus occurs throughout the Tunisian coast, but more
Reference	FSB-Isu-oxy-01	
Sex	Female	
Morphometric measurements	mm	% TL
Total length (TL)	880	100
Head length	270	30.7
Prebranchial length	190	21.6
Preorale length	60	6.8
Prenasal length	45	5.1
Intergill length	80	9.1
Eye with	22	2.5
Eye height	18	2.0
Internasal length	4	0.5
Mouth width	85	9.7
Distance between snout 1st gill	210	23.9
Precaudal length	670	76.1
Pelvic fin length	45	5.1
Pelvic height	45	5.1
Pelvic inner margin	20	2.3
Pelvic anterior margin	30	3.4
Pelvic posterior margin	30	3.4
First dorsal height	55	6.3
First dorsal base	75	8.5
First dorsal inner margin	25	2.8
First dorsal posterior margin	43	4.9
First dorsal anterior margin	80	9.1
Second dorsal height	13	1.5
Second dorsal base	15	1.7
Second dorsal inner margin	10	1.1
Second dorsal posterior margin	10	1.1
Second dorsal anterior margin	23	2.6
Pectoral inner margin	35	4.0
Pectoral anterior margin	160	18.2
Pectoral posterior margin	90	10.2
Pectoral fin length	50	5.7
Total body mass (g)	4200	
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Tab. 2: Morphometric measurements (mm and %TL) of the specimen of Alopias vulpinus (Ref. ISPB-Alo-vul-01). Tab. 2: Morfometrične meritve (mm in %TL) primerka vrste Alopias vulpinus (Ref. ISPB-Alo-vul-01).
Reference	ISPB- Alo-vul-01	
Sex	Male	
Morphometric measurements	mm	% TL
Total length (TL)	3775	100.00
Precaudal length	1840	48.74
Pre first dorsal length	830	21.99
Pre first dorsal length	160	4.24
Pre pectoral length	530	14.04
Head length	580	15.36
Prebranchial length	430	11.39
Preorale length	120	3.18
Pre-pelvic length	1350	35.76
Distance between	210	5.56
Eye with	35	0.93
Eye height	50	1.32
Mouth width	170	4.50
Pectoral fin length	335	8.87
Pectoral inner margin	480	12.72
Pectoral anterior margin	605	16.03
Pectoral posterior margin	200	5.30
Anal fin length	30	0.79
First dorsal posterior margin	290	7.68
First dorsal base	230	6.09
First dorsal inner margin	260	6.89
First dorsal anterior margin	345	9.14
Second dorsal height	30	0.79
Second dorsal base	35	0.93
Second dorsal inner margin	20	0.53
Second dorsal anterior margin	40	1.06
Second dorsal posterior margin	220	5.83
Tail anterior margin	1935	51.26
Total body mass (kg)	120	
frequently in northern areas. However, BradaT et al. (2002) reported the capture of 3 specimens in the Gulf of Gabes in the south. Routine monitoring of elasmo-branch species in the area of Bizerte-Ras Jebel offered us the opportunity to collect 4 specimens: on 14 May 2015, two specimens were captured measuring 4 m and 3.8 m, and weighing 130 kg and 120 kg, respec-
Fig. 5: Alopias vulpinus (Ref. ISPB-Alo-vul-01). A. General morphology without tail, scale bar = 300 mm. B. Head, lateral view, scale bar = 100 mm. C. Jaws, lateral view, scale bar = 30 mm. D. Snout, lateral view, scale bar = 200 mm.
Sl. 5: Alopias vulpinus (Ref. ISPB-Alo-vul-01). A. Morfologija morskega psa brez repa, merilo = 300 mm. B. Glava s strani, merilo = 100 mm. C. čeljusti s strani, merilo = 30 mm. D. Gobec s strani, merilo = 200 mm.
tively. Morphometric measurements were recorded for the smallest A. vulpinus and summarized in Table 2, its head was recovered and deposited in the Institut Supérieur de Pêche et d'Aquaculture de Bizerte (Tunisia), under catalogue number ISPB-Alo-vul-01 (Fig. 5). On 5 December 2018, a third specimen measuring 3.0 m in TL and weighing 80 kg was captured. A fourth specimen was captured on 4 April 2019 measuring 4.0 m and weighing 150 kg.
The four specimens were captured by longlines at a depth of approximately 100 m, on muddy-sandy bottoms. They were identified as A. vulpinus following the main characters: short snout, eyes rather small and not reaching the dorsal surface of the head, first dorsal fin closer to pectoral than pelvic fins. A related thresher shark, A. superciliosus, differs from A. vulpinus in having larger eyes, which reach the dorsal surface of the head, and the first dorsal closer to pelvic than pectoral fins (Quéro et al., 2003). It is the first time that so many specimens were captured in such a short time, though according to fishermen such captures are rather common in the area, which may indicate a viable population inhabiting the area.
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Smoothback angelshark Squatina oculata Bonaparte, 1840
Squatina oculata is known in the eastern Atlantic, south of the Strait of Gibraltar, from Morocco (Lloris & Rucabado, 1998) to Angola (Capape et al., 2002). The species is rather abundant off the coast of Senegal, where it plays an important role in craft fishery. There the sharks are exploited for their fins, meat and the oil extracted from their livers for therapeutic purposes (Capape et al., 2002).
Roux (1984) wrongly noted that S. oculata is only present in the western Mediterranean Basin, however, the species is indeed unknown off the Mediterranean coast of France (Capape et al., 2000). Tortonese (1956) noted its occurrence in Italian waters, and Zava et al. (2016) collected 4 juvenile specimens from the Strait of Sicily. Erguden et al. (2019) found a female S. oculata in Turkish waters and eastwards the species is also recorded in the Levant Basin (Golani, 2005).
S. oculata used to be caught quite abundantly off the Tunisian coast, especially in northern areas. The captured specimens were used to provide information about the species' reproductive biology (Capape et al., 1991). Additionally, Bradai et al. (2002) noted the
captures of some specimens southwards, in the Gulf of Gabes. Later, 4 adult specimens, 2 males and 2 females, were caught in the study area, their average total length was 1020 mm (Mnasri, 2008). On 26 December 2018, a female was captured in our study area, reaching 1300 mm in TL and weighing 5 kg. It was recorded based on a photograph taken by a fisherman (Fig. 6), which was helpful in identifying the specimen as S. oculata owing to the lack of the median line of spines, the hind tips of pelvic fins not reaching the level of first dorsal fins, and the specimen displaying a greyish colour with white spots on dorsal surface and dark bars on tail. This was probably one of the latest Mediterranean specimens found to date and confirmed the scarcity of the species in this sea. Similarly, its closely related congeneric species S. squatina (Linnaeus, 1758) has also been subjected to fishing pressure and has, following Giusto & Ragonese (2014), almost disappeared not only from Sicilian waters, but other areas as well.
DISCUSSION
Previous and new discoveries of the mentioned elasmobranch species suggest that the northern Tunisian
Fig. 6: Smoothback angelshark Squatina oculata, general morphology, scale bar = 200 mm. Sl. 6: Pegasti sklat Squatina oculata, morfologija, merilo = 200 mm.
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coast could be a hotspot for large sharks. Such phenomenon could be explained by the geographical location of the Tunisian waters in the central Mediterranean Sea, an inevitable passageway between western and eastern basins at a halfway between Atlantic and sub-tropical marine influences. Additionally, the richness of marine biodiversity sustains the hypothesis of nursery areas, especially for viviparous species, which look for the best environmental conditions before laying their litters in the wild (Rafrafi-Nouira, 2016). Biological richness minimizes the pressure of inter- and intraspecific competition for food between sharks considered as top predators (Stergiou & Karpouzi, 2002).
On the other hand, the warming of the Mediterranean waters encourages the occurrence of species in areas where they were previously unknown or rare. The best instance of this phenomenon is Carcharhinus plumbeus, abundantly captured in the Gulf of Gabes and at present in northern areas as well (Capape et al., 2018a). Captures of C. plumbeus are equally numerous off the Algerian coast (Hemida et al., 2002), the sharks probably migrating along Maghreb shores from west to east. Similar patterns could also be taken into consideration in relation to the recent abundance of Isurus oxy-rinchus and Alopias vulpinus off the northern Tunisian coast. Information provided by experienced fishermen
indicates that both species are regularly captured there.
Since large sharks are locally targeted due to their high economical value, they are not discarded at sea after the capture. They are landed at fishing sites, where they are immediately sold, despite recommendations from Tunisian authorities. Thus, it appears that large sharks have not disappeared from Tunisian waters completely, therefore the opinion of Ferretti et al. (2008) about the loss of large sharks in the area is partially contrasted. However, due to their K-selected characteristics (Camhi et al., 1998), most elasmobranch species are considered to be threatened. Still, the actual relative abundance of large sharks captured from the northern Tunisian coast shows their populations have not experienced a drastic decline in this area.
The captures of few S. oculata along the northern Tunisian coast remain questionable. Were they occasional or is a viable population of this species still present? For fishermen, captures of squatinid species are considered a rather amazing event. Recent findings of S. oculata (Mnasri 2008; Zava et al., 2016; Erguden et al., 2019; this study) suggest that the species is critically endangered, following Morey (2019), yet not extirpated. In any case, further records are needed before it is possible to confirm or refute the presence of a viable population of this species in the central Mediterranean.
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DODATNI ZAPISI O POJAVLJANJU REDKIH MORSKIH PSOV IZ SEVERNE TUNIZIJE
(OSREDNJE SREDOZEMSKO MORJE)
Sihem RAFRAFI-NOUIRA
Unité de Recherches Exploitation des Milieux aquatiques, Institut Supérieur de Pêche et d'Aquaculture de Bizerte, Université de
Carthage, BP 15, 7080 Menzel Jemil, Tunisia
Youssouph DIATTA & Almamy DIABY
Laboratoire de Biologie marine, Institut fondamental d'Afrique noire, (IFAN Ch. A. Diop), Université Cheikh Anta Diop de Dakar, BP
206, Dakar, Senegal.
Christian CAPAPÉ
Laboratoire d'Ichtyologie, Université de Montpellier, case 104, 34095 Montpellier cedex 5, France
e-mail: capape@univ-montp2.fr
POVZETEK
Na podlagi rutinskega monitoringa vzdolž severne tunizijske obale so bili pridobljeni podatki o primerkih nekaterih večjih plenilskih vrst kot so beli morski volk, Carcharodon carcharias (Linnaeus, 1758), atlantski mako Isurus oxyrinchus Rafinesque, 1810, in navadna morska lisica Alopias vulpinus (Bonnaterre, 1788). Ti ulovi kažejo, da se ti morski psi še vedno pojavljajo v Sredozemskem morju, vendar so za oceno prisotnosti viabilne populacije na raziskanem predelu potrebni še dodatni podatki. Ujeti primerek pegastega sklata Squatina oculata Bonaparte, 1840 pa je verjetno eden izmed zadnjih primerkov te vrste v Sredozemskem morju. Status te vrste je tako še vedno nejasen, saj ni jasno ali je vrsta kritično ogrožena ali morda izumrla.
Ključne besede: veliki plenilski morski psi, razširjenost, status, osrednje Sredozemsko morje, ogrožene vrste
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RECENTNE SPREMEMBE V SREDOZEMSKI BIODIVERZITETI CAMBIAMENTI RECENTI NELLA BIODIVERSITÁ MEDITERRANEA RECENT CHANGES IN MEDITERRANEAN BIODIVERSITY
ANNALES ■ Ser. hist. nat. ■ 28 ■ 2018 ■ 2
received: 2019-01-19	DOI 10.19233/ASHN.2019.04
ESTABLISHMENT OF THE NON-INDIGENOUS PRAWN PENAEUS PULCHRICAUDATUS STEBBING, 1914 IN THE MARINE AREA OF CYPRUS
Thodoros E. KAMPOURIS
Marine Sciences Department, School of the Environment, University of the Aegean. University Hill, Mytilene,
Lesvos Island, 81100, Greece e-mail: mard16012@marine.aegean.gr
Costas CONSTANTINOU
13, Iakovou Patatsou, 2362 Ayios Dometios, Nicosia, Cyprus loannis E. BATJAKAS
Marine Sciences Department, School of the Environment, University of the Aegean. University Hill, Mytilene,
Lesvos Island, 81100, Greece
ABSTRACT
The paper provides strong evidence on the establishment of the Lessepsian prawn Penaeus pulchricaudatus (Decapoda, Dendrobranchiata, Penaeidae) in Cypriot waters based on the occurrences reported in the present study and in previous records. On 3 September 2018, several P. pulchricaudatus individuals of different sizes were observed and one photographed in situ in Protaras, Trinity Beach. The individual, upon sight, was estimated to measure 15-17 cm in total length. The crustacean diversity of Cyprus is rather underestimated, even in common native species. This species should be considered as established in Cyprus, since several individuals of various sizes were observed during the sighting described herein and the species has so far been reported from three different locations along the coast of Cyprus (considering the previous records from Cape Greco and Cape Andreas).
Key words: Penaeus pulchricaudatus, Decapoda, non-indigenous species, Cyprus, Levantine Sea, eastern
Mediterranean Sea
STABILIMENTO DEL GAMBERO NON INDIGENO PENAEUS PULCHRICAUDATUS STEBBING, 1914 NELL'AREA MARINA DI CIPRO
SINTESI
L'articolo fornisce una forte evidenza dello stabilimento del gambero lessepsiano Penaeus pulchricaudatus (Decapoda, Dendrobranchiata, Penaeidae) nelle acque cipriote, in base ai ritrovamenti riportati nel presente studio e a segnalazioni precedenti. Il 3 settembre 2018 sono stati osservati diversi esemplari di P. pulchricaudatus di dimensioni diverse, uno dei quali fotografato in situ a Protaras, Trinity Beach. La lunghezza totale di questo esemplare e stata stimata a vista (15-17 cm). La diversita dei crostacei di Cipro e piuttosto sottostimata, anche per le comuni specie autoctone. Questa specie lessepsiana dovrebbe venir considerata come stabilita a Cipro, poiche durante l'avvistamento qui riportato sono stati osservati diversi individui di varie dimensioni. La specie e stata finora segnalata in tre diverse localita lungo la costa di Cipro (considerando anche i ritrovamenti precedenti di Capo Greco e Capo Andreas).
Parole chiave: Penaeus pulchricaudatus, Decapoda, specie non indigena, Cipro, Mar di Levante, Mediterraneo
orientale
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INTRODUCTION
Citizen-scientists are contributing to monitoring alien and rare species in the Mediterranean Sea (e.g., Giovos et al., 2018; Kampouris et al., 2018a, b & c). There are several projects and initiatives successfully underway in the basin (e.g., Kondylatos et al., 2017; Zenetos et al., 2017; Bariche et al., 2018; Giovos et al., 2018). But although the social media are increasing the probability of data collection through direct involvement, some scientists remain sceptical (Katsanevakis & Moustakas, 2018).
It should not be a surprise that Cyprus, which is less than 400 nm distant from the Suez Canal, is heavily impacted by the introduction of non-indigenous species (Chartosia & Michailidis, 2016). The crustacean diversity of Cyprus is rather underestimated, even in common native species (Chartosia & Theodosiou, 2018). Perhaps the most comprehensive work is the study by Lewinsohn & Holthuis (1986), which inevitably lacks information, especially in relation to non-indigenous and rare species.
The name Penaeus pulchricaudatus (Stebbing, 1914) was believed to be a junior synonym of a species of global economic importance, Penaeus japonicus. The Penaeus japonicus species complex exhibits genetic differences throughout its geographical distribution (Tsoi et al., 2014). P. pulchricaudatus occurs naturally in Australia, the western Indian Ocean, the South China Sea and the Red Sea. The population in the Mediterranean Sea, which originated from the Red Sea, is expanding northwards and the species is considered a Lessepsian migrant (Tsoi et al., 2014). Regarded as an established species in the south Aegean Sea (Kampouris et al., 2018b, and references within), it constitutes an important component of prawn fishery in Greece and Turkey (Can et al., 2004; Corsini-Foka et al., 2015). In
Cyprus, the first report of the species (as P. japonicus) dates to 1986 (Lewinsohn & Holthuis, 1986), but it is still undetermined if P. pulchricaudatus is established in Cyprus and what its population status is.
MATERIAL AND METHODS
On 3 September 2018, several P. pulchricaudatus individuals of different sizes were observed and one photographed in situ (Fig. 1) by one of the authors (C.C.) of the paper in Protaras, Trinity Beach, Cyprus (35°03'05.2"N 34°01'23.2"E, approximately), on a sandy bottom at a depth of 3-7 m, during a night dive with a Nikon D810 camera. For the purposes of the present paper only one photograph is presented.
RESULTS AND DISCUSSION
The identification of the species was based on high-resolution photos taken by one of the authors (C.C.) and on the visual identification criteria described in earlier studies (Tsoi et al., 2014; Kampouris et al., 2018b). WoRMS (2018) was used for taxonomy and systematics. The individual's total length was estimated as 15-17 cm. It was sighted as crawling slowly across the bottom (Fig. 2). The visual identification criteria are: 1. well-developed ridges and grooves on carapace, 2. body colour beige with brown transverse bands extending from top to midline, 3. pereiopods yellow to cream-whitish, 4. flagella brown, 5. pleopods yellowish to reddish with white and brown spots/blotches at base (Tsoi et al., 2014; Kampouris et al., 2018b).
The present work provides further evidence that citizen science can contribute importantly to non-indigenous species monitoring by complementing scientific knowledge. The P. pulchricaudatus species should be considered as established in Cyprus, based on the obser-
Fig. 1: Map of Cyprus, indicating sampling location (black triangle).
Sl. 1.: Zemljevid Cipra z označeno lokaliteto vzorčenja (črn trikotnik).
Fig. 2. The Penaeus pulchricaudatus from Protaras, Trinity Beach, Cyprus, and its microhabitat. Sl. 2: Kozica vrste Penaeus pulchricaudatus iz lokalitete Protaras, Trinity Beach, Ciper, in njen mikrohabitat.
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Thodoros E. KAMPOURIS et al.: ESTABLISHMENT OF THE NON-INDIGENOUS PRAWN PENAEUS PULCHRICAUDATUS STEBBING, 1914 ..., 37-42
vation of several individuals of various sizes in the wider area on this occasion and based on previous records, all following the methodologies used in earlier studies on non-indigenous species assessments (Thessalou-Legaki et al., 2006; Dulcic et al., 2011; Katsanevakis, 2011). Moreover, considering earlier records (Lewinsohn & Holthuis, 1986), the species has been observed in three different areas along the coast of Cyprus.
Underwater photography and videography are nowadays extensively used for non-indigenous and rare species detection and monitoring. They have proven very successful and useful in many cases, sometimes providing unique findings (e.g., Marcelli et al., 2016, Kondylatos et al., 2017; Bariche et al., 2018; Deidun et al., 2018; Kampouris et al., 2018c).
The taxonomy of the Dendrobranchiata, the penaeid prawns, is a rather typical example of uncertainty and controversy in science (see De Grave & Fransen, 2011). Perhaps the most striking example is the Penaeus, where even the correct spelling of the genus is a matter of controversy (see Tsoi et al., 2014 and references within for details). P. pulchricaudatus was introduced via the Suez Canal, contributing to an even wider phenomenon of the Lessepsian migration (Tsoi et al., 2014).
CONCLUSIONS
The concurrently present kuruma prawn P. japonicus should not be excluded as a potential non-indigenous species in the Mediterranean Sea, since it is cultivated in many European and Mediterranean countries (Quigley et al., 2013 and references therein). Further research, perhaps on a molecular basis, would be required to support this hypothesis.
The establishment of P. pulchricaudatus along the coast of Cyprus is not surprising, since there are many other Lessepsian species already regarded as established in the marine area of Cyprus, Parupeneus forsskali, Chartosia & Michailidis (2016), for example. Moreover, other penaeid species, such as P. monodon (e.g., Alfaro-Montoya et al., 2015; Zink et al., 2018), P. japonicus and P. pulchricaudatus (e.g,. Quigley et al., 2013; Kampouris et al., 2018b) and P. aztecus (e.g., Kampouris et al., 2018a, b; Zava et al., 2018) are acknowledged as aliens in many other parts of the world, which corroborates their invasive nature.
To better understand the geographical extent of P. pulchricaudatus' establishment and the factors affecting it, systematic surveys are needed (Maceda-Veiga et al., 2013; Nunes et al., 2017). Other penaid species that might already be established in Cyprus are P. hathor and P. aztecus, both extensively recorded in the Levantine and south Aegean Seas (see Kampouris et al., 2018b and references therein for details).
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Thodoros E. KAMPOURIS et al.: ESTABLISHMENT OF THE NON-INDIGENOUS PRAWN PENAEUS PULCHRICAUDATUS STEBBING, 1914 ..., 37-42
TUJERODNA KOZICA PENAEUS PULCHRICAUDATUS STEBBING, 1914, USTALJENA
VRSTA V VODAH CIPRA
Thodoros E. KAMPOURIS
Marine Sciences Department, School of the Environment, University of the Aegean. University Hill, Mytilene, Lesvos Island, 81100,
Greece
e-mail: mard16012@marine.aegean.gr
Costas CONSTANTINOU
13, lakovou Patatsou, 2362 Ayios Dometios, Nicosia, Cyprus Ioannis E. BATJAKAS
Marine Sciences Department, School of the Environment, University of the Aegean. University Hill, Mytilene, Lesvos Island, 81100,
Greece
POVZETEK
Avtorji poročajo o lesepski selivki, tujerodni kozici Penaeus pulchricaudatus (Decapoda, Dendrobranchiata, Penaeidae) v ciprskih vodah, ki jo lahko na podlagi novih podatkov iz pričujoče študije in predhodnih zapisov smatramo za ustaljeno vrsto. Tretjega septembra 2018 so bili številni različno veliki osebki kozice P. pulchricaudatus opaženi, eden od njih pa fotografiran v naravnem okolju na lokaliteti Protaras, Trinity Beach. Slednji naj bi meril med 15-17 cm totalne dolžine. Biodiverziteta rakov Cipra je razmeroma podcenjena, tudi na nivoju domorodnih rakov. Na podlagi opazovanj in drugih predhodnih zapisov s treh lokalitet (upoštevaje zapise iz lokalitet Cape Greco in Cape Andreas) vzdolž ciprske obale bi morali tujerodno kozico obravnavati kot ustaljeno vrsto.
Ključne besede: Penaeus pulchricaudatus, Decapoda, tujerodne vrste, Ciper, Levantsko morje, vzhodno
Sredozemsko morje
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Bariche, M., C. Constantinou & N. Sayar (2018): First confirmed record of the white-spotted puffer Arothron hispidus (Linnaeus, 1758) in the Mediterranean Sea. Bioinvasions Rec, 7(4), 433-436.
Can, M.F., Y. Mazlum, A. Demirci & M. Aktas (2004): The catch composition and Catch per Unit of Swept Area (CPUE) of Penaeid shrimps in the bottom trawls from iskenderun Bay, Turkey. TrJFAS, 4, 87-91.
Chartosia, N. & N. Michailidis (2016): First confirmed presence of the Red Sea goatfish Parupeneus forsskali (Fourmanoir & Gueze, 1976) from Cyprus. Mar Biodivers Rec, 9, 33.
Chartosia, N. & M. Theodosiou (2018): Some new additions to the crustacean decapods of Cyprus. In: Chartosia et al. New Mediterranean Biodiversity Records (July 2018). pp. 409-410. Mediterr Mar Sci, 19(2), 398-415.
Corsini-Foka, M., A. Zenetos, F. Crocetta, M.E. finar, F. Ko^ak, D. Golani, S. Katsanevakis, K. Tsiamis, E. Cook,
C.	Froglia, M. Triandaphyllou, S. Lakkis, G. Kondylatos, E. Tricarico, A. Zuljevic, M. Almeida, F. Cardigos, S. ^aglar, F. Durucan, A.M.D. Fernandes, J. Ferrario, I. Haberle, P. Louizidou, J. Makris, M. Maric, D. Micu, C. Mifsud, C. Nall, E. Kytinou, D. Poursanidis, D. Spigoli, G. Stasolla, S. Yapici & H.E. Roy (2015): Inventory of alien and cryptogenic species of the Dodecanese (Aegean Sea, Greece): collaboration through COST action training school. Manag Biol Invasion, 6(4), 351-366.
De Grave, S. & C.H.J.M. Fransen (2011): Carideorum Catalogus: The Recent Species of the Dendrobranchiate, Stenopodidean, Procarididean and Caridean Shrimps (Crustacea: Decapoda). Zool Med Leiden, 85(9), 195589.
Deidun, A., D. De Castro & M. Bariche (2018): First record of the azure demoiselle, Chrysiptera hemicyanea (Actinopterygii: Perciformes: Pomacentridae), in the Mediterranean Sea. Acta Ichthyol Piscat, 48(1), 87-91.
Dulcic, J., P. Tutman, S. Matic-Skoko & B. Glamuzina (2011): Six years from first record to population establishment: the case of the blue crab, Callinectes sapidus, Rathbun, 1896 (Brachyura, Portunidae) in the Neretva River Delta (South-eastern Adriatic Sea, Croatia). Crus-taceana, 84(10), 1211-1220.
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D.	Marmara & P. Kleitou (2018): First records of the fish Abudefduf sexfasciatus (Lacepede, 1801) and Acanthurus sohal (Forsskal, 1775) in the Mediterranean Sea. Bioinvasions Rec, 7(2), 205-210. DOI: 10.3391/ bir.2018.7.2.14
Kampouris, T.E., F. Tiralongo, A. Golemaj, I. Giovos, N. Doumpas & I.E. Batjakas (2018a): Penaeus aztecus Ives, 1891 (Decapoda, Dendrobranchiata, Penaeidae): On the range expansion in Sicilian waters and on the first record from Albanian coast. Int. J. Fish. Aquat. Stud, 6(4), 468-471.
Kampouris, T.E., I. Giovos, N. Doumpas, A. Stergioti & I.E. Batjakas (2018b): First record of Penaeus pul-chricaudatus (Stebbing, 1914) and the establishment of P. aztecus, Ives, 1891 and P. hathor (Burkenroad, 1959) (Decapoda, Dendrobranchiata, Penaeidae) in Cretan waters, Greece. J. Black Sea/Medit. Environ, 24(3), 199-211.
Kampouris, T.E., V. Kouloumperis & I.E. Batjakas (2018c): First documented record of the Palaemonid shrimp Brachycarpus biunguiculatus (Lucas, 1846) (Decapoda, Caridea, Palaemonidae) from Aegean Sea, Greece. Spixiana, 41(2), 188.
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Tsoi, K.H., K.Y. Ma, T.H. Wu, S.T. Fennessy, K.H. Chu & T.Y. Chan (2014): Verification of the cryptic species Penaeus pulchricaudatus in the commercially important
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kuruma shrimp P. japonicus (Decapoda: Penaeidae) using molecular taxonomy. Invertebr Syst, 28, 476-490.
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received: 2018-10-30	DOI 10.19233/ASHN.2019.05
OCCURRENCE OF A LESSEPSIAN SWIMMING CRAB, PORTUNUS SEGNIS (CRUSTACEA: DECAPODA), IN SOUTHERN AEGEAN SEA, TURKEY
Aytag OZGUL
Ege University Faculty of Fisheries, 35440 Urla, Izmir, Turkey e-mail: aytac.ozgul@ege.edu.tr
Okan AKYOL
Ege University Faculty of Fisheries, 35440 Urla, Izmir, Turkey
ABSTRACT
On 19 June 2018, two specimens of Portunus segnis (Forskal, 1775) were observed at a fish market in Urla, Izmir. According to the fishmonger, these blue swimming crabs had been caught incidentally with a gill net in the Akkoy Lagoon, Didim in the southeastern Aegean Sea. This paper presents a new record confirming a northward extension of the range of P. segnis in the Aegean Sea.
Key words: Portunidae, Blue swimming crab, Lessepsian species, Aegean Sea
PRESENZA DEL GRANCHIO NUOTATORE LESSEPSIANO, PORTUNUS SEGNIS (CRUSTACEA: DECAPODA), NEL MAR EGEO MERIDIONALE, TURCHIA
SINTESI
Il 19 giugno 2018, due esemplari di Portunus segnis (Forskal, 1775) sono stati trovati in un mercato del pesce a Urla, Smirne (Izmir). Secondo il pescivendolo, questi granchi nuotatori blu erano stati catturati accidentalmente con una rete da posta nella laguna di Akkdy, Didim nel mar Egeo sudorientale. L'articolo presenta un nuovo ritrovamento della specie, che conferma un'estensione verso nord della distribuzione di P. segnis nel mar Egeo.
Parole chiave: Portunidae, granchio nuotatore blu, specie lessepsiana, mar Egeo
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INTRODUCTION
Portunus segnis (Forskal, 1775) is a marine nocturnal blue swimming crab living in coastal and brackish waters on muddy and sandy bottoms at depths of 0-40 m, characterised by seasonal migration to estuaries and lagoons (CABI, 2018). Native to the western Indian Ocean from Pakistan to South Africa, P. segnis spread from the Red Sea (Lai et al., 2010) into the Mediterranean as a Lessepsian migrant, and is now found throughout the eastern and central regions of the Mediterranean Sea (CABI, 2018).
As a history of introduction, it was one of the earliest species (as Neptunus pelagicus) to enter the Mediterranean through the Suez Canal, as it was recorded in Port Said, Egypt, as early as 1898. During the 1920s, it was widely recorded in the Levant (i.e., Israel, Lebanon, Syria and Turkey) (CABI, 2018). It has since spread as far west as the northern Tyrrhenian Sea, Italy (Crocetta, 2006), the Gulf of Gabes, Tunisia (Rabaoui et al., 2015) and Maltese waters (Deidun & Scibarras, 2016).
In Turkey, P. segnis is one of the 50 exotic crustaceans, 19 of which belong to the infraorder of Brachyura; seven of these species, namely Callinectes sapidus, Mar-supenaeus japonicus, Melicertus hathor, Metapenaeus monoceros, M. stebbingi, Penaeus semisulcatus, and P segnis are of commercial importance to fisheries (Ate§ et al., 2013). The swimming crab is well-known in the southeastern Anatolian coast. Ozcan (2012) stated that P. segnis was commercially important for local fish markets in the Bays of Mersin and Iskenderun. Altug et al. (2011) mentioned P. segnis both in the Sea of Marmara and the northern Aegean Sea, but failed to provide any concrete details.
In the Aegean Sea, P. segnis has been reported from the Rhodes Island (Greece), southern Aegean Sea (Corsini-Foka et al., 2004). Yoke§ et al. (2007) reported one female specimen of P. segnis (CL = 56 mm) from Palamutbuku, and one female (CL = 65 mm) and one male (CL = 61 mm) specimen from Karacasogut, Goko-va Bay. These were the first records of P. segnis in the Turkish Aegean Sea (Fig. 1). This paper presents a new record confirming a northward extension of the range of P. segnis in the Aegean Sea.
MATERIAL AND METHODS
On 19 June 2018, two specimens of Portunus segnis (Fig. 2) measuring 75 mm (male) and 81 mm (female) in carapace length (CL) were purchased at a fish market in Urla, Izmir. According to the fishmonger these swimming blue crabs had been caught incidentally with a gill net in the Akkoy Lagoon, Didim (approx. coordinates: 37°28'N - 12°23'E), in the southeastern Aegean Sea, on a sandy/muddy bottom at a depth of 2-3 m (Fig. 1). Once the existence of these blue crabs in the Akkoy Lagoon had been confirmed (C. Ovalioglu,
Fig. 1: Capture sites of Portunus segnis specimens in the Aegean Sea between 1991 and 2018: (1) Plimmiris (SE Rhodes), August 1991, 1S / Karakonero (NE Rhodes), March 2000, 1$ / Gulf of Trianda (NW Rhodes), March 2000, 2$ (Corsini-Foka et al. 2004); (2) Palamutbükü, 12 August 2004, 1$ / Karacasögüt, Gökova Bay, 26 June 2006, 1$ 1S (Yokes et al., 2007); (3) Akköy Lagoon, 19 June 2018, 1$ 1S (this study).
Sl. 1.: Lokalitete, kjer so bili ujeti primerki rakovice vrste Portunus segnis v Egejskem morju med leti 1991 in 2018: (1) Plimmiris (JV Rodos), Avgust 1991, 1S / Karakonero (JV Rodos), Marec 2000, 1$ / Zaliv Trianda (SZ Rodos), Marec 2000, 2$ (Corsini-Foka et al., 2004);
(2)	Palamutbükü, 12 Avgust 2004, 1$ / Karacasögüt, Zaliv Gökova, 26 junij 2006, 1$ 1S (Yokes et al., 2007);
(3)	laguna Akköy, 19 junij 2018, 1$ 1S (pričujoča raziskava).
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Fig. 2: Specimens of Portunus segnis captured in the SE Aegean Sea; (a) male, (b) female (Photo: O. Akyol). Sl. 2: Primerki vrste Portunus segnis ujeti v JV Egejskem morju; (a) samec, (b) samica (Foto: O. Akyol).
pers. comm.), the specimens were measured to the nearest millimetre, fixed in 5% formaldehyde solution and deposited in the Ichthyological Collection of Ege University, Faculty of Fisheries, under the catalogue number ESFM-MAL/2018-01. Findings: Carapace width 2.2-2.3 times the length, median frontal teeth minute or obsolete, usually inconspicuous, appearing confluent or with wide gap between lateral median teeth. Chelipeds narrow, elongated, merus length in adult males up to 4.5 times the width, but in most specimens with shorter; anterior margin of merus of cheliped usually with 3 spines. Ambulatory legs relatively more elongated, slender, merus length of 4th pereiopod 3.3-4.4 times the width. Colour: Males with dark olive green/blue carapace with numerous pale white spots on surface particularly posteriorly and antero-laterally; the spots do not tend to merge to form reticulating bands. Females similar in pattern to males except for the tips of chelipeds, which are red tinged with a brownish red, instead of blue tinged with a deep rust red (Lai et al., 2010). Description and measurements of P. segnis are in complete accordance with those in Lai et al. (2010), Ozcan (2012), Rabaoui et al. (2015) and Hajjej et al. (2016).
RESULTS AND DISCUSSION
The morphometric measurements of P. segnis are indicated in Table 1. The CL in both samples is larger than that of the samples of Gokova and Palamubuku reported by Yoke§ et al. (2007). The population of the blue swimming crab along the Turkish Aegean Sea is on the rise and gaining commercial importance. While crabs are normally caught using a special fish basket, some are also incidentally captured by gill nets, particularly in the Akkoy Lagoon, Southern Aegean Sea. The fishermen
complain over the crab causing a lot of damage to their gill nets (C. Ovalioglu, pers. comm.).
It is manifest that P. segnis is gradually widening its expansion range towards northern latitudes of the Aegean Sea. Therefore, it might soon find its way to the Bay
Tab: 1: Morphometric characteristics of the Portunus segnis captured in the SE Aegean Sea. Tab. 1: Morfometrične značilnosti primerkov vrste Portunus segnis, ujetih v JV Egejskem morju.
Dimensions (mm)		
Characteristics	S	?
Carapace length (CL)	75	81
Carapace width (CW)	145	157
Frontal margin (FM)	24	26
Posterior margin (PM)	49	61
Anterio-lateral border (ALB)	62	67
Posterio-lateral border (PLB)	59	61
Dactylus length (DAL)	56	46
Manus length (MAL)	116	102
Merus length (MEL)	86	61
Merus width (MEW)	19	19
Abdomen length (AL)	47	55
Abdomen width (AW)	49	62
Telson length (TL) in the abdomen	9	9
Telson width (TW) in the abdomen	7	12
Penultimate segment length (PL)	16	17
Penultimate segment width (PW)	17	46
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of Izmir, in the northern Aegean Sea, as it occurred with the Atlantic blue crab, Callinectes sapidus (Dailianis et al., 2016). The blue crab should be monitored and new fishing gears should be developed to help reduce the damage to fish gill nets in the area.
ACKNOWLEDGMENTS
The authors thank Rüzgar Özgül, who is little son of A. Özgül, for directing our attention to the crabs.
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POJAVLJANJE LESEPSKE PLAVAJOČE RAKOVICE, PORTUNUS SEGNIS (CRUSTACEA: DECAPODA), V JUŽNEM EGEJSKEM MORJU, TURČIJA
Aytag OZGUL
Ege University Faculty of Fisheries, 35440 Urla, Izmir, Turkey e-mail: aytac.ozgul@ege.edu.tr
Okan AKYOL
Ege University Faculty of Fisheries, 35440 Urla, Izmir, Turkey
POVZETEK
Devetnajstega junija 2018 sta bila opažena dva primerka rakovice vrste Portunus segnis (Forskal, 1775) na ribji tržnici v mestu Urla, Izmir. Sodeč po izjavi ribjega trgovca sta bili plavajoči rakovici slučajno ujeti v ribiško mrežo v laguni Akkoy Lagoon (Didim) v jugovzhodnem Egejskem morju. Pričujoči zapis predstavlja nov podatek o širjenju areala rakovice P. segnis proti severu Egejskega morja.
Ključne besede: Portunidae, modra plavajoča rakovica, lesepska selivka, Egejsko morje
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Exotic crustaceans of the Turkish coast. Arthropods, 2(1), 20-25.
CABI (2018): Portunus segnis [original text by E. Shalaeva]. In: Invasive Species Compendium. Wallingford, UK: CAB International. www.cabi.org/isc. (accessed date: 02 July 2018).
Corsini-Foka, M., G. Kondylatos & P.S. Economidis (2004): Occurrence of the lessepsian species Portunus pelagicus (Crustacea) and Apogon pharaonis (Pisces) in the marine area of Rhodes Island. Med. Mar. Sci., 5(1), 83-89.
Crocetta, F. (2006): First record of Portunus pelagicus (Linnaeus, 1758) (Decapoda: Brachyura: Portunidae) in the northern Tyrrhenian Sea. Crustaceana, 79(9), 1145-1148.
Dailianis, T., O. Akyol, N. Babali, M. Bariche, F. Crocetta, V. Gerovasileiou, R. Ghanem, M. Gokoglu, T. Hasiotis, A. Izquierdo-Munoz, D. Julian, S. Katsane-vakis, L. Lipej, E. Mancini, CH. Mytilineou, K. Ounifi Ben Amor, A. Ozgül, M. Ragkousis, E. Rubio-Portillo, G. Servello, M. Sini, C. Stamouli, A. Sterioti, S. Teker, F. Tiralongo & D. Trkov (2016): New Mediterranean Biodiversity Records (July 2016). Med. Mar. Sci., 17(2), 608-626.
Deidun, A. & A. Scibarras (2016): A further record of the blue swimmer crab Portunus segnis Forskal, 1775 (Decapoda: Brachyura: Portunidae) from the Maltese Islands (Central Mediterranean). BioInvasions Records, 5(1), 43-46.
Hajjej, G., A. Sley, & O. Jarboui (2016): Morpho-metrics and length-weight relationship in the blue swimming crab, Portunus segnis (Decapoda, Brachyura) from the gulf of Gabes, Tunisia. International Journal of Engineering and Applied Sciences, 3(12), 10-16.
Lai, J.C.Y., P.K.L., Ng & P.J.F. Davie (2010): A revision of the Portunus pelagicus (Linnaeus, 1758) species complex (Crustacea: Brachyura: Portunidae), with the recognition of four species. The Raffles Bulletin of Zoology, 58(2), 199-237.
Ozcan, T. (2012): The swimming crab Portunus segnis (Forskal, 1775): host for the barnacle Chelonibia platula (Ranzani, 1818) from the Turkish coast. J. Black Sea/Medit. Environ., 18(3), 271-278.
Rabaoui, L., M., Arculeo, L., Mansour & S. Tlig-Zouari (2015): Occurrence of the lessepsian species Portunus segnis (Crustacea: Decapoda) in the Gulf of Gabes (Tunisia): first record and new information on its biology and ecology. Cah. Biol. Mar. 56, 169-175.
Yoke?, M.B., S.U. Karhan, E. Okus, A. Yuksek, A. Aslan-Yilmaz, I. Noyan Yilmaz, N. Demirel, V. Demir & B.S. Galil (2007): Alien crustacean Decapods from the Aegean coast of Turkey. Aquatic Invasions, 2(3), 162-168.
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received: 2019-03-26	DOI 10.19233/ASHN.2019.06
OCCURRENCE AND UNUSUAL ABUNDANCE OF RETICULATED LEATHERJACK STEPHANOLEPIS DIASPROS (OSTEICHTHYES: MONACANTHIDAE) FROM THE LAGOON OF BIZERTE (NORTHERN TUNISIA, CENTRAL MEDITERRANEAN SEA)
Moez SHAIEK & Sihem RAFRAFI-NOUIRA
Université de Carthage, Unité de Recherches Exploitation des Milieux aquatiques, Institut Supérieur de Pêche et d'Aquaculture de
Bizerte, BP 15, 7080 Menzel Jemil, Tunisia
Christian CAPAPÉ
Laboratoire d'Ichtyologie, Université de Montpellier, case 104, 34095 Montpellier cedex 5, France
e-mail: capape@univ-montp2.fr
ABSTRACT
This paper reports some unusual captures of the Lessepsian migrant identified as Stephanolepis diaspros Fraser-Brunner, 1940 in the Lagoon of Bizerte, a brackish area located in northeastern Tunisia. It appears that at present a viable population is successfully established in this restricted area due to the fact that the species finds the local environmental conditions adequate for living and reproducing.
Key words: distribution, expansion range, brackish area, description, colour patterns
PRESENZA E ABBONDANZA INUSUALE DI MONACANTO RETICOLATO STEPHANOLEPIS DIASPROS (OSTEICHTHYES: MONACANTHIDAE) NELLA LAGUNA DI BIZERTA (TUNISIA SETTENTRIONALE, MEDITERRANEO CENTRALE)
SINTESI
L'articob riporta alcune insolite catture del migrante lessepsiano identificato come monacanto reticolato Stephanolepis diaspros Fraser-Brünner, 1940 nella Laguna di Biserta, un'area salmastra situata nel nordest della Tunisia. Attualmente sembra che una popolazione vitale si sia stabilita con successo in quest'area ristretta, dove la specie probabilmente trova condizioni ambientali locali adeguate per vivere e riprodursi.
Parole chiave: distribuzione, intervallo di espansione, area salmastra, descrizione, modelli di colore
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INTRODUCTION
The reticulated leatherjack Stephanolepis diaspros Fraser-Brunner, 1940 is a Lessepsian migrant sensu Por (1948) which entered the Mediterranean Sea through the Suez Canal. Since its first record from the Levant Basin (Steinitz, 1927), the species has successfully invaded the eastern Mediterranean Sea (Golani, 1998; Golani et al., 2017), currently maintaining a viable population in Turkish waters (Taskavak & Bilecenoglu, 2001).
Furtherly, S. diaspros migrated toward western Mediterranean areas and reached the Gulf of Gabes, southern Tunisia (Chakroun, 1966), where it found adequate environmental conditions to develop and reproduce in the wild (Zouari-Ktari et al., 2008; Zouari-
Fig. 1: Capture sites of Stephanolepis diaspros in the central Mediterranean Sea. 1. Gulf of Gabes (Chakroun, 1966). 2. Lagoon of Bizerte (Bdioui et al., 2004). 3. Off Tabarka (Ben Amor & Capape, 2008). 4. Off Bizerte (this study). 5. Lagoon of Bizerte (this study). The black star and square indicate the captures of the species in the waters surrounding the Island of Lampedusa and the Islands of Malta, respectively (Deidun et al., 2015). Sl. 1: Lokalitete, kjer so bili ujeti primerki vrste Stephanolepis diaspros v osrednjem Sredozemskem morju. 1. Gabeški zaliv (Chakroun, 1966). 2. Laguna pri Bizerti (Bdioui et al., 2004). 3. Pri Tabarki (Ben Amor & Capape, 2008). 4. Pri Bizerti (ta študija). 5. Laguna pri Bizerti (ta študija). Črna zvezdica in kvadrat prikazujeta lokaliteti ulova v vodah okoli otoka Lampedusa in Malte (Deidun et al., 2015).
Ktari & BradaT, 2011). The first specimen from northern Tunisia was recorded in the Lagoon of Bizerte (Bdioui et al., 2004) and subsequent ones off Tabarka, a city located close to the Algerian border (Ben Amor & Capape, 2008).
Through routine monitoring regularly and frequently conducted in northern Tunisian waters other S. diaspros have been found in the area, mainly in the Lagoon of Bizerte. These new records are presented herein and commented to explain this unusual occurrence of S. diaspros as a possible settlement of the species in this lagoon.
MATERIAL AND METHODS
On 7 July 2018, a specimen of Stephanolepis diaspros was captured off Bizerte (Fig. 1), a city located in northern Tunisia (37° 17' 40.4" N and 9° 56' 05.0" E), by trammel net on sandy bottom at a depth of 20 m approximately, together with some grey triggerfish Balistes capriscus Gmelin, 1789.
The Lagoon of Bizerte is a brackish water body located in northeastern Tunisia, between 37° 8' and 37° 14' N, and between 9° 46' and 9° 56' E. It appears as an ellipse, 11 km wide and 13 km long, connected to the Mediterranean Sea by an artificial navigation channel with a maximum depth of 12 m, which facilitates the invasion of the area by S. diaspros. The average and maximum depths of the lagoon are 7 m and 12 m, respectively, the bottoms sandy, muddy and detritic and in places covered by seagrass meadows (Zaouali, 1974). At least 15 teleost and 8 elasmobranch species have been recorded in the Lagoon of Bizerte, an area with two landing sites, commercially exploited by artisanal craft fisheries (Harzallah, 2003; El Kamel et al., 2009).
A total of 32 specimens of S. diaspros were collected with the assistance of local fishermen working in the area and aware of the fishing grounds. This participative monitoring method combined with interviews of fishermen is known as local ecological knowledge (LEK). It constitutes complementary support and a source of information increasing and improving the reliability and therefore the quality of our data, following the protocols of Azzurro et al. (2011) and CIESM (2018).
All fresh specimens were measured to the nearest millimetre and weighed to the nearest gram. The Shap-iro-Wilk test for normality of the sample was performed, with P < 0.05. The chi-square test was used to determine the significance (P < 0.05). The relation between total length (TL) and total body weight (TBW) was used as a complement to feeding studies following Froese et al. (2011), to assess if Stephanolepis diaspros is able to develop in its new habitat. This LWR is TBW = aTLb, and was converted into its linear regression, expressed in decimal logarithmic coordinates and correlations were assessed by least-squares regression (log TBW = log a + b log TL). Significance of constant b differences
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n "x	ITALY
Tyrrhenian Sea	
3 « 2 S	Sldty
+	MALTA
TUNISIA 1	Central
N ■-„	Mediterranean Sea
	
200 Km	
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was assessed to the hypothesis of isometric growth if b = 3, positive allometry if b > 3, negative isometry if b > 3 (Pauly, 1983). A comparison of means was carried out using ANOVA. These two latter tests were performed using the STAT VIEW 5.0 logistic model.
Morphometric measurements and meristic counts were recorded, following Ben Amor & Capapé (2008), in the specimen caught off Bizerte and three specimens from the Lagoon of Bizerte (see Table 1). These four specimens were fixed in 10% buffered formaldehyde and preserved in 75% ethanol. One specimen was deposited in the Ichthyological Collection of the Faculté des Sciences de Bizerte, under the catalogue number FSB-Ste-dia-01, and the other 3 in the Ichthyological Collection of the Institut de Pêche et d'Aquaculture de Menzel Jemil under catalogue numbers ISPAB-Ste-dia-01, ISPAB-Ste-dia-02 and ISPAB-Ste-dia-03, respectively.
RESULTS AND DISCUSSION
The occurrence of Stephanolepis diaspros in those Tunisian regions where the species was previously unknown or rare could result from hydrobiological changes, especially temperature rise, which has affected Tunisian waters and the entire Mediterranean Sea for several decades (Francour et al., 1994; Ben Raïs Lasram
& Mouillot, 2009). Such occurrence in restricted areas is not a fortuitous event, it confirms the opinion of Ounifi-Ben Amor et al. (2019), who noted that Tunisian lagoons are hotspots for intrusion of non-indigenous species.
All specimens were identified as Stephanolepis diaspros in complete agreement with Tortonese (1967, 1986), Golani et al. (2017), Dulcic & Pallaoro (2003) and Bdioui et al. (2004). The specimen from off Bizerte displayed a brown to green-grey colour, with posterior dark areas and sinuous grey lines on the sides, dark bands non visible in caudal (Fig. 2). The specimens from the Lagoon of Bizerte exhibited a diversity of colour patterns and the phenomenon of polychromatism cannot be totally ruled out (Fig. 3). These colour differences suggest that the specimens caught off the northern coast of Tunisia could be S. hispidus (Linnaeus, 1766) according to Ben Amor & Capape (2008). However, a new revision of the genus Stephanolepis Gill, 1862 is needed prior to drawing any definite conclusions; S. hispidus and S. diaspros are well separated geographically, the former occurs in the Atlantic Ocean and the latter in the eastern Mediterranean (Tortonese, 1986).
At present, S. diaspros occurs throughout the central Mediterranean Sea, and a viable population is successfully established in the Gulf of Gabes, southern Tunisia (Zouari-Ktari & BradaT, 2011). The species is continuing its migration toward northern areas, as corroborated by
I
Fig. 2: The specimen of Stephanolepis diaspros captured off Bizerte (ref. FSB-Ste-dia-01), scale bar = 50 mm. Sl. 2: Primerek vrste Stephanolepis diaspros ujet pri Bizerti (ref. FSB-Ste-dia-01), merilo = 50 mm.
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Fig. 3: The lot of specimens of Stephanolepis diaspros collected in the Lagoon of Bizerte, scale bar = 80 mm. Sl. 3: Številni primerki vrste Stephanolepis diaspros, ujeti v laguni pri Bizerti, merilo = 80 mm.
the single specimen reported from the Lagoon of Bizerte by Bdioui et al. (2004) and now by the 32 specimens included in this study. Some of the latter were collected off the city of Tabarka close to the Algerian border (Ben Amor & Capape, 2008) and one specimen was captured off Bizerte (this study). Additionally, findings of the species in waters surrounding the Island of Lampedusa, close to the Tunisian coast, and the Islands of Malta confirm such hypothesis (Deidun et al., 2015).
Some fishermen working in the Lagoon of Bizerte were interviewed to provide further substantiating information about the captures of S. diaspros in the area. These captures occurred in May, June and, to a smaller extent, July. The fishermen would find 4-6, maximum 8 specimens per fishing trip and the captures occurred throughout the lagoon, so apparently there was no preferential site (Fig. 4). S. diaspros has a low economic value in the area, so the collected specimens were not auctioned and sold at landing sites, rather consumed by the fishermen themselves and their families. The abundance of captures in the Lagoon of Bizerte is a recent phenomenon - just two years ago, S. diaspros
Fig. 4: Map of the Lagoon of Bizerte indicating the capture sites of Stephanolepis diaspros: black disc (Bdioui et al., 2004), black stars (this study). Sl. 4: Zemljevid lagune pri Bizerti z označenimi lokalitetami, kjer so bili ujeti primerki vrste: črni krogec (Bdioui et al., 2004), črne zvezdice (ta študija).
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was still unknown to the local fishermen and often misidentified as the grey triggerfish B. capriscus.
The specimen of S. diaspros caught off Bizerte measured 215 mm in TL and its total body weight was 186 g. The TL of the 32 specimens collected in the Lagoon of Bizerte ranged between 96 mm and 235 mm, their TBW between 14 g and 235 g. Zouari-Ktari & BradaT (2011) noted that the Tunisian specimens sampled in the Gulf of Gabes reached the first sexual maturity at about 80 mm in females and 110 mm in males, thus we assume that our specimens were probably adults. Additionally, Zouari-Ktari et al. (2008) noted that specimens from the same area fed on benthic organisms and phytobenthos, and the large diversity of prey species found in the stomach contents indicated that S. diaspros is omnivorous and opportunistic. Availability and accessibility of similar prey species and the presence of large seagrass meadows (Zaouali, 1974) could explain the successful settlement of S. diaspros in this brackish area. This may be confirmed by the LWR (log TBW = -4.73 3.01 + log TL; r = 0.98; n = 32), a slightly positive allometry indicating that S. diaspros found sufficient resources locally to live in the area (Fig. 5).
Information provided by the fishermen working in this area (LEK) showed that other species with a diet similar to that of S. diaspros, such as the grey triggerfish Balistes capriscus or the salema Sarpa salpa (Linnaeus, 1758), are rarely captured. There was a single capture of the Lessepsian migrant dusky spinefoot Siganus lu-ridus (Ruppell, 1829) in the lagoon (Ounifi-Ben Amor et al., 2016), but with no new records following. However, the pressure of interspecific and/or intraspecific competition for food among these omnivorous teleost species cannot be totally ruled out. Therefore, regular
1 -|-------1--,-1--,- t........... 7-T-1--------,-1 , -
1.95 2 2.05 2.1 2.15 2.2 2.25 2.3 2.35 2.4 log TL
Fig. 5: The size (TL) versus total body weight (TBW) relationship in the specimens collected in the Lagoon of Bizerte (this study) expressed in logarithmic coordinates.
Sl. 5: Razmerje med velikostjo (TL) in celotno telesno težo (TBW) pri primerkih ujetih v laguni Bizerte (ta študija), izraženo v logaritmičnih koordinatah.
monitoring of S. diaspros should be carried out to assess the role of the species in its new environment. To reach this goal, further captures of the species are necessary for studying, in particular, its reproductive biology, diet and feeding habits.
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Tab. 1: Morphometric measurements, meristic counts and total body weight recorded in the specimens of Stepha-nolepis diaspros collected off Bizerte (ref. FSB-Ste-dia-01) and in the Lagoon of Bizerte (ISPAB-Ste-dia-01, ISPAB-Ste-dia-02 and ISPAB-Ste-dia-03).
Tab. 1: Morfometrične meritve, meristična štetja in celotna masa telesa primerkov afriškega kostoroga, ujetih pri Bizerti (ref. FSB-Ste-dia-01) in v laguni pri Bizerti (ISPAB-Ste-dia-01, ISPAB-Ste-dia-02 in ISPAB-Ste-dia-03).
References	FSB-Ste-dia-01		ISPAB-Ste-dia-01		ISPAB-Ste-dia-02		ISPAB-Ste-dia-03	
Measurements	mm	% TL	mm	% TL	mm	% TL	mm	% TL
Total length (TL)	215	100	235	100	180	100	160	100
Standard length (SL)	185	86.05	200	85.11	150.00	83.33	137	85.63
Head length	55	25.58	56.96	24.24	43.85	24.36	40.02	25.01
First predorsal length	48.66	22.63	56.98	24.25	43.45	24.14	36.07	22.54
Second predorsal length	94.52	43.96	100.5	42.77	80.47	44.71	74.59	46.62
Preanal length	97.51	45.35	108.68	46.25	86.85	48.25	78.05	48.78
Prepectoral length	49.49	23.02	52.5	22.34	44.38	24.66	40.15	25.09
First dorsal fin length	13.57	6.31	14.31	6.09	12.50	6.94	12.58	7.86
Second dorsal fin length	73.43	34.15	74.64	31.76	57.04	31.69	52.86	33.04
Anal fin length	65.84	30.62	69.59	29.61	54.58	30.32	47.02	29.39
Pectoral fin length	9.36	4.35	11.62	4.94	8.40	4.67	7.56	4.73
Caudal fin length	24.29	11.30	25.83	10.99	20.58	11.43	16.43	10.27
Maximal body length	85.55	39.79	87.89	37.40	70.44	39.13	65.67	41.04
Eye diameter	11.44	5.32	14.2	6.04	10.63	5.91	9.59	5.99
Interorbital length	12.39	5.76	14.41	6.13	11.44	6.36	9.67	6.04
Preorbital length	35.68	16.60	39.6	16.85	32.62	18.12	25.62	16.01
Postorbital length	6.12	2.85	9.29	3.95	7.21	4.01	6.74	4.21
Meristic counts								
First dorsal fin rays	I		I		I		I	
Second dorsal fin rays	31		31		31		31	
Anal fin rays	31		31		31		31	
Pectoral fin rays	13		13		13		13	
Caudal fin rays	12		12		12		12	
Total body mass (gram)	186		225		93		70	
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POJAVLJANJE IN NENAVADNA ŠTEVILČNOST AFRIŠKEGA KOSTOROGA, STEPHANOLEPIS DIASPROS (OSTEICHTHYES: MONACANTHIDAE) IZ LAGUNE PRI BIZERTI (SEVERNA TUNIZIJA, OSREDNJE SREDOZEMSKO MORJE)
Moez SHAIEK & Sihem RAFRAFI-NOUIRA
Université de Carthage, Unité de Recherches Exploitation des Milieux aquatiques, Institut Supérieur de Pêche et d'Aquaculture de
Bizerte, BP 15, 7080 Menzel Jemil, Tunisia
Christian CAPAPÉ
Laboratoire d'Ichtyologie, Université de Montpellier, case 104, 34095 Montpellier cedex 5, France
e-mail: capape@univ-montp2.fr
POVZETEK
Avtorji poročajo o nenavadnih ulovih ribje lesepske selivke vrste Stephanolepis diaspros Fraser-Brunner, 1940 v laguni pri Bizerti, brakičnem okolju v severovzhodni Tuniziji. Kaže, da se je v tem omejenem okolju zaradi ugodnih življenjskih razmer za preživetje in razmnoževanje vzpostavila viabilna populacija te vrste.
Ključne besede: razširjenost, širjenje areala, brakično okolje, opis, barvni vzorci
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REFERENCES
Azzurro, E., P. Moschella, F. Maynou (2011): Tracking signal of changes in Mediterranean fish diversity based on Local Ecological Knowledge. Plos ONE, 6(9), e24885.
Bdioui, M., H. Gharssallah, L. Ben Naceur & R. M'Rabet (2004): Première mention du poisson-bourse Stephanolepsis diaspros (Fraser-Brunner, 1940) dans la lagune de Bizerte. Bull. Inst. Natn Sci Technol Mer Salammbô, 31, 119-121.
Ben Amor, M.M. & C. Capapé (2008): Occurrence of a filefish closely related to Stephanolepis diaspros (Osteichthyes: Monacanthidae) off northern Tunisian coast (south-western Mediterranean). Cah. Biol. Mar., 49(4), 323-328.
Ben Raïs Lasram, F. & D. Mouillot (2009): Increasing southern invasion enhances congruence between endemic and exotic Mediterranean fish fauna. Biol. Inv., 11(3), 697-711.
Chakroun, F. (1966): Capture d'animaux rares en Tunisie. Bull. Inst. Natn Scient. Tech. Océanogr. Pêche Salammbô, 1(2), 75-79.
CIESM (2018): Engaging marine scientists and fishers to share knowledge and perceptions - Early lessons. CIESM Workshop Monograph n° 50 [F. Brialy, Ed.] CIESM Publisher, Monaco, 218 pp.
Deidun, A., L. Castriota, M. Falautano, G. Mara-ventano, E. Prazzi & F.Andaloro (2015): Documenting the occurrence of he Lessepsian fish Stephanolepis diaspros within the Strait of Sicily, central Mediterranean. J. Black Sea /Medit. Environ., 21(1), 1-11.
Dulcic, J. & A. Pallaoro (2003): First record of the filefish, Stephanolepsis diaspros (Monacanthidae) in the Adriatic Sea. Cybium, 27(4), 321-322.
El Kamel-, O., N. Mnasri, J. Ben Souissi, M. Boumaïza, M. M. Ben Amor & C. Capapé (2009): Inventory of elasmobranch species caught in the Lagoon of Bizerte (north-eastern Tunisia, central Mediterranean). Pan-Amer. J. Aquat. Sci., 4(4), 383-412.
Francour, P., C. F. Boudouresque, J.G. Harmelin., M.L Harmelin-Vivien. & J.-P. Quignard (1994): Are the Mediterranean waters becoming warmer? Mar. Poll. Bull., 28 (9), 523-526.
Froese, R., A. C. Tsikliras & K.I. Stergiou (2011): Editorial note on weight-length relations of fishes. Acta Ichthyol. Piscat., 41(4), 261-263.
Golani, D. (1998): Distribution of Lessepsian migrant fish in the Mediterranean. Ital. J. Zool., 65, suppl., 95-99.
Golani, D., L. Orsi-Relini L., E. Massuti E. & J.-P. Quignard, J. Dulcic & E. Azzurro (2017): CIESM Atlas of Exotic Fishes in the Mediterranean Sea: alien fishes, invasive fishes. World Wide Web electronic publication. http// www.ciesm.org/atlas/appendix1.html, version 01/2017.
Harzallah, A. (2003): Transports de polluants dans la lagune de Bizerte simulés par un modèle de circulation d'eau. Bull. Inst. Natn Sci Technol Mer Salammbô, 31, 119-121.
Ounifi-Ben Amor, K., S. Rafrafi-Nouira, O. El Kamel-Moutalibi & M.M. Ben Amor (2016): Westernmost occurrence of the dusky spinefoot Siganus luridus (Osteichthyes, Siganidae) along North African coasts. Arxius Miscel-Lània Zool., 14, 99-207.
Ounifi-Ben Amor, K., M.M. Ben Amor & J. Ben Souissi (2018): Tunisian Lagoons: Hotspots and nursery grounds for non indigenous fauna. In: First Mediterranean Symposium on the Non-Indigenous Species (Antalya, Turkey, 17-18 January 2019), pp. 101-102.
Pauly, D. (1983): Some simple methods for assessment of tropical fishes. FAO Fish. Tech. Papers, 234, 3-10.
Por, F. D. (1978): Lessepsian migration. Ecological studies 23. Springer-Verlag, Berlin, New-York, 228 pp.
Steinitz, W. (1927): Beiträge zur Kenntnis der Küstenfauna Palästinas. I. Pubblic. Staz. Zool. Napoli, 8(3-4), 311-353.
Taskavak, E. & K. I. Bilecenoglü (2001): Length-weigth relationships for 18 Lessepsian (Red Sea) immigrant fish species from the eastern Mediterranean coasts of Turkey. J. Mar. Biol. Assoc. U. K., 81(5), 895-896.
Tortonese, E. (1986): Monacanthidae. In: Whitehead, P.J.P., M.L. Bauchot, J.-C. Hureau, J. Nielsen & E. Tortonese (eds): Fishes of the North-eastern Atlantic and the Mediterranean, Vol. 3. Unesco, Paris, pp. 13381339.
Tortonese, E. (1967): Un pesce plettognato nuovo per i mari italiani: Stephanolepis diaspros, Fraser Brünner. Doriana, 4(181), 1-4.
Zaouali,, J. (1974): Les peuplements dans les bi-ocœnoses lagunaires tunisiennes. Etude de la biologie de l'espèce pionnière Cerastoderma glaucum Poiret. PhD. Thesis. University of Caen, France, 344 pp.
Zouari-Ktari, R. & M.N. Bradai (2011): Reproductive biology of the lessepsian Reticulated leatherjack Stephanolepis diaspros (Fraser-Brünner, 1940) in the Gulf of Gabès (eastern Mediterranean Sea). Rev. Fish Biol. Fisheries, 21(3), 641-648
Zouari-Ktari, R., M.N. Bradai & A. Bouain (2008): The feeding habits of the Lessepsian fish Stephanolepis diaspros (Fraser-Brunner, 1940) in the Gulf of Gabès (eastern Mediterranean Sea). Cah. Biol. Mar., 49(4), 329-335.
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IHTIOLOGIJA ITTIOLOGIA ICHTHYOLOGY
ANNALES ■ Ser. hist. nat. ■ 29 ■ 2019 ■ 1
received: 2019-05-17	DOI 10.19233/ASHN.2019.07
MARINE CRYPTOBENTHIC FISH FAUNA OF SLOVENIA (NORTHERN
ADRIATIC SEA)
Domen TRKOV
Marine Biology Station, National Institute of Biology, Piran, Fornače 41, 6330 Piran;
Jožef Stefan International Postgraduate School, Jamova cesta 39, 1000 Ljubljana, Slovenia
e-mail: domen.trkov@nib.si
Borut MAVRIČ, Martina ORLANDO-BONACA & Lovrenc LIPEJ
Marine Biology Station, National Institute of Biology, Piran, Fornače 41, 6330 Piran
ABSTRACT
Cryptobenthic fish fauna constitute one of the less studied fish groups in the Adriatic Sea. As regards Slovenian coastal waters, only few papers dealing with cryptobenthic fish assemblages have been published to date. All the available data about cryptobenthic fish species in the Slovenian sea are presented in this paper, with particular interest in their geographic and depth distribution. Altogether 798 specimens of 11 different species were collected. Thorogobius macrolepis and Chromogobius quadrivittatus were found in Slovenian territorial waters for the first time only recently. The majority of fishes have been recorded using new techniques, associated with SCUBA diving equipment and the use of the narcotic Quinaldine.
Key words: cryptobenthic habitats, fish assemblage, coastal waters, northern Adriatic Sea
FAUNA ITTICA CRIPTOBENTONICA MARINA DELLA SLOVENIA (ADRIATICO
SETTENTRIONALE)
SINTESI
La fauna ittica criptobentonica costituisce uno dei gruppi di pesci meno studiati nel mare Adriatico. Per quanto riguarda le acque costiere della Slovenia, finora sono stati pubblicati solo pochi articoli riguardanti questo gruppo. L'articolo presenta tutti i dati disponibili sulle specie ittiche criptobentoniche del mare sloveno, con particolare interesse per la loro distribuzione geografica e batimetrica. Complessivamente sono stati raccolti 798 esemplari di 11 specie. Thorogobius macrolepis e Chromogobius quadrivittatus sono stati trovati per la prima volta nelle acque territoriali slovene solo di recente. La maggior parte dei pesci e stata catturata usando nuove tecniche associate alle attrezzature subacquee e all'uso di narcotici.
Parole chiave: habitat criptobentonici, comunita ittiche, acque costiere, mare Adriatico settentrionale
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INTRODUCTION
Despite the fact that the ichthyofauna of the Adriatic Sea is relatively well studied, information about the Slovenian part of Gulf of Trieste is still scant (Lipej et al., 2005). Numerous recent studies have contributed to filling the gap in the knowledge of the marine ich-thyofauna in the Slovenian sea (e.g. Lipej et al., 2005; 2016a; 2018a; Orlando-Bonaca & Lipej, 2005; Orlan-do-Bonaca & Trkov, 2016). However, little is known about cryptobenthic fish fauna and its occurrence in the area. "Cryptobenthic" (Miller, 1979) species are species whose "small body size permits exploitation of restricted habitats, where food and shelter are obtained in, or in relation to, conditions of substrate complexity and/or restricted living space, with a physical barrier likely to be interposed between the small fish and sympatric predators". Therefore, they are hardly observed by divers and are usually not detected in conventional ichthyofaunal surveys (Henriques, 2002). The qualitative definition of cryptobenthic fish (Depczynski & Bellwood, 2003) and the recent quantitative definition of cryptobenthic reef fish (Brandl et al., 2018) were based exclusively on fish size, while Kovacic et al. (2012) suggested that cryptobenthic refers to benthic positioning, since it is ecologically meaningful. Lipej et al. (2016b) divided cryptobenthic fish species into real cryptobenthic species (that are always hidden) and large cryptobenthic fish species (large-sized fish species that occasionally leave their hiding places, but more or less permanently use them). Exhibiting such cryptic life style, affords them protection against predators (Hofrichter & Patzner, 2000). Smith-Vaniz et al. (2006) concluded that around 64% of fish fauna can be missed by visual census due to their hiding habits. Therefore, knowledge about the occurrence and ecology of cryptobenthic remains very fragmented at global scale.
Cryptobenthic fish species in the Adriatic Sea have attracted scientific interest in the last two decades, as evidenced by various studies (e.g. Kovacic, 1997, 2005; Santin et al., 2005; Santin, 2008; Brandl et al., 2012; Kovacic et al., 2012, Glavicic et al., 2016). Some papers highlighting the occurrence of cryptobenthic species have also been published for the Slovenian part of the Adriatic Sea, such as those of Lipej & Richter (1999), Lipej et al. (2005, 2012, 2016b), Orlando-Bonaca & Lipej (2007, 2008) and Orlando-Bonaca & Trkov (2016). Moreover, knowledge about cryptobenthic fish assemblages is increasing due to the development of new approaches and techniques, associated with SCUBA diving and suitable fish sampling (Glavicic & Kovacic, 2016).
The aim of the current study is to present all available information about the occurrence of cryptobenthic fish species (including new unpublished data), their habitat preferences and depth distribution in Slovenian coastal waters.
MATERIAL AND METHODS
Study area
The study was conducted in the Slovenian part of the Gulf of Trieste, the northernmost part of both the Adriatic and Mediterranean Seas. Although the sea-bed of the Slovenian sea is predominantly soft sedimentary of fluvial origin, the bottom along the coastline (approximately 46.7 km) is mostly rocky, consisting mainly of Eocene Flysch layers, with alternating solid sandstone and soft maerl (Ogorelec et al., 1997). The area is characterized by the lowest winter temperatures (usually below 10°C) in the Mediterranean Sea (Boicourt et al., 1999). Average salinity is about 37, influenced by fresh water inputs near the coast, mainly from the Isonzo River (Mozetič et al., 1998). The embayed situation of the Gulf of Trieste, with dominant winds blowing in an offshore direction (mainly from the North-East) and very shallow waters, creates quite sheltered conditions (Boicourt et al., 1999). In the past decades, the Slovenian coastal area has suffered from many anthropogenic impacts such as new infrastructure, intensive fishing, sewage outfalls and mariculture; therefore, only 18% of the coastline is still in its natural state (Turk, 1999).
Fieldwork
The information about cryptobenthic specimens was obtained from: a) existing published literature sources (Lipej & Richter, 1999; Lipej et al., 2005; Orlando-Bonaca & Lipej, 2007, 2008; Orlando-Bonaca &Trkov, 2016), b) specific sampling of cryptobenthic fish fauna performed from July 1998 to March 2019, and c) specific sampling of clingfish (Gobiesocidae) fauna performed from October 2016 to March 2019.
All sampling surveys were carried out in Slovenian coastal waters. Specimens were collected or recorded by snorkelling or SCUBA diving in mediolittoral and infralittoral belts. Additionally, some specimens were also collected in shallow waters and tide pools during low tide. Fish were searched for in different hiding places such as under stones, boulders, shells, empty Lithophaga lithophaga (Linnaeus, 1758) burrows or inside natural cavities such as caves, cavities, holes, clefts etc. Searches for fish were also carried out in Posidonia oceanica meadows, in rhizomes (matte) in particular.
To facilitate the collection of fish, the narcotic Quinaldine (Sigma-Aldrich) was used (in Lipej et al., 2005, specific sampling of cryptobenthic fish fauna and specific sampling of clingfish fauna). Quinaldine was diluted to 1:15 solution with alcohol. When a cryptobenthic fish was sighted, the narcotic was sprayed into the hiding place using a laboratory wash bottle. The anesthetized fish were then caught with a hand net. Endolithic specimens were expelled from
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Fig. 1: UTM quadrants with numbers of cryptobenthic species present within.
Sl. 1: UTM kvadrati z označenim številom kripto-bentoških vrst, ugotovljenih v njih.
the burrows with the help of a thin stick, and caught using a plastic bag placed over the burrow opening, as proposed by Kotrschal (1988). This method was used to assess blennioid fish assemblages in Slovenian coastal waters by Orlando-Bonaca & Lipej (2007, 2008). Basic ecological data on the sampling locality were collected at each site. For identification purposes, one specimen of each species per location was taken; the others were recorded and then released. All collected specimens are kept, and identified by a collection number, in the collection of the Marine Biology Station in Piran (MBS),
National Institute of Biology, and fulfil the standards proposed by Bello et al. (2014). For identification purpose, the fish identification keys of Jardas (1996), Marčeta (1999) and Kovačic (2008) were used.
Data analyses
In order to present the data on cryptobenthic fish occurrence, the Slovenian sea was divided into 73 UTM quadrants (2 x 2 km) according to the approach of Lipej et al. (2018b). The coastal area considered in this study is comprised within 24 UTM quadrants. On the maps for single species, increasing dot size denotes the increasing number of specimens found within a quadrant.
RESULTS
In the last two decades, a total of 798 cryptobenthic specimens were found at 45 localities, within 14 different UTM quadrants (58.3% of 24 coastal quadrants; Fig. 1) along the Slovenian coastline. Specimens belong to 11 cryptobenthic fish species from four families (Tab. 1; Figs. 2 and 3).
The number of collected specimens was the highest in 2 quadrants: the first covering the area of Piran (305 specimens), and the second comprising the area from Piran to Portorož, including the waters in front of the MBS (263 specimens). The highest number of species (8 species) were recorded in 4 adjacent quadrants, ranging from Strunjan to Portorož including protected area of Natural Monument Cape Madonna Piran. The absence of cryptobenthic fish in some coastal quadrants is due to the lack of sampling surveys in inaccessible areas
Tab. 1: Number of specimens per fish species and their proportion according to the number of all cryptobenthic fish found in Slovenian coastal waters.
Tab. 1: Število primerkov posameznih ribjih vrst in njihov delež glede na celotno število kriptobentoških rib, ugotovljenih v slovenskih obalnih vodah.
Family	Number of species	Species	Number of Specimens	Percentage (%)
		Chromogobius quadrivittatus	1	0.1
		Millerigobius macrocephalus	53	6.6
Gobiidae	5	Thorogobius ephippiatus	1	0.1
		Thorogobius macrolepis	2	0.3
		Zebrus zebrus	38	4.8
		Apletodon incognitus	202	25.3
Gobiesocidae	3	Lepadogaster candolii	173	21.7
		Lepadogaster lepadpogaster	237	29.7
Blenniidae	2	Microlipophrys nigriceps	48	6.0
		Parablennius zvonimiri	33	4.1
Clinidae	1	Clinitrachus argentatus	10	1.3
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Fig. 2: Cryptobenthicgobies in the Slovenian Sea: A) Chromogobius quadrivittatus, B) Millerigobius macrocephalus, C) Thorogobius macrolepis, D) Thorogobius ephippiatus and E) Zebrus zebrus.
Sl. 2: Kriptobentoški glavači v slovenskem morju: A) Chromogobius quadrivittatus, B) Millerigobius macrocephalus, C) Thorogobius macrolepis, D) Thorogobius ephippiatus in E) Zebrus zebrus.
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such as ports and harbours rather than to unsuitable habitats for these species. It should also be taken into consideration that the sampling effort and sampling methods were not the same in all UTM quadrants. Thus, data on the abundance or on the diversity of the
UTM quadrants are not comparable. On coastal rocky bottoms, 10 cryptobenthic fish species were found, while on sedimentary bottom only 4 species were observed. The distribution of the fish according to depth is presented in Fig. 4.
Fig. 3: Cryptobenthic fish species in the Slovenian Sea: A) Apletodon incognitus, B) Lepadogaster lepadogaster, C) Lepadogaster candolii, D) Microlipophrys nigriceps, E) Parablennius zvonimiri and F) Clinitrachus argentatus. Sl. 3: Kriptobentoške vrste rib v slovenskem morju: A) Apletodon incognitus, B) Lepadogaster lepadogaster, C) Lepadogaster candolii, D) Microlipophrys nigriceps, E) Parablennius zvonimiri in F) Clinitrachus argentatus.
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Fig. 4: Depth distribution of cryptobenthic fish species in the Slovenian Sea: Millerigobius macrocephalus; Zebrus zebrus; Apletodon incognitus; Lepadogaster lepadogaster; Lepadogaster candolii; Microlipophrys nigriceps; Parablennius zvonimiri; Clini-trachus argentatus. On abscissa axis are relative frequencies of occurrence (%), on ordinary axis is shown depth range (m). Sl. 4: Globinska razširjenost kriptobentoških vrst rib v slovenskem morju: Millerigobius macrocephalus; Zebrus zebrus; Apletodon incognitus; Lepadogaster lepadogaster; Lepadogaster candolii; Microlipophrys nigriceps; Parablennius zvonimiri; Clini-trachus argentatus. Na abscisi so relativne frekvence pojavljanja (%), na ordinati pa je prikazan globinski razpon (m).
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Family Gobiidae
Chromogobius quadrivittatus (Steindachner, 1863)
A single specimen of C. quadrivittatus was captured on 26th July 2018 between Salinera and Pacug (Fig. 5). It was found in a rocky environment (boulder field) where it was hiding under a stone at a depth of 1.5. This finding represents the first record of this species in Slovenia. The specimen is housed in the ichthyological collection of the MBS: IC-MBP 334.
Fig. 5: Occurrence of Chromogobius quadrivittatus in the Slovenian Sea. The size of the dots is shown at the right of the map and is ranking from the smallest to the biggest, based on number of specimens found within quadrant: 1 specimen, 2-3 specimens, 4-5 specimens, 6-15 specimens, > 16 specimens.
Sl. 5: Pojavljanje vrste Chromogobius quadrivittatus v slovenskem morju. Velikost krogcev je prikazana na desni strani zemljevida z naraščajočim zaporedjem števila ugotovljenih primerkov na kvadrat: 1 primerek, 2-3 primerki, 4-5 primerkov, 6-15 primerkov, > 16 primerkov.
Millerigobius macrocephalus (Kolombatovic, 1891)
Altogether, 53 specimens of M. macrocephalus were found within 8 UTM quadrants (Fig. 6). The majority of the specimens were found in rocky environments at depths between 1 and 4 m (87.5%), where they were hiding mostly under stones or in rocky clefts. Few specimens were found also in seagrass meadow under isolated stones. Specimens are housed in the ichthyological collection of the MBS: IC-MBP 006 and IC-MBP 023.
Thorogobius ephippiatus (Lowe, 1839)
Only one specimen of T. ephippiatus was found. It was observed on 9th August 2005 within the Cape Madonna Nature Monument of Piran (Fig. 7). The specimen was observed at a depth of 10 m in a cavity beneath sandstone rocks, covered with sand (Lipej et al., 2005).
Fig. 6: Occurrence of Millerigobius macrocephalus in the Slovenian Sea. For explanation of dot size see Fig. 5. Sl. 6: Pojavljanje vrste Millerigobius macrocephalus v slovenskem morju. Glej Sl. 5 za pojasnilo glede velikosti posameznih krogcev.
Thorogobius macrolepis (Kolombatovic, 1891)
Two specimens of T. macrolepis were found in Slovenian coastal waters, both of them in the Cape Madonna Natural Monument of Piran (Fig. 8). The first specimen was observed by one of the authors (B.M.) on 22th September 2015, while the second specimen was observed by a photographer, Borut Furlan, on 18th March 2017. Both specimens were found in a sheltered cavity covered with rough sand at a depth of around 10 m.
Fig. 7: Occurrence of Thorogobius ephippiatus in the Slovenian Sea. For explanation of dot size see Fig. 5. Sl. 7: Pojavljanje vrste Thorogobius ephippiatus v slovenskem morju. Glej Sl. 5 za pojasnilo glede velikosti posameznih krogcev.
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Fig. 8: Occurrence of Thorogobius macrolepis in the Slovenian Sea. For explanation of dot size see Fig. 5. Sl. 8: Pojavljanje vrste Thorogobius macrolepis v slovenskem morju. Glej Sl. 5 za pojasnilo glede velikosti posameznih krogcev.
Zebrus zebrus (Risso, 1827)
Specimens of Z. zebrus were found in 8 UTM quadrants (Fig. 9). Altogether, 38 specimens were recorded in shallow waters, less than 3 m deep. Specimens were mostly found in rocky environments under stones and in rocky clefts, while some of them were also recorded in Cymodocea nodosa and P. oceanica meadows, where they were hiding under seashells and single stones. Some specimens were also found under stones in tide pools in lower mediolittoral areas. Specimens are housed in the ichthyological collection of the MBS: IC-MBP 063 and IC-MBP 066.
Family Gobiesocidae
Apletodon incognitus Hofrichter & Patzner, 1997
Altogether, 202 specimens of A. incognitus were found that were present in 10 UTM quadrants (Fig. 10). Specimens were found in C. nodosa and P. oceanica meadows or nearby, where they were hiding on noble pen shells (Pinna nobilis), in dead oyster shells (Ostrea edulis), attached to noble pen shells and in dead sea-shells on the sea bottom. More than 97% of the speci-
Fig. 10: Occurrence of Apletodon incognitus in the Slovenian Sea. For explanation of dot size see Fig. 5. Sl. 10: Pojavljanje vrste Apletodon incognitus v slovenskem morju. Glej Sl. 5 za pojasnilo glede velikosti posameznih krogcev.
Fig. 9: Occurrence of Zebrus zebrus in the Slovenian Sea. For explanation of dot size see Fig. 5. Sl. 9: Pojavljanje vrste Zebrus zebrus v slovenskem morju. Glej Sl. 5 za pojasnilo glede velikosti posameznih krogcev.
Fig. 11: Occurrence of Lepadogaster candolii in the Slovenian Sea. For explanation of dot size see Fig. 5. Sl. 11: Pojavljanje vrste Lepadogaster candolii v slovenskem morju. Glej Sl. 5 za pojasnilo glede velikosti posameznih krogcev.
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mens were found at depths between 2 and 6 m, while the majority were present at depths between 4 and 5 m. Specimens are housed in the ichthyological collection of the MBS: IC-MBP 252 and IC-MBP 253.
Lepadogaster candolii Risso, 1810
Altogether, 173 specimens of L. candolii were found in 7 UTM quadrants (Fig. 11). Specimens were mostly found under stones in rocky environment, while a small proportion of them were also found in C. nodosa and P. oceanica meadows, where they were hiding under stones and on or under seashells (e.g. P. nobilis, O. edu-lis). Most of the specimens (86.0%) were present in the depth range from 1 to 4 m. The specimens are housed in the ichthyological collection of the MBS: IC-MBP 031 and IC-MBP 038.
Lepadogaster lepadogaster (Bonnaterre, 1788)
Specimens of L. lepadogaster were found in 8 UTM quadrants (Fig. 12). Altogether, 237 specimens were observed and all of them were found under stones in rocky environment (boulder field). The specimens were observed in shallow waters, mostly less than 2 m deep (98.3%), with the majority (64.7%) above 1 m. The specimens were housed in the ichthyological collection of the MBS: IC-MBP 281.
Family Blenniidae
Microlipophrys nigriceps (Vinciguerra, 1883)
Altogether, 48 specimens of M. nigriceps were observed in 4 UTM quadrants (Fig. 13). The majority of specimens (89.6%) were observed in the depth range from 3 to 9 m. The specimens were found in the rocky
Fig. 12: Occurrence of Lepadogaster lepadogaster in the Slovenian Sea. For explanation of dot size see Fig. 5. Sl. 12: Pojavljanje vrste Lepadogaster lepadogaster v slovenskem morju. Glej Sl. 5 za pojasnilo glede velikosti posameznih krogcev.
Fig. 13: Occurrence of Microlipophrys nigriceps in the Slovenian Sea. For explanation of dot size see Fig. 5. Sl. 13: Pojavljanje vrste Microlipophrys nigriceps v slovenskem morju. Glej Sl. 5 za pojasnilo glede velikosti posameznih krogcev.
littoral, mostly in dimly lit habitats such as the underside of boulder terraces. They were hiding in precoralligenous formations, where they also occupied empty burrows excavated by L. lithophaga. The specimens are housed in the ichthyological collection of the MBS: IC-MBP 124.
Parablennius zvonimiri (Kolombatovic, 1892)
Specimens of P. zvonimiri were observed on the shady side of boulders and in precoralligenous formations in
Fig. 14: Occurrence of Parablennius zvonimiri in the Slovenian Sea. For explanation of dot size see Fig. 5. Sl. 14: Pojavljanje vrste Parablennius zvonimiri v slovenskem morju. Glej Sl. 5 za pojasnilo glede velikosti posameznih krogcev.
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Fig. 15: Occurrence of Clinitrachus argentatus in the Slovenian Sea. For explanation of dot size see Fig. 5. Sl. 15: Pojavljanje vrste Clinitrachus argentatus v slovenskem morju. Glej Sl. 5 za pojasnilo glede velikosti posameznih krogcev.
a rocky environment. They were recorded in dimly lit habitats such as overhanging rocks, where they were dwelling in empty L. lithophaga burrows. The specimens were found at depths from 1 to 10 m. Altogether, 33 specimens were found in 5 UTM quadrants (Fig. 14). The species share the same microhabitat with M. nigri-ceps. The specimens are housed in the ichthyological collection of the MBS: IC-MBP 145.
Family Clinidae
Clinitrachus argentatus (Risso, 1810)
All specimens of this species were observed in shallow waters less than 1 m deep. With the exception of one, the specimens were found in algal cover, such as Cystoseira spp., Halopithys incurva and Dictyota dichotoma. Altogether, 10 specimens were recorded in 8 different UTM quadrants (Fig. 15). The specimens are housed in the ichthyological collection of the MBS: IC-MBP 146.
DISCUSSION
Cryptobenthic fish species are often overlooked due to their cryptic life style (Henriques, 2002). Because they live in heterogeneous environments such as caves, cavities, holes, under stones and clefts, sampling is very demanding. In such cases, anaesthetics such as Quinaldine, proved to be helpful in facilitating the collection of specimens.
Among the 11 cryptobenthic species found in Slovenian coastal waters, two species of the family Gobiidae, T. macrolepis and C. quadrivittatus, were observed for
the first time in Slovenian territorial waters in recent years. Marceta (1999) mentioned at least one finding of C. quadrivittatus near Trieste, and that considered it as an expected species for the adjacent Slovenian waters. T. macrolepis and C. quadrivittatus were both recorded in the nearby Kvarner area, as well (Ahnelt & Kovacic, 1997; Kovacic, 1997, 2005). T. macrolepis was often overlooked in the past, probably not only due to its cryptic lifestyle, but also because it occurs in deeper environments (Miller, 1986; Bilecenoglu & Yokes, 2016). These new observations indicate that the species is more widespread than it was previously assumed (Kovacic, 2005; Bilecenoglu & Yokes, 2016). According to Bilecenoglu & Yokes (2016), the species appears on sediments near small caves, sloping rocky bottoms and coralligenous grounds, where it hides when divers try to approach. C. quadrivittatus was also often overlooked in the past, but new findings show that it is more widespread than previously assumed (Ahnelt, 1990, 1991; Kovacic, 2005, 1997). Specimens are rarely found, and it is presumed that they are not numerous (Ahnelt, 1991). The species occurs in shallow waters, often in tide pools, where it hides under stones (Ahnelt, 1990, 1991).
Among cryptobenthic fish fauna in Slovenian waters, gobies are represented with the highest number of species (Tab. 1), which is in accordance with the results obtained for nearby areas, as reported in many studies (Kovacic, 1997; Kovacic et al., 2012; Glavicic et. al., 2016). Clingfishes were by far the most numerous cryptobenthic fish. L. lepadogaster was the most numerous species (n = 237), followed by A. incognitus (n = 202) and L. candolii (n = 173). These 3 species represent 76.7% of all observed cryptobenthic specimens, but the number does not reflect the actual density of fish species, as they were sampled with the highest effort.
Two species - C. quadrivittatus and L. lepadogaster - occurred only in rocky environment, where they were hiding under stones. Species as T. ephippiatus and T. macrolepis require a specific rocky habitat type with caves and cavities of steep rock faces (Miller, 1986; Kovacic, 1997). Probably, as regards Slovenian waters, this type of habitat is only found in the Natural Monument Cape Madonna protected area, where the species were in fact recorded. Moreover, this restricted area is inhabited by high number of cryptobenthic fish species per UTM quadrant, as well. This is in accordance with Lipej et al. (2003), who reported on the correlation between the high diversity of a fish assemblage and the diversity of habitat types in this area. Similar dimly lit habitats, such as overhanging rocks, are also important habitats for two syntopical sciaphilic blennies, M. nigriceps and P. zvonimiri, which generally hide in precoralligenous formations and dwell in empty L. lithophaga burrows (lipej et al., 2005; Orlando-Bonaca & Lipej, 2008; Lipej et al., 2016b). The presence of three other cryptobenthic species, L. candolii, M. macrocephalus and Z. zebrus,
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are not related only to rocky environment, but were also observed in seagrass meadows where they were hiding under shells and other objects on the sea bottom. C. argentatus also occurs in rocky environment, but it is the only species that is strongly associated with a dense macroalgal belt (e.g. Cystoseira spp.), which provides shelter to this species (Orlando-Bonaca & Trkov, 2016). Santin (2008) reported that the removal of canopy forming algae did not affect the structure of cryptic fish assemblages, but we believe this result does not apply to C. argentatus.
Regarding depth distribution, three species, C. argentatus, L. lepadogaster and C. quadrivittatus, occur only in very shallow waters, mostly less than 2 m deep, while Z. zebrus also occurs in slightly deeper areas (down to 3 m). As tidal amplitude is around ± 90 cm in this part of the Adriatic (Janekovic & Kuzmic, 2005; Cosoli et al., 2013), tidal dynamics have a big impact on the distribution of these species. With the exception of C. argentatus, which probably withdraws to deeper water at the low tide, the other 3 mentioned species can also be found in tide pools in the lower mediolittoral. The occurrence of Z. zebrus and C. quadrivittatus in tide pools has already been reported by some authors (e.g. Ahnelt, 1990, 1991; Nieto & Alberto, 1992). Other species, such as M. macrocephalus, L. candolii and A. incognitus, were mostly present in deeper waters in the infralittoral belt (depth range from 1 to 7 m). The presence of M. nigriceps and P. zvonimiri is mainly related to the availability of suitable hiding habitats, which occur deeper on the sea bottom (depth range from 1 to 10 m). Overall, T. ephippiatus and T. macrolepis were observed in the deepest areas, which is in accordance
with (Miller, 1986), who stated that other species from this genus also prefer habitats somewhat deeper than other gobiid species.
Unlike the rocky environment, the sedimentary environment is much poorer in number of cryptobenthic fish species (Tab. 2). In the shallowest part of the sedimentary coast, no cryptobenthic fish species were observed, probably due to the lack of hiding places, which is related to the low spatial heterogeneity of this habitat. Deeper on the sedimentary bottom, where seagrass meadows appear, 4 cryptobenthic fish species were recorded. L. candolii, M. macrocephalus and Z. zebrus, also found on the rocky bottom, were present in seagrass meadows too. Only A. incognitus showed a strong preference for seagrass meadows, where it occupies seashells, which is in accordance with the conclusions of Hofrichter & Patzner (2000). The latter researchers also observed juvenile and subadult specimens of A. incognitus on seagrass leaves and under sea urchins. Unlike Horichter & Patzner (2000), we did not observe any cryptobenthic fish under sea urchins.
Cryptobenthic fish were found only down to a depth of 10 m, since in deeper waters the bottom is mainly sedimentary and there is a lack of cryptic habitats. This is also the reason why cryptobenthic species were found only in the quadrants located near the coast. Shallow waters and the lack of cryptic habitats on sedimentary bottom, are probably the main reasons for lower species richness and absence of some species compared to the results of other authors (e.g. Kovacic, 1997; Patzner 1999; Kovacic et al., 2012; Glavicic et al., 2016). In our research, stones (5 species; Tab. 2.) were the most common hiding place in the rocky environment, followed by
Tab. 2: Hiding places occupied by cryptobenthic fish species. Tab. 2: Skrivališča kriptobentoških vrst rib.
	Stones and rocks	Precoralligen with endolithic burrows*	Overhanging rocks*	Seagrass meadows**	Dense algal belt
Lepadogaster lepadpgaster	+	-	-	-	-
Lepadogaster candolii	+	-	-	+	-
Apletodon incognitus	-	-	-	+	-
Cliniceps argentatus	-	-	-	-	+
Chromogobius quadrivittatus	+	-	-	-	-
Millerigobius macrocephalus	+	-	-	+	-
Zebrus zebrus	+	-	-	+	-
Thorogobus ephippiatus	-	-	+	-	-
Thorogobus macrolepis	-	-	+	-	-
Microlipophrys nigriceps	-	+	-	-	-
Parablennius zvonimiri	-	+	-	-	-
cavity beneath boulders*, seashells**
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overhanging rocks (4 species), which is in accordance with the results published by Kovacic (1997). Within seagrass meadows, seashells seem to be an important microhabitat, since 3 cryptobenthic fish species were observed using them as a hiding place.
Clearly, the results show that cryptobenthic species richness is much higher on the rocky coast than on sedimentary bottoms, due to the higher spatial heterogeneity of the first environment. Santin et al. (2005) reported that rugosity, as a qualitative measure of habitat complexity, is important for explaining the variability in cryptic assemblages, underlining the importance of hiding places for the occurrence of cryptobenthic fish. Certain epi-benthic fishes, such as other gobies (Gobius cruentatus, G. cobitis, G. paganellus) and blennies (Microlipophrys canevae, Parablennius incognitus) were found in similar hiding places. Kovacic (1997) also reported on similar observations of hiding non-cryptobenthic fish species in cryptic habitats, leading to interspecific competition for space, which is well-known for blennies (Goldschmid & Kotrschal, 1981; Koppel, 1988).
Up to now, 243 fish species have been confirmed in the Slovenian sea (Lipej & Orlando-Bonaca, 2019). Based on that, cryptobenthic fish species represent 4.5% of fish fauna in the Slovenian sea and 5.3% in term of bony fish species. A comparison between cryptobenthic fish fauna lists produced by other northern Adriatic authors (Kovacic, 1997, 8 species; Kovacic et al., 2012, 6 species; Santin et al., 2005, 17 species) can be misleading as some species of epibenthic fish were considered as cryptobenthic by certain authors
(Santin et al., 2005), while for some fish species, such as P. zvonimiri, classification differs between authors (e.g. Illich & Kotrschal, 1990; Kovacic et al., 2012). In this research, P. zvonimiri and M. nigriceps, were considered as cryptobenthic species, as they occupy empty L. lith-ophaga burrows and inhabit dimly lit habitats. However, based on the published literature (e.g. Kovačič, 1997; Horichter & Patzner, 2000; Kovacic et al., 2012; Brandl et al., 2012) dealing with the occurrence of cryptobenthic fish species in the northern Adriatic, and new sampling techniques, other species are expected to be found in Slovenian waters in the future. This could be the case for two clingfish species, such as Opeatogenys gracilis (Canestrini, 1864) that is expected to be found in seagrass meadows, and Gouania willdenowi (Risso, 1810) that could be detected in a rocky environment on gravel beaches (gravel size 0.2 - 2 cm).
ACKNOWLEDGMENTS
We would like to express our gratitude to Žiga Dobrajc, to whom we dedicate this contribution. Special thanks go to Dr. Jurgen Herler, who helped us in studying coastal fish assemblages in Slovenian coastal waters in the summer of 2001. We are thankful to Milijan Šiško for his assistance and support in the preparation of the maps. Last but not least, we would like to thank Tihomir Makovec, Samo Alajbegovic, Borut Furlan, Valter Žiža and Marjan Richter, who contributed important findings and thus to the knowledge of cryptobenthic fish assemblages.
MORSKA KRIPTOBENTOŠKA FAVNA RIB SLOVENIJE (SEVERNI JADRAN)
Domen TRKOV
Marine Biology Station, National Institute of Biology, Piran, Fornače 41, 6330 Piran; Jožef Stefan International Postgraduate School, Jamova cesta 39, 1000 Ljubljana, Slovenia
e-mail: domen.trkov@nib.si
Borut MAVRIČ, Martina ORLANDO-BONACA & Lovrenc LIPEJ
Marine Biology Station, National Institute of Biology, Piran, Fornače 41, 6330 Piran
POVZETEK
Kriptobentoška ribja favna je ena izmed najmanj raziskanih ribjih skupin v Jadranskem morju. V slovenskih obalnih vodah je bilo do danes le nekaj objavljenih prispevkov, ki navajajo kriptobentoško ribjo skupnost. V pričujočem prispevku avtorji navajajo vse razpoložljive podatke o kriptobentoških ribjih vrstah s posebnim poudarkom na njihovo geografsko in globinsko razširjenost. Skupno je bilo zbranih 798 primerkov, ki pripadajo 11 različnim vrstam. Vrsti Thorogobius macrolepis in Chromogobius quadrivittatus sta bili v slovenskih vodah odkriti šele pred kratkim. Večina rib je bila potrjenih z novimi vzorčevalnimi tehnikami, povezanimi z avtonomnim potapljanjem in z uporabo narkotičnega sredstva Quinaldine.
Ključne besede: kriptični habitati, ribja skupnost, obalne vode, severni Jadran
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received: 2018-11-20	DOI 10.19233/ASHN.2019.08
SPATIAL AND TEMPORAL DISTRIBUTION OF ANCHOVY (ENGRAULIS ENCRASICOLUS) AND SARDINE (SARDINA PILCHARDUS) EGGS IN SLOVENIAN TERRITORIAL WATERS (NORTHERN ADRIATIC)
Polona PENGAL
REVIVO, Institute for ichthyological and ecological research PE Ljubljana, Staretova 1, 1233 Dob, Slovenia
e-mail: polona.pengal@ozivimo.si
Eva HORVAT
REVIVO, Institute for ichthyological and ecological research, Šmartno 1 72, 2383 Šmartno pri Slovenj Gradcu, Slovenia
e-mail: eva.horvat@ozivimo.si
Mihael J. TOMAN
Department of Biology, Biotechnical faculty of University of Ljubljana, Jamnikarjeva ulica 101, 1000 Ljubljana, Slovenia
e-mail: mihaeljozef.toman@bf.uni-lj.si
ABSTRACT
Sardine ("Sardina pilchardus) and anchovy (Engraulis encrasicolus) have an important ecological role and are commercially the most important small pelagic species in the Adriatic. In the northern Adriatic Sea sardine and anchovy stocks are overexploited and in overexploitation. Understanding the ecology of these stocks through time is of crucial importance for their sustainable management. In the present work we recognized the most important sardine and anchovy spawning areas and periods in Slovenian territorial waters. Sampling was performed once a month for one year (August 2014-July 2015) at 10 sampling stations, evenly distributed around the Slovenian territorial waters following the Daily Egg Production Method (DEPM) protocol. Despite of low winter temperatures sardine eggs were recorded from September to April, with two spawning peaks, in November and February. The highest number of sardine and anchovy eggs were recorded in the north-western part of the Slovenian territorial waters and in the Koper Bay. Anchovy eggs were recorded from May to November, with the spawning peak in August.
Key words: small pelagic, anchovy, sardine, spawning season, fish eggs, northern Adriatic Sea
DISTRIBUZIONE SPAZIALE E TEMPORALE DI UOVA DI ACCIUGA (ENGRAULIS ENCRASICOLUS) E SARDINA (SARDINA PILCHARDUS) IN ACQUE TERRITORIALI SLOVENE (ADRIATICO SETTENTRIONALE)
SINTESI
La sardina (Sardina pilchardus) e ¡'acciuga (Engraulis encrasicolus) hanno un importante ruolo ecologico e sono le specie pelagiche commercialmente più importanti dell'Adriatico. Nell'Adriatico settentrionale le scorte di sardine e acciughe sono sovrasfruttate e in sovrasfruttamento. Comprendere í'ecoíogia di questi stock nel tempo è di cruciale importanza per la loro gestione sostenibile. Nel presente lavoro abbiamo riconosciuto le più importanti aree e periodi di deposizione delle sardine e delle acciughe nelle acque territoriali slovene. Il campionamento è stato eseguito una volta al mese per un anno (agosto 2014-luglio 2015) in 10 stazioni di campionamento, distribuite uniformemente nelle acque territoriali slovene, seguendo il protocollo del metodo di produzione giornaliera dell'uovo (DEPM). Nonostante le basse temperature invernali, le uova di sardine sono state ritrovate da settembre ad aprile, con due picchi di deposizione delle uova in novembre e febbraio. Il numero più elevato di uova di sardine e acciughe è stato registrato nella parte nord-occidentale delle acque territoriali slovene e nella baia di Capodistria. Le uova di acciuga sono state ritrovate da maggio a novembre, con il picco di deposizione delle uova nel mese di agosto.
Parole chiave: piccolo pelágico, acciuga, sardina, stagione della deposizione delle uova, uova di pesce, Adriático settentrionale
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INTRODUCTION
Sardine (Sardina pilchardus; Walbaum, 1972) and anchovy (Engraulis encrasicolus; Linnaeus, 1758) dominate the pelagic environment in the northern and central Adriatic Sea and have a wide impact on its trophic web (Morello et al., 2009). These small pelagic stocks also provide high economic yields for the fisheries sector of all countries around the Adriatic Sea. Coordinating and aligning interests and efforts among countries with such differences in economic and social importance of fisheries on the national level is complicated. For these reasons different management measures are difficult and slow to be implemented and meanwhile small pelagic stocks remain overexploited (COM, 2017). To understand and to be able to predict stock development through time, different stock assessment methods are continuously being developed and data are collected through scientific surveys as well as from the fisheries.
Daily Egg Production Method (DEPM) was developed in the late 1970s in California and has since been applied to several European anchovy stocks in the Mediterranean Sea (Alheit, 1993; Somarakis et al., 2004; Mandic et al., 2015). An important contribution that enabled application of the DEPM method to the Adriatic anchovy stock was that of REGNER (1985), who determined the developmental parameters of anchovy in the Adriatic Sea. Following from his research, the DEPM protocol for the small pelagic species of the Adriatic Sea has recently been developed in the framework of the AdriaMed project (Mandic et al., 2014). According to the DEPM protocol, the full extent of the species' spawning area should be surveyed to enable valid stock assessment with this method Somarakis et al., 2004.
Anchovy and sardine have mirror like reproductive strategies and oceanographic parameters - especially salinity and temperature - are of crucial importance in explaining the coexistence of the two species (Morello et al., 2009). Stirn et al., (1974) pointed out that this two species have more or less spatially competitive relationship. When considering geological timescale it seems that abundant population of anchovy, inhabiting energetically rich western waters of Northern Adriatic and high food plasticity in sardine, who probably had to adapt to remaining available habitats, points out one of the clues that there is a competitive relationship among adult fish for feeding areas (Morello et al., 2009). Stirn et al., (1974) noticed that in late spring, when sardine is still spawning and anchovy is migrating to the north and starting to spawn, areals of both species are not overlapping. This spatial separation in spring is visible also in distribution of their eggs (Stirn et al., 1974). In winter, adult sardines migrate southwards from feeding areas such as Gulf of Trieste, Venice and Istrian coast, towards island Dugi Otok for spawning (Morello et al., 2009; Skrivanic et al., 1973). On the contrary, the main anchovy spawning activity takes place in warmer
months in the offshore waters of island Dugi Otok towards the coastal Istrian waters (Morello et al., 2009) and the coastal waters between the Gulf of Trieste and the Gargano peninsula, with the highest abundance of eggs in the Gulf of Trieste and off the mouth of the river Po (Morello et al., 2009; Regner, 1996). Therefore, we expected Slovenian coastal territorial waters to be an important spawning ground for anchovy, but only of minor importance for sardine spawning.
Developmental time of anchovy and sardine eggs depends on temperature and is shortest during warmer water temperatures (Regner, 1987, 1996) minimizing exposure time of the most vulnerable, egg developmental stage. In such conditions egg sizes are smaller, since there is need to provide safety and nutrition to the embryo for much shorter time in such conditions (Riveiro et al., 2004). In addition, smaller eggs have been observed later in the spawning season, when first year individuals tend to spawn (Regner, 1985). In view of this knowledge, we would expect sardine and anchovy eggs to be larger when their first spawning in the year occurs and when environmental conditions are not yet the most suitable. The eggs should be smallest during peak spawning and medium sized to large towards the end of the spawning period when environmental conditions are becoming less suitable.
In view of this knowledge, we would expect sardine and anchovy eggs to be larger when their first spawning in the year occurs and when environmental conditions are not yet the most suitable. The eggs should be smallest during peak spawning and medium sized to large towards the end of the spawning period when environmental conditions are becoming less suitable, which is also in line with results of anchovy egg developmental stage duration in Boka Kotarska Bay in Montenegro (Mandic. 2011).
As a partner of the AdriaMed project, Slovenia is contributing to development and application of the DEPM for the stock assessment of small pelagic fish in the Adriatic Sea (Pengal et al., 2014). Therefore, the initial spatial study of egg distribution performed in August 2014 and supported by the AdriaMed project was extended by ZZRS (Fisheries Research Institute of Slovenia) to also gain insight into temporal distribution of spawning for both small pelagic species in Slovenian coastal territorial waters. Thus, this study provides results of the spatial and temporal distribution of spawning for sardine and anchovy in Slovenian territorial waters.
MATERIAL AND METHODS Location and sampling
The studied area is situated in the southern part of the shallow Gulf of Trieste, which is the northernmost part of the Adriatic Sea (Fig. 1). Larger part of the gulf belongs
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to the infralittoral zone with typical flat muddy bottom, composed of clayey silt (Ogorelec et al., 1991), while other the rest of the habitat types are limited to small dispersed areas (Lipej et al., 2006). Slovenian territorial waters (studied area) is extremely shallow, with mean depth of 18.7 m (Ogrin, 2012). Because of its shallow nature with a mean depth of 35 m, northern Adriatic is extremely productive, but becomes hydrographically unstable and subjected to environmental variability during winter (Stirn, 1968).
In all the seasons there is a general inflow into the Gulf of Trieste at its south-eastern, deeper part, while the outflow appears along the gulf's axis near the sea surface and is driven by the dominant ''bora'' wind during winter. The surface layer of the Gulf of Trieste is dominated by seasonal winds and typical (anti)cyclonic circulations formed in different seasons, suggesting lower current speeds in the central part of the Gulf (Zavatarelli et al., 2003; Malacic et al., 2009). Stronger currents are typical near the capes such as Cape Madona in Piran (Ogrin, 2012).
Sampling was performed for twelve months from August 2014 to July 2015 on ten sampling stations, positioned app. 3 nautical miles apart in the Slovenian territorial waters. Due to adverse weather conditions sampling was impossible to perform in October and in January on stations 6 to 10. Sampling stations were reached by a boat of ZZRS and exact locations found with a handheld GPS unit.
The Daily egg production method (DEPM) protocol (Mandic et al., 2014; Pengal et al., 2014) was followed and sampling was conducted using WP2 net with mesh size of 200 |jm and mouth diameter of 0,264 m2. The net was towed from 5 m above the bottom to the surface with a hauling speed of 1 m/s. The samples were immediately preserved in 3 % solution of buffered formaldehyde and analysed at the Department of Biology at the Biotechnical Faculty of University of Ljubljana.
At each sampling station water temperature [°C], salinity, oxygen levels [mg/L] and dissolved oxygen [%] for each meter of the water column were measured by means of a Hatch CTD probe (Horvat, 2017). In August, November and December, salinity measurements were not collected at all sampling stations due to probe failure. Therefore, salinity of peak spawning for anchovy (August) was estimated using July data.
Mean monthly air and water temperatures for each month were also collected from Slovenian Environmental Agency (ARSO; Strojan, 2014a, b, c; Strojan, 2015 a, b ,c, d, e). Speed and direction of currents were gained from the stainless-steel buoy "Vida" (45° 32' 55,68'' N, 13° 33' 1,89'' E), where an AWAC current meter from Nortek As is mounted at the seafloor, at the depth of 22 m. Additionally, the direction of wind was collected from Vida (NIB, 2017) during sampling of each station. For sampling stations 1, 5, 6, 7, and 8 Chlorophyll-a concentrations [jg/L] were obtained
Fig. 1: Geographic position of ten sampling stations (1 - 10) in Slovenian territorial waters inside the Gulf of Trieste.
Sl. 1: Enakomerna razporeditev desetih vzorčnih postaj (1 - 10) v teritorialnih vodah Slovenije (Tržaški zaliv).
from the Slovenian Environmental Agency for months August (2014)-January (2015) and June-July (2015) (Sever, 2016).
Analysis
Sardine and anchovy eggs were sorted from the samples and counted in the laboratory. Eggs were then measured with the program CellSense Standard under the microscope (Olympus Cx41) with 10 X 4 magnification. Eleven egg developmental stages and 5 developmental classes (A-E) were determined for sardine eggs following the proposal of the General Fisheries Council for the Mediterranean (karlovac, 1967; GFCM, 1975). Ten developmental stages were determined for anchovy eggs according to Regner's templates from AdriaMed Training Course (REGNER, 1985). Additional literature Re et al., (2009) and Mandic (2011) was referenced to determine the ages of sardine eggs. Regner's (1985) formula for developmental time and mean correction time were used to calculate the spawning interval.
Monthly abundance of sardine or anchovy eggs per m2 were calculated for each sampling station using Tan-aka's formula (Regner, 1985; Regner et al., 1987). Since sardine and anchovy eggs were only found at a small number of stations (less than 50 %) in most months, the empty stations were omitted from the calculation of mean monthly abundance of eggs per station (as per Karlovac (1964) and Mandic (2011)). Finally, categorization by Karlovac (1964) was used to determine the spawning intensity category for the survey area. Information on length of adult sardine and anchovy fish that were caught in Slovenian territorial waters during our survey were retrieved from the database of the Fisheries Research Institute of Slovenia (ZZRS).
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RESULTS
In total, 1646 eggs were collected, of which 68 were sardine, 951 anchovy and 627 were unidentified eggs belonging to other species. Of those, 3 sardine and no anchovy eggs were found during the incomplete January sampling and these eggs were omitted from the analysis (Fig. 2). Moreover, 34 anchovy and 3 sardine eggs were damaged so that it was impossible to determine their developmental stage or measure them. These eggs were used for the calculations of abundance, but not for the other analysis.
Abiotic parameters
The water depth at sampling stations ranged from 18 to 25 m. With the exceptions of May and August, there was no clear stratification of the water column during our sampling, data is in more detail presented in Horvat (2017). Temperature in the water column was gradually decreasing towards the bottom in the summer months without a clear thermocline (Fig. 3). On the contrary, salinity was lowest on the surface and gradually increasing towards the bottom, with an exceptionally strong pycnocline with a pronounced low surface salinity layer in November, when the sampling was performed after a rainfall event and freshwater lingered on the surface for a few days. The only month with the mean water column salinity below 38 was May.
Persistence of low oxygen levels in the bottom layer was detected throughout the summer months, from July to the end of September at most sampling stations. Oxygen content was high throughout the water column during the winter months.
Sardine
The highest abundance of sardine eggs and persistence were detected at stations 6 and 7 located towards the central part of Gulf of Trieste and the Koper Bay (Tab. 1). No sardine egg was found in the samples from station 3 in this survey and only individual eggs were identified at the neighbouring stations 2 and 4, which are located off the Savudrija cape. Low presence of sardine eggs was also determined for stations closest to the shore. Higher abundances were calculated for station 10, just off the Cape Madona, the deepest part of the Slovenian territorial waters.
The eggs occurred in the sampling area from September to April with the first spawning peak in November and a second, lower spawning peak detected in February (Fig. 4a). Medium sardine spawning intensity was determined for the earliest occurrence of sardine eggs in Slovenian territorial waters in late September with a mean of 11 eggs/m2. In November, mean abundance of 19 eggs/m2 was found in the sampling area, which indicates Slovenian territorial waters as an area of strong spawning intensity for sardine. Mean water column temperature at peak spawning was 17.84 °C and salinity 37.97. During the second abundance peak in February sardine eggs were found at five sampling stations (6-10) with on average 8 eggs/m2 which corresponds to a low intensity spawning event. The lowest mean water column temperature (9.76 °C) and the highest salinity (38.39) during the survey were recorded for this sampling. The latest occurrence of sardine eggs in Slovenian
July	November
Salinity	Salinity
35 36 37 38	35 36 37 3K 39
Fig. 2. Total number of sardine and anchovy eggs found in the samples from all stations by month with surface (Surf) and mean water column (WC) temperatures (temp) and salinities (sal).
Sl. 2: Skupno število iker sardele in sardona iz vseh vzorčnih postaj, predstavljeno po mesecih, vključno s temperaturo površinske vode (Surf) in povprečno temperaturo vodnega stolpca (WC) in slanostjo (sal).
Fig. 3. Water temperature, salinity and oxygen profiles as a mean of all stations during peak spawning of anchovy (July; see Materials and methods) and sardine (November).
Sl. 3: Povprečne vrednosti vodnega stolpca vseh vzorčnih postaj za temperaturo, slanost in kisik tekom viška drsti sardona (julij; glej Material and methods) in sardele (november).
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territorial waters was determined for April (on average 4 eggs/m2).
The minimum egg developmental time (38.78 hours) for any station during our survey was calculated at station 8 in September and the maximum (137.01 hours) at station 6 in February. The shortest mean developmental time (39.21 hours) for sardine eggs was determined for September and the longest for February (128.25 hours; Fig. 4a), while in November it was the second shortest (51.80 hours).
Eggs stages B and C were detected in most samples, whereas stages A, D and E occurred only occasionally. Stage A was detected only in February, stages B and C from September to April and stage D in September and November. Stage E was never recorded.
Sardine eggs collected during this survey varied in size from 1.30 (in December) to 1.90 mm (in February; Fig. 4b). The smallest mean egg sizes were calculated for the autumn samples September (1.50 +/- 0.08 mm), November (1.55 +/- 0.09 mm) and December (1.54 +/- 0.02 mm). The largest mean egg sizes were detected in February (1.73 +/- 0.01 mm). Furthermore, the eggs containing the smallest oil drops were collected in September (mean of 0.15 +/- 0.03 mm) and the largest in February (mean 0.21 +/- 0.05 mm).
Anchovy
The highest abundance of anchovy eggs in the survey area were consistently detected at stations from 5 to 9, located towards the central part of the Gulf of Trieste and the Koper Bay (Tab. 1). The abundance decreased towards the mouth of the Gulf as well as towards the shore. Furthermore, stations 6-9 exhibited 100% persistence during the spawning season, with eggs being
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S. 4: Številčnost iker, razvojni čas (a), povprečni premer vseh iker in oljne kapljice (b) po vzorčnih postajah in mesecu drsti sardele.
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detected at these stations each month from May to November. We recorded the lowest abundances as well as persistency at station 3. Only during peak spawning in August anchovy eggs were present at all stations.
Anchovy eggs were detected in planktonic community of the Slovenian territorial waters between May and November, with the peak spawning recorded in August (Fig. 5a, Tab. 1). When the season's earliest anchovy eggs were identified in May at stations 3-10 (on average 30 eggs/m2), mean water column temperature for these stations was 16.8 °C and salinity 37.57. The calculated abundance of anchovy eggs during peak spawning in August ranged from 8 eggs/m2 at station 3 to 629 eggs/ m2 at station 9. However, the mean abundance of eggs for this period was 189.77 eggs/m2. During peak spawning the mean water column temperature at positive stations was 23.75 °C and salinity around 38.09 (see Materials and Methods). Spawning intensity and persistence gradually decreased from September (94 eggs/m2) to November, when the lowest egg abundances were detected (19 eggs/m2) at stations 6-9.
Based on the temperature measurements, the mean developmental time for eggs was shortest in August (31 hours) and longest in May (72 hours). Most eggs from
August samples were determined to be in stages IV and V (70.94 % of all eggs), which corresponds to highest spawning intensity between 1:00 and 2:30 o'clock in the night (Fig. 6). Furthermore, 93 % of eggs found in August samples were spawned between 21:00 in the evening and 8:00 in the morning.
The minimum length of anchovy eggs in the samples from Slovenian territorial waters was 1.07 mm and the maximum was 1.52 mm (Fig. 5b). The smallest mean egg sizes (length: 1.20 +/- 0.02 mm; Fig. 5b) were calculated for samples collected during the abundance peak in August. On the contrary, eggs were largest (length: 1.40 +/- 0.02 mm) towards the beginning and end of the spawning season.
DISCUSSION
As suggested by Regner (1985) temperature and salinity seem to be the most important factors determining spawning period and limiting spawning area of the small pelagic species in the Adriatic.
No significant correlation was found between abiotic (temperature, salinity, chl-a, ...) and biotic (egg abundance, size, occurrence,.) parameters, so the PCA
Fig. 5 Abundance of eggs, developmental time (a), mean egg length (b) by month for each sampling station during the spawning period for anchovy.
Sl. 5: Številčnost iker, razvojni čas (a), povprečna dolžina iker (b) po vzorčnih postajah in mesecu drsti sardona.
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results are not presented in this article. The lack of correlation is attributable to the small surface, low depth and stable conditions of the Slovenian territorial waters, lacking the required diversity for such analysis.
Our findings confirm past findings (Stirn, 1968; Stirn et al., 1974; Morello et al., 2009) with anchovy spawning mainly during warmer months (Stirn, 1968; Stirn et al., 1974; Morello et al., 2009) in Slovenian territorial waters. In spring, the last sardine eggs were detected in April and the first anchovy eggs were found in May, completely separating spawning periods of the two species. In autumn, on the other hand, spawning periods were overlapping from September to November, when eggs of both species were found in the samples. The prolonged spawning of anchovy till November was recorded in 2014, which is a usual spawning period for central and southern Adriatic (Zavodnik, 1970; Regner, 1972; Morello et al., 2009; Mandic, 2011) but not for the Northern Adriatic (Stirn, 1968; Stirn et al., 1974; Morello et al., 2009). We assume that one of the reasons might be the persistence of unusually high November mean sea water temperatures when comparing it to the mean November sea temperatures since 1981 at the Measurement station Koper (Strojan, 2014b). High abundances of anchovy eggs were still detected in the September samples, but low numbers collected in November were indicating the end of the spawning period. On the contrary, only individual sardine eggs were found in September samples and the first spawning peak was determined in November. The relatively low abundance of sardine eggs in September could be attributed to the numerous presence of anchovy who is more abundant and, thus, dominant in the area (Stirn, 1986). On the other hand, Slovenian territorial waters also represent the marginal area of sardine spawning range due to extreme environmental conditions during winter (Stirn, 1968, Gacic et al., 1997; Shaltout et al., 2014).
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Sl. 6: Številčnost iker sardona (N/m2) z "za nazaj" preračunanim časom drsti med viškom drsti v avgustu.
Sardine
The distribution of sardine eggs detected in this survey confirms the highest density of sardine eggs in the central open waters of the Gulf of Trieste. The abundance of eggs declines towards the entrance to the Gulf and towards the shores. Recent studies of currents in the Gulf of Trieste (Bogunovic et al., 2008) suggest that direction and speed of sea currents are the major reason for the described distribution of eggs. On the other hand, the average age for all sampled sardine eggs was approximately 16 hours at the time of sampling and considering the regular occurrence of strong winds and marine currents in the Gulf during winter time (Ogrin, 2012), the areas identified may not represent the actual spawning grounds.
The low absolute number of sardine eggs detected in this survey agree with other studies conducted in the northern Adriatic which found the spawning intensity in this area consistent with a periphery of the main sardine spawning grounds (Regner et al., 1987; Stirn, 1968). Contrary to Stirn (1968), we can confirm sardine spawning in the Gulf of Trieste despite the low temperatures during winter. Sardine spawn with strong intensity in November as well as with medium intensity in September, December and February (Karlovac, 1964). Considering the trends observed, it is reasonable to conclude that spawning occurred also in October and January in Slovenian territorial waters. We predict that spawning intensity in October and January would also fall at least within the medium intensity category, if sampling was feasible during our survey.
Sardine eggs occurred in the survey area when mean water column temperature ranged from 9.20 to 22.00 °C and salinity range from 36.70 to 39.00. The first spawning peak in November was characterized by mean water column temperature of 17.77 °C and salinity around 37.80, calculated at stations where sardine eggs were found and salinity was around 37.80 (see Material and Methods).
According to previous research (Morello et al., 2009; Regner et al., 1987; Stirn, 1968), environmental conditions for peak spawning of sardine during this survey were the most suitable in January, when we also assumed the spawning peak would occur. Unfortunately, unsuitable weather conditions only allowed us to sample stations 1 to 5 and 10 in this month. Thus, the stations with otherwise highest abundances of eggs observed were not sampled and so the abundance is not comparable with other sampling months. Therefore, we allow the possibility that the highest sardine spawning peak in Slovenian territorial waters occurred in January.
The eggs recorded in this study were generally larger than those recorded by Mandic et al., (2014) in Boka Kotorska Bay (Montenegro), suggesting that conditions for sardine spawning in the Gulf of Trieste are less suitable. Furthermore, the largest sardine eggs were found in
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February and March, which can be partly explained by least favourable environmental conditions (low sea temperatures and salinity). Adults were not sampled during our survey and there is a lack of data from Data Collection Framework (DCF) for winter months, so we cannot confirm if length of fish also affected the size of eggs.
It was expected that egg stages D and E would be less frequent in all samples due to high mortality rates, since sampling was done in North Adriatic where, referring to Regner et al. (1987), mortality of sardine eggs and larvae is higher (coefficient of instantaneous mortality: 0.65) is higher than in the mean calculated on the entire Adriatic (coefficient of instantaneous mortality: 0.56). The exceptional occurrence of stage D eggs in November samples could indicate lower predator pressure during that time which is consistent with lower gelatinous plankton densities in northern Adriatic during autumn (Palmieri et al., 2014; Malej et al., 2004). Focused studies should be conducted to understand these dynamics.
Anchovy
The Gulf of Venice and the Gulf of Trieste are known to be the main spawning areas for anchovy in the Adriatic (Gamulin, 1983; Morello et al., 2009). Similar to sardine, we found that anchovy eggs are the most abundant towards the central open waters of the Gulf of Trieste and decline in number towards the shores and entrance to the Gulf. On the contrary to what is shown by sardine, we can conclude and confirm (Štirn, 1968; Štirn et al., 1974; Regner, 1985; Regner et al., 1987; Dulčic, 1995) that these are the actual spawning grounds of anchovy, since the currents are very weak or absent during summer months (Malačic et al., 2009) and the eggs are expected to linger where they were spawned.
During our survey anchovy spawned in Slovenian territorial waters between May and November. The first occurrence of eggs in May was characterized by the mean water column temperature of 16.44 °C and salinity 38.09. While exceptional presence of anchovy eggs until November has been reported in the central and southern Adriatic before (Regner, 1972), this study is the first to confirm occurrence of late, November spawning in the colder northern Adriatic. We assume the prolonged spawning coincided with higher water column temperatures (mean of 17.50 °C) in November during our survey, which were 2.6 °C higher than average (mean of 14.90 °C; Strojan, 2014b).
From abundance of anchovy eggs peak spawning intensity was determined for August, with mean water column temperature 23.75 °C and salinity from 37,40-38, confirming previous findings for northern Adriatic (Štirn, 1968; Regner, 1985). The anchovy spawning intensity gradually increased during the 3 spring months (May-July), exploded in August and finally decreased during the autumn months (Sep-Nov). In line with Regner (1985), this pattern closely followed the observed water column temperature changes. Furthermore, salinity measured
during peak spawning in the Slovenian territorial waters is at the higher end of the previously observed range (28-38.5; Morello et al., 2009; Stirn, 1968).
Moreover, Regner (1985; Morello et al., 2009) observed that anchovy eggs from the open sea are larger than those from the coastal areas such as Gulf of Trieste and Lugovaj (1964; as cited in Regner, 1985) found that salinity also affects egg sizes, which are smaller and more elongated in lower salinities. We can confirm these hypothesis, since the eggs collected during this survey are one of the smallest (0.49-0.56 x 1.17-1.43 mm) recorded in the Adriatic Sea (Lugovaj, 1964; Regner, 1985; Zorica et al., 2014; Mandic, 2011). Length measurements refer to formalin-preserved eggs, no correction of size was performed. In addition, the smaller egg sizes can also be attributed to the smaller size of individuals representing the northern Adriatic anchovy stock (Levi et al., 1994). Adults were not sampled during our survey and there is a lack of DCF data during winter months, so we cannot confirm these relationships for Slovenian territorial waters.
The anchovy daily spawning interval determined in this survey is wider compared to previous studies and shifted towards the early morning hours (peak from 0:30 - 5:00 am; Fig. 6b). In the area of Chioggia (Venice Bay) Varagnolo (1964) reported spawning of anchovy to occur between 18:00-20:00, while Somarakis (2004) assumed anchovy spawn between 22:00 and 2:00 in the Eastern Mediterranean.
For the future surveys, we recommend that since the DEPM application presumes the coverage of entire spawning area, Slovenian territorial waters should be included in the future samplings to avoid underestimation of the SSB. In addition, due to the opposing spawning periods of sardine and anchovy, separate surveys should be performed to collect data, and protection of the spawning grounds for these two species should be managed separately.
CONCLUSIONS
For anchovy the main spawning season occurred in autumn in northern Adriatic, confirming Stirn's findings (1968). However, since predicted climate change could shift the sardine spawning area further north, affecting the current equilibrium with potentially considerable effects on small pelagic fisheries of northern Adriatic, the spawning of these two species should be closely monitored. Future studies should try to predict the impact of climate change on the spawning areas, the consequent change in competitive interaction among these two species and the potential fisheries implications for the Adriatic. Future DEPM studies should also include chlorophyll-a, phyto-plankton and zooplankton measurements, since data are not available and is not a good indicator of production in the Slovenian territorial waters, since heavy maritime traffic causes suspension of the mud throughout the year, distorting this correlation.
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ACKNOWLEDGEMENTS
Research leading to this publication was made possible by the contribution of FAO AdriaMed project and ZZRS who also trusted us the field samples for further identification. Special thanks to Tomaž Modic, Aljaž Jenič and Blaž Cokan for their support and field work. Ron ten Boer identified the eggs in the first months of the survey. Our thanks to Milica Mandic for kindly helping
us with the literature and the identification of eggs. Maja Sever (Slovenian Environment Agency) has generously provided data on chlorophyll-a from Slovenian territorial waters. Prof. Ingrid Catic and prof. Anita Marusic from Institut za oceanografiju i ribarstvo, Split kindly provided the articles from Acta Adriatica. Roman Lustrik and Zan Kuralt kindly reviewed and added constructive comments on QGis figures.
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PROSTORSKO IN ČASOVNO POJAVLJANJE IKER SARDELE IN SARDONA V SLOVENSKEM TERITORIALNEM MORJU
Polona PENGAL
REVIVO, Institute for ichthyological and ecological research PE Ljubljana, Staretova 1, 1233 Dob, Slovenia
e-mail: polona.pengal@ozivimo.si
Eva HORVAT
REVIVO, Institute for ichthyological and ecological research, Šmartno 1 72, 2383 Šmartno pri Slovenj Gradcu, Slovenia
e-mail: eva.horvat@ozivimo.si
Mihael J. TOMAN
Department of Biology, Biotechnical faculty of University of Ljubljana, Jamnikarjeva ulica 101, 1000 Ljubljana, Slovenia
e-mail: mihaeljozef.toman@bf.uni-lj.si
POVZETEK
Glavno obdobje drsti sardona v severnem Jadranu tekom naše raziskave je bilo jeseni, s čimer potrjujemo Štirnova (1968) odkritja. Zaradi pričakovanih klimatskih sprememb lahko pričakujemo, da se bo drst sardele pomaknila proti severnim območjem Jadrana, kar bi lahko vplivalo na trenutno ravnovesje staležev med malimi pelaškimi vrstami rib severnega Jadrana, zato predlagamo podrobnejše spremljanje drsti obeh vrst. V prihodnjih študijah bi bilo priporočljivo na podlagi različnih modelov predvideti kako se bodo spreminjala območja drsti, zaradi njunega kompetitivnega odnosa, in kakšen bo potencialni vpliv teh sprememb na njun ulov znotraj Jadrana. DEPM raziskave bi morale vključevati tudi beleženje zooplanktona, fitoplanktona in klorofila-a, saj se meritve s strani države ne opravljajo redno po celotnem območju teritorialnih voda Slovenije ter niso dober ali dovolj natančen pokazatelj primarne produkcije skozi leto, saj na meritve močno vpliva morski promet (tovorne ladje in križarke), ki povzroča dvig in mešanje sedimenta skozi vse leto.
Ključne besede: male pelaške ribe, sardon, sardela, drst, obdobje drsti, ikre, severno Jadransko morje
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received: 2019-01-24	DOI 10.19233/ASHN.2019.09
OVERVIEW OF TROPHIC LEVELS RECORDED IN TELEOST SPECIES FROM NORTHERN TUNISIAN WATERS (CENTRAL MEDITERRANEAN SEA)
Sihem RAFRAFI-NOUIRA
Unité de Recherches Exploitation des Milieux aquatiques, Institut Supérieur de Pçche et d'Aquaculture de Bizerte, Université de
Carthage, BP 15, 7080 Menzel Jemil, Tunisia
Youssouph DIATTA
Laboratoire de Biologie marine, Institut fondamental d'Afrique noire, (IFAN Ch. A. Diop), Université Cheikh Anta Diop de Dakar, BP
206, Dakar, Senegal.
Christian CAPAPÉ
Laboratoire d'Ichtyologie, case 104, Université de Montpellier, 34 095 Montpellier cedex 5, France
e-mail: capape@univ-montp2.fr
ABSTRACT
This paper reports about the observations made with regard to 21 teleost species comprising 1657 specimens from the northern Tunisian coast. These specimens were found in an area with sufficient prey species to allow them to live and develop, as confirmed by the size to total body weight relationship. The high values of vacuity index are probably due to both sampling and fishing methods. Crustaceans and teleosts are the prey most frequently consumed by these species. Additionally, the high trophic levels (TROPH) (± 3.00) indicated that these teleost species belong among carnivores. Of all the species examined, only one, Sarpa salpa with TROPH = 2.00, was found to be herbivorous.
Key words: Teleost species, trophic level, vacuity index, relation the total length vs the total body weight,
competition for food, Tunisian coast
REVISIONE DEI LIVELLI TROFICI DI SPECIE DI TELEOSTEI IN ACQUE TUNISINE SETTENTRIONALI (MEDITERRANEO CENTRAE)
SINTESI
L'articolo riporta le osservazioni fatte su 21 specie di teleostei comprendenti 1657 esemplari provenienti dalla costa settentrionale tunisina. Gli esemplari sono stati trovati in un'area con una quantità di prede sufficiente per consentire loro di vivere e svilupparsi, come confermato dal rapporto tra le dimensioni corporee e il peso corporeo totale. Gli alti valori dell'indice di vacuità sono probabilmente dovuti sia al campionamento che ai metodi di pesca. Crostacei e teleostei sono le prede più frequentemente consumate da queste specie. Gli alti livelli trofici (TROPH) (± 3,00) hanno inoltre evidenziato che tali specie di teleostei sono carnivore. Di tutte le specie esaminate solo una, Sarpa salpa, con TROPH = 2,00, è risultata erbivora.
Parole chiave: teleostei, livello trofico, indice di vacuità, relazione tra lunghezza totale e peso corporeo totale,
competizione alimentare, costa tunisina
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INTRODUCTION
Fishery and aquaculture are believed to play an important role in Tunisian economy, which explains why studies related to these patterns have been the subject of several papers (see BradaT, 2000; Rafrafi-Nouira, 2016). The entire Tunisian coast, including lagoons, has been continuously investigated since Vinciguerra (1882) to assess, in qualitative and quantitative terms, the status and the biodiversity of local ichthyofauna. Several studies focused on fish species occurring in northern areas (Castany, 1955; Ben Mustapha, 1966; Lubet & Azzouz, 1969; El Kamel-Moutalibi, 2014; Mnasri-Sioudi, 2014; Rafrafi-Nouira, 2016).
The aim of this paper is to point out the interrelationships between fish species caught off Ras Jebel and its closely related areas, and their potential preys. Thus, the trophic levels were determined for some species of commercial interest commonly observed in fish markets. Following Stergiou & Karpouzi (2002), estimation of trophic level plays a major role in monitoring fishery resources and their effect on ecosystems. Additionally, following Froese et al. (2011),
Fig. 1: Map of Tunisia indicating the capture area (rectangle) of 21 teleost species from the northern Tunisian coast. GT: Gulf of Tunis; GH: Gulf of Hammamet; GG: Gulf of Gabès.
Sl. 1: Zemljevid Tunizije z označeno lokaliteto (pravokotnik) ulova 21 vrst kostnic ob severni tunizijski obali. GT: Tuniški zaliv; GH: Hamameški zaliv; GG: Gabeški zaliv.
the size versus total body weight relationship was calculated for each species to point out if they found sufficient food in the wild to live and develop.
MATERIAL AND METHODS
Of the 124 fish species captured in northern Tunisian waters, 21 teleost species were targeted, comprising 1657 specimens sampled for this study between 2010 and 2015. According to the information provided by experienced local fishermen, the specimens were collected throughout the year off the northern and northeastern Tunisian coast, including the Gulf of Tunis (Fig. 1), by commercial fishing vessels using trawl over sandy and muddy bottoms, and gill nets and longlines on rocky bottoms, at depths ranging from 50 to 200 m. Each sampled specimen was identified using books and field guides, such as Whitehead et al. (1984-1986), Louisy (2002) and Quero et al. (2003). All fresh specimens were delivered to the laboratory, where they were measured for total length (TL) to the nearest millimetre and weighed for total body weight (TBW) to the nearest gram.
For each specific sample the Shapiro-Wilk's test of normality was performed, with P < 0.05. The Chi-square test was used to determine significance (P < 0.05). The total length (TL) to total body weight (TBW) relation was used to complement the feeding studies following Froese et al. (2011). This relationship is TBW = aTLb, and was converted into its linear regression, expressed in decimal logarithmic coordinates, and correlations were assessed by least-squares regression. Like so: log TBW = log a + b log TL. Significance of constant b differences was assessed to the hypotheses of isometric growth if b = 3, positive allometry if b > 3, and negative isometry if b > 3 (Pauly, 1983). Comparison of means was carried out using ANOVA. These two latter tests were performed using the STAT VIEW 5.0 logistic model.
Once the fresh specimens were collected, their stomach contents were immediately removed by dissection, sorted and identified to the lowest taxonomic level (species level where possible), using taxonomic keys and field guides (Perrier 1964, 1975, Louisy, 2002). The prey items were counted and weighed to the nearest decigram after removal of surface water by blotting them with tissue paper. When prey items found in the stomachs were incomplete, the prey count was based on the number of different typical parts, such as beaks for cephalopods, claws and legs for crustaceans, carapaces for decapod crabs, shell and foot for bivalves, operculum and shell for gastropods, and the whole vertebral column and otoliths for teleost species. We assumed two or more prey species if the legs of crustaceans were different in size and shape, and a single prey species if they were very similar. The same methodology was used for determining vegetal preys. Preys not identified in the laboratory were preserved in 10% buffered formalin to be subsequently examined by specialists.
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The analyses of food composition and feeding habits of these 21 species were based on the following indices suggested by Hureau (1970), Hyslop (1980) and Rosecchi & Nouaze (1987). The food composition and feeding habits of C. conger were studied using the following indices suggested by Hyslop (1980):
•	Vacuity Index, VI = number of empty stomachs/ total number of stomachs x 100;
•	Mean number of prey per stomachs: MN = total number of prey ingested/total number of full stomachs;
•	Percentage of numerical abundance: %N = (number of prey item i/total number of prey) x 100;
•	Percentage in weight: %W = (weight of prey item i/total weight of all prey) x 100;
•	Percentage of frequency of occurrence: %F = (number of stomachs containing prey item i/total number of full stomachs) x 100.
The trophic level (TROPH) of each species area was calculated using TrophLab (Pauly et al., 2000), a standalone Microsoft Access routine for estimating trophic levels, downloadable from FishBase (Froese & Pauly, 2014). Statistical differences (P < 0.05) in basic diet composition as a function of size and season were established by applying the Chi-square test (Sokhal & Rohlf, 1987).
The trophic level for any consumer species i is
where Trophy is the fractional trophic level of prey j, DCij is the fraction of j in the diet of i, and G is the total number of prey species (Pauly et al., 1998; Pauly & Christensen, 2000; Pauly & Palomares, 2000):
All categories of preys identified in the present study were used to evaluate the trophic level of each teleostean species.
Following Stergiou & Karpouzi (2002), the trophic level values ranging from 2.0 to 4.5 and 3 categories of species were taken into consideration: pure herbivores = 2.0-2.1, omnivores with a preference for vegetable material = 2.1-2.9, omnivores with a preference for animal preys 2.9-3.7, carnivores feeding exclusively on animal preys =3.7-4.5.
RESULTS
All data recorded and calculated in the present paper are summarized in Table 1. The TL-TBW relationships revealed positive allometry in 13 species, low negative allometry in 3 species, and negative allometry in 5 species. The lowest negative allometry was recorded in Dicentrarchus labrax with b=1.23.
The vacuity index (VI) reached high values in 16 species, low values in 5 species, and in a single species, Sarpa salpa, it equalled 0.00. In this species, all the stomachs observed contained food or remains of food already described in materials and methods.
Overall, the two important zoological groups found in the guts were crustaceans and teleosts. Both groups were found together in 11 species, while teleosts were present in 20 species altogether. A single species, S. salpa, did not consume such preys, rather foraging for algae and seagrass. Among other groups also found in the stomach contents, cephalopods, annelids and sipunculids were the most frequent.
The trophic level (TROPH) reached high values - i.e., close to or higher than 3.00 - in 16 species. Conversely, it displayed low values in 5 species: Dentex dentex (2.37), Diplodus annularis (2.57), D. puntazzo (2.24), D. vulgaris (2.73), which belong among omnivorous species, and in S. salpa (2.00), which is a pure herbivorous species. The TROPH of species caught in Tunisian waters is generally close to the data recorded by Stergiou and Karpouzi (2002), except in those concerning sparid species, which ranged between 3.80 and 4.50.
DISCUSSION
The size (TL) versus total body weight relationships exhibited positive allometry for most of the species studied in the present paper, indicating that they found in the wild sufficient prey to be able to live and develop in this area. The northern coast of Tunisia revealed high biodiversity, including potential prey species belonging to several zoological groups (Rafrafi-Nouira, 2016). All species presented herein are targeted by fishermen for local consumption or export, which enhances their commercial interest and increases their value for the local economy. Conversely, only 7 species displayed negative allometry, which phenomenon could be explained by sampling hazards, but competitive pressure for food, which reduces the availability of prey familiar to certain species, cannot be totally ruled out either.
Conversely, the vacuity index (VI) displayed high values in most species, which could be explained by the non-availability of prey in the wild despite the local biodiversity richness. Such a pattern could also be the result of sampling periods, and the availability of certain prey could vary according to the season (Rafrafi-Nouira, 2016). Sampling methods and use of fishing gears cannot be totally excluded either (Sallami et al., 2014; Rafrafi-Nouira et al., 2016). All specimens sampled off the northern Tunisian coast were caught by trawling and generally spent considerable time in nets prior to being landed, therefore certain prey was completely digested and the stomachs of predators were thus found empty when analysed. This hypothesis is corroborated by the digested remains of prey found in the stomach contents
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Tab. 1: Parameters recorded in 21 teleost species collected from the northern coast of Tunisia. * Data from Sellami et al. (2015); ** Data from Rafrafi-Nouira et al. (2015); VI: vacuity index; C: crustaceans; T: teleosts; OG: other groups. TROPH 2: data from Stergiou & Karpouzi (2002).
Tab. 1: Izračunani parametri za 21 vrst kostnic, ujetih ob severni tunizijski obali. * Podatki iz vira Sellami et al. (2015); ** Podatki iz vira Rafrafi-Nouira et al. (2015); VI: indeks polnosti; C: raki; T: kostnice; OG: druge skupine. TROPH 2: podatki iz Stergiou & Karpouzi (2002).
Species	Total length (TL) vs total body weight (TBW)	%VI	C	T	OG	TROPH 1	TROPH 2
Gnathophis mystax (Delaroche, 1809) *	log TBW = - 5.88 + 3.09log TL, n = 48, r = 0.96	60.41	+	+	+	3.51	3.55
Belone belone (Linnaeus, 1758)	log TBW = - 5.79 + 2.94log TL, n =13, r = 0.97	69.23	-	+	-	4.50	-
Epinephelus marginatus (Lowe, 1834)	log TBW = - 5.14 + 3.11 log TL, n = 20, r = 0.99	65.00	+	+	+	3.51	4.13
Serranus scriba (Linnaeus, 1758)	log TBW = - 5.17 + 3.13 log TL, n = 76, r = 0.98	21.05	+	+	+	3.27	3.70
Dicentrarchus labrax (Linnaeus, 1758)	log TBW = - 0.58 + 1.23 log TL, n = 16, r = 0.91	75.00	+	+	-	4.20	-
Sciena umbra (Linnaeus, 1758)	log TBW = - 5.32 + 3.15 log TL, n = 63, r = 0.98	69.84	+	+	+	3.41	3.80
Dentex dentex (Linnaeus, 1758)	log TBW = - 4.34 + 2.75 log TL, n = 16, r = 0.97	81.25	+	+	+	2.37	4.50
Diplodus annularis (Linnaeus, 1758)	log TBW = - 3.88 + 2.58 log TL, n = 120, r = 0.96	70.45	+	+	-	2.57	3.40
Diplodus puntazzo (Cetti, 1777)	log TBW = - 4.77 + 2.98log TL, n = 31, r = 0.99	56.10	-	+	+	2.24	3.30
Diplodus sargus (Linnaeus, 1758)	log TBW = - 4.89 + 3.04log TL, n = 58, r = 0.98	23.07	+	+	+	3.09	3.38
Diplodus vulgaris (Linnaeus, 1758)	log TBW = - 4.89 + 3.02 log TL, n = 112, r = 0.96	94.00	-	+	+	2.73	3.70
Lithognathus mormyrus (Linnaeus, 1758)	log TBW = - 5.16 + 3.10 log TL, n = 43, r = 0.96	93.02	-	+	-	3.50	3.50
Oblada melanura (Linnaeus, 1758)	log TBW = - 5.18 + 3.11 log TL, n =32, r = 0.98	68.75	-	+	-	2.80	3.10
Sarpa salpa (Linnaeus, 1758)	log TBW =- 4.93 + 3.03 log TL, n =109, r = 0.93	0.00	-	-	+	2.00	2.50
Sparus aurata Linnaeus, 1758	log TBW = - 4.69 + 2.91 log TL, n = 80, r = 0.98	37.5	+	+	+	3.81	3.42
Labrus merula Linnaeus, 1758	log TBW = - 5.49 + 3.27 log TL, n =51, r = 0.99	80.40	+	+	-	3.20	3.47
Labrus viridis Linnaeus, 1758	log TBW = - 3.79 + 2.53 log TL, n = 65, r = 0.97	65.00	-	+	+	3.38	3.84
Symphodus melops (Linnaeus, 1758)	log TBW = -5.05 + 3.12 log TL, n = 68, r = 0.97	76.19	-	+	+	3.26	-
Symphodus tinca (Linnaeus, 1758)	log TBW = - 5.16 + 3.10 log TL, n =42, r = 0.97	68.96	-	+	+	3.32	3.26
Chelon labrosus (Risso, 1827)	log TBW = - 4.09 + 2.61 log TL, n =14, r = 0.89	95-94	-	+	-	3.50	-
Scorpaena porcus Linnaeus, 1758 **	log TBW = - 4.60 + 3.09 log TL, n =715, r = 0.96	41.11	+	+	+	3.48	3.82
which remained unidentifiable. Similar patterns were observed in previous studies about food and feeding habits of species from northern Tunisian waters (Mnasri et al., 2012; El Kamel-Moutalibi et al., 2013; Sallami et al., 2014; Rafrafi-Nouira et al., 2016).
Two zoological groups prevailed in the stomach contents: crustaceans and osteichthyans, thus confirming previous observations concerning other species inhabiting the same marine areas (Rafrafi-Nouira, 2016). Similarly, other preys were found, such as cephalopods,
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annelids, bivalves, and echinoderms, the number and weight of these animals depending on the species, and on the prey and predator sizes. Additionally, ontogenic changes were probably related to the biological environment and therefore prey availability.
The trophic levels of the 21 sampled species from northern Tunisian waters are similar to those estimated by Stergiou & Karpouzi (2002). Of these species, 17 could be considered top predators playing an important role in the regulation of the local marine ecosystem. Inter- and intraspecific competitive pressure for food cannot be completely avoided, which was probably the case with the sparid species, which occupied a lower TROPH level than other species, as sea grass and algae were recorded in their guts. Such findings could be considered as occasional or at least the result of a local abundance of marine plants that fishes would feed on in addition to other prey items. S. salpa is the best example of the effect of such abundance, as indicated
by its low TROPH = 2.00 and VI = 0.00; namely, large amounts of algae and seagrass were found in the guts of the examined specimens throughout the year.
The study of food and feeding habits presented in this paper not only showed that viable populations of several animal species occurred in the area, but also enhanced the knowledge of local biodiversity. However, monitoring of fishery activities following recommendations and suggestions included in CIESM (2018) should be carried out to avoid drastic declines of populations, as was the case in other marine areas throughout the Mediterranean Sea.
ACKNOWLEDGEMENTS
The authors are grateful to the fishermen of the study area who kindly provided us specimens. They wish to thank also two referees for helpful and useful comments allowing us to improve the scientific quality of the paper.
PREGLED TROFIČNIH NIVOJEV PRI RIBAH KOSTNICAH VZDOLŽ SEVERNOTUNIZIJSKIH VODA (OSREDNJE SREDOZEMSKO MORJE)
Sihem RAFRAFI-NOUIRA
Unité de Recherches Exploitation des Milieux aquatiques, Institut Supérieur de Pçche et d'Aquaculture de Bizerte, Université de
Carthage, BP 15, 7080 Menzel Jemil, Tunisia
Youssouph DIATTA
Laboratoire de Biologie marine, Institut fondamental d'Afrique noire, (IFAN Ch. A. Diop), Université Cheikh Anta Diop de Dakar, BP
206, Dakar, Senegal.
Christian CAPAPÉ
Laboratoire d'Ichtyologie, case 104, Université de Montpellier, 34 095 Montpellier cedex 5, France
e-mail: capape@univ-montp2.fr
POVZETEK
V prispevku avtorji poročajo o rezultatih, ki se nanašajo na 1657 primerkov rib kostnic, ujetih vzdolž severnotu-nizijske obale, ki pripadajo 21 vrstam. Primerki so bili ujeti v okolju, bogatem s plenom, kar je razvidno iz odnosa med velikostjo in telesno maso. Visoke vrednosti indeksa polnosti prebavila so verjetno posledica vzorčevalnih in ribiških metod. Najbolj pogosti skupini plena so raki in kostnice. Poleg tega visoki trofični nivo (TROPH) (± 3.00) potrjuje, da so obravnavane kostnice predvsem plenilke. Med vsemi obravnavanimi vrstami je le salpa rastlinojeda (TROPH = 2.00).
Ključne besede: kostnice, trofični nivo, indeks polnosti, odnos med telesno dolžino in maso, kompeticija za
hrano, obala Tunizije
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Bradaï, M.N. (2000): Diversité du peuplement ichtyque et contribution à la connaissance des sparidés du golfe de Gabès. Thesis, University of Sfax (Tunisia), 600 pp.
Castany, G. (1955): Le Haut-Bassin Siculo-Tunisien. Etude de morphologie et de géologie sous-marines. Bull. stn. Océanogr. Salammbô, 52, 3-12.
CIESM (2018): Engaging marine scientists and fishers to share knowledge and perceptions - Early lessons. CIESM Workshop Monograph n° 50 [F. Briand, ed.], CIESM Publisher, Paris, Monaco, 218 pp.
El Kamel-Moutalibi, O., N. Mnasri, M. Boumaïza, C. Reynaud & C. Capapé (2013): Diet of common torpedo Torpedo torpedo (Chondrichthyes:Torpedinidae) from the Lagoon of Bizerte (northeastern Tunisia, central Mediterranean). Cah. Biol. Mar., 54(2), 209-220.
El Kamel-Moutalibi, O. (2014). Les élasmobranches de la lagune de Bizerte (Nord Tunisien,Centre Méditerranée): Biodiversité et biologie de la torpille ocellée Torpedo torpedo (Linneaus,1758). Thesis, University of Carthage (Tunisia), 233 pp.
Froese, R., A.C. Tsikliras & K.I. Stergiou (2011): Editorial note on weight-length relations of fishes. Acta Ichthyologica et Piscatoria, 41, 261-263.
Froese, R. & D. Pauly (2014): FishBase. [version 06/2014] http://www.fishbase.org
Hureau, J. (1970): Biologie comparée de quelques poissons antarctiques (Notothenûdae). Bull. Inst. Océanogr, Monaco, 68,1-244.
Hyslop, E.J. (1980): Stomach contents analysis: a review of methods and their application. J. Fish Biol., 17, 411- 429.
Louisy, P. (2002): Guide d'identification des poissons marins Europe et Méditerranée. Paris, Ulmer édition, Paris, 430 pp.
Lubet, P. & A. Azzouz (1969): Etude des fonds chalutables du golfe de Tunis. Bull. Inst. océanogr. Salammbô, 1(3), 87-111.
Mnasri, N., O. El Kamel, M. Boumaïza, C. Reynaud & C. Capapé. (2012): Food and feeding habits of the small-spotted catshark, Scyliorhinus canícula (Chondrichthyes: Scyliorhinidae) from the northern coast of Tunisia (central Mediterranean). Cah. Biol. Mar., 53(1), 139-150.
Mnasri-Sioudi, N. 2014. Les élasmobranches de la côte septentrionale de la Tunisie: Biodiversité et étude écobiologique d'une espèce pleurotrême Scyliorhinus canícula (Linneaus, 1758). Thesis, University of Carthage (Tunisia), 239 pp.
Pauly, D. (1983): Some simple methods for assessment of tropical fishes. FAO Fish. Tech. Papers, 234, 3-10.
Pauly, D., A. Trites, E. Capuli & V. Christensen (1998): Diet composition and trophic levels of marine mammals. ICES J. Mar. Sci., 55, 467-481.
Pauly, D. & V. Christensen (2000): Trophic levels of fishes. In: Fishbase 2000: Concepts, Design and Data Sources, (R. Froese., D. Pauly eds), ICLARM, Manila, Philippines, pp. 181.
Pauly, D., R. Froese, P. Sa-a, M.L. Palomares, V. Christensen & J. Rius (2000): TrophLab Manual. ICLARM, Manila, Philippines.
Pauly, D. & M.L. Palomares (2000): Approaches for dealing with three sources of bias when studying the fishing down marine food web phenomenon. In Fishing Down the Mediterranean Food Webs? (F. Briand ed.). CIESM Workshop Series, 12, 61-66.
Perrier, R. (1964): La faune de la France illustrée. 1B. Vers et némathelminthes. Delagrave, Paris, 179 pp.
Perrier, R. (1975): La faune de la France illustrée. II. Arachnides et crustacés. Delagrave, Paris, 220 pp.
Quéro, J.C., P. Porché & J.J. Vayne (2003): Guide des poissons de l'Atlantique européen. Les Guides du naturaliste. Delachaux & Niestlé: Lonay (Switzerland)-Paris, 465 pp.
Rafrafi-Nouira, S., O. El Kamel-Moutalibi, M. Boumaïza, C. Reynaud & C. Capapé (2016): Food and feeding habits of black scorpionfish, Scorpaena porcus (Osteichthyes: Scorpaenidae) from the northern coast of Tunisia (central Mediterranena). J. Ichthyol, 56(1), 107123.
Rafrafi-Nouira, S. (2016): Catalogue raisonné des espèces de poissons capturées devant Ras Jebel et autres régions marines de Tunisie septentrionale: aspects morphologiques, biométriques et bio-écologiques. Thesis, University of Carthage (Tunisia), 509 pp.
Rosecchi, E. & Nouaze Y. (1987): Comparaison de cinq indices alimentaires utilisés dans l'analyse des contenus stomacaux. Rev. Inst. Pêch. Marit., 49, 111-123.
Sallami, B., M. Ben Salem, C. Reynaud & C. Capapé (2014): Diet of Mediterranean Moray Eel Muraena helena (Actinopterygii: Anguilliformes: Muraenidae) from the northeastern Tunisian coast (central Mediterranean). Acta Ichthyol. Piscat., 44(4), 273-283.
Sokhal, R.R. & F.J. Rohlf (1987): Biometry. Freeman: San Francisco, CA, 859 pp.
Stergiou K.I. & V.S. Karpouzi (2002): Feeding habits and trophic levels of Mediterranean fish. Rev. Fish Biol. Fish. 11, 217-254.
Whitehead, P.J.P., M.L. Bauchot, J.-C. Hureau, J. Nielsen & E. Tortonese (1984-1986): Fishes of the North-eastern Atlantic and the Mediterranean, Unesco, Paris, Vol. 1., Vol. 2., Vol. 3, 1473 pp.
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received: 2018-12-11	DOI 10.19233/ASHN.2019.10
SPONTANEOUS VEGETATION ON SLAG HEAPS IN SOUTHERN CROATIA
NenadJASPRICA
Institute for Marine and Coastal Research, University of Dubrovnik, P.O. Box 83, HR-20000 Dubrovnik, Croatia
e-mail: nenad.jasprica@unidu.hr
Marija PANDlA
Primary School Murterski Skoji, Put Skole 8, HR-22243 Murter, Croatia
Milenko MILOVIC
"Antun Vrancic" Grammar School, Put Gimnazije 64, HR-22000 Sibenik, Croatia
ABSTRACT
A phytosociological investigation of spontaneous vegetation on seven-year-old ferro-manganese and silico-man-ganese slag heaps in southern Croatia showed a predominance of ruderals and weeds (Chenopodietea, Artemisietea vulgaris) and taxa of dry open habitats (Festuco-Brometea, Sedo-Scleranthetea). The limited number and cover of woody taxa seem to indicate an early successional stage in the process of development of natural vegetation. However, we recommend removing the heaps from the area and initiating soil remediation according to Croatian law, EU standards and obligations.
Key words: phytosociology, ruderal vegetation, industrial waste, Mediterranean climate, Dalmatia, eastern Adriatic
VEGETAZIONE SPONTANEA SU ACCUMULI DI SCORIE NELLA CROAZIA MERIDIONALE
SINTESI
Lo studio fitosociologico della vegetazione spontanea su accumuli di scorie di ferro-manganese e silico-manga-nese nel sud della Croazia, risalenti a sette anni addietro, ha messo in evidenza una predominanza di specie ruderali e infestanti (Chenopodietea, Artemisietea vulgaris) e di taxa di habitat aridi e aperti (Festuco-Brometea, Sedo-Scle-ranthetea). Inoltre, un limitato numero di taxa arborei e arbustivi, con ridotta copertura, suggerisce l'insediarsi di un primo stadio della successione nel processo di sviluppo della vegetazione. Tuttavia si consiglia la rimozione degli accumuli di scorie dall'area e l'avvio della bonifica dei suoli, come previsto dalle leggi croate e secondo gli standard e gli obblighi dell'Unione Europea.
Parole chiave: fitosociologia, vegetazione ruderale, rifiuti industriali, clima mediterraneo, Dalmazia, Adriatico
orientale
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INTRODUCTION
The Electrodes and Ferroalloys Factory (TEF) in the city of Sibenik, southern Croatia, is a former factory in which the production of pig iron, steel and ferrous alloys took place almost throughout the 20th century, ceasing in 1995. With the decommissioning of the facilities at the TEF site (total surface area of 22 hectares) various types of waste, such as ferro-manganese and silico-manganese slag, tar, phenolic residues, carborundum, graphite electrode scraps, etc. were left at the site. In the period from May 2010 to February 2011, a total of 140,000 tons of ferro-manganese and silico-manganese slag were moved to the village of Biljane Donje near the city of Zadar (Fig. 1). In recent times, only a smaller area with ca. 6,000 m3 of the slag can still be found at the former TEF site in the city of Sibenik. Slag is typically dumped in heaps with no subsequent remediation.
Dumping sites for ash and slag waste represent a major challenge in terms of biological reclamation and introduction of vegetation. This is due to the disadvantageous properties of such waste, including the absence of soil organic matter (SOM), as well as nitrogen deficiency, high compaction, poor air-water ratio and high alkaline reaction (Kovar, 2004). The onset and development of vegetation at localities of such origin are important topics in restoration ecology (Rehounkova et al., 2011; Prach et al., 2014. and references therein). Such localities offer a unique opportunity for monitoring spontaneous processes of colonization/succession of organisms on these "artificial islands" and following biotic interactions in the process (Prach & Pysek, 1994).
Fig. 1: Geographical position of the study areas in southern Croatia, eastern Adriatic. Sl. 1.: Geografska lega raziskanega območja v južni Hrvaški, vzhodni Jadran.
In the NW Balkans, studies of spontaneous vegetation development in these habitats, based on phytoso-ciological research, including description of particular plant associations, have been reported from Bosnia and Herzegovina (Lakusic et al., 1977, 1978; Grgic & Lakusic, 1987) and Montenegro (Vukicevic & Avdalovic, 1982). In Croatia, such sites are still awaiting phytoso-ciological investigation. The matter is addressed by the present study, which examines spontaneous vegetation on seven-year-old slag heaps in southern Croatia.
MATERIAL AND METHODS Study area
The study was carried out in southern Croatia, in two areas: 1) the area of TEF situated in the city of Sibenik (43°44'43.1" N, 15°52'56.9" E), and 2) the landfill in the village of Biljane Donje, situated 20 kilometres east of the city of Zadar (44°05'47.9" N, 15°28'55.5" E) (Figs. 1 and 2). The slag heaps on the two sites originated from the production of ferroalloys in TEF, and have not been moved or replaced in the last seven years. The altitude of the sites is ca. 10 and 180 m a.s.l. in Sibenik and Biljane Donje, respectively. The heaps top out at about 1.5(-2) to 15 m above the level of the ground. The region has a typical Mediterranean climate: summers are warm and dry, winters mild and rainy, mean annual temperature 15.0-15.4 °C and mean annual precipitation 773-860 mm (data from the meteorological stations of the Croatian Meteorological and Hydrological Service in Sibenik and Zadar for the 1976-2006 period; Milovic, 2008; Jasprica et al., 2015). The vegetation surrounding the landfill in Sibenik is mainly composed of planted Pinus halepensis and urban ruderal plant communities (Milovic, 2002). In Biljane Donje, the vegetation surrounding the landfill is a mosaic of preserved forest patches (mainly dominated by Carpinus orientalis and Quercus pubescens) and vineyards.
In general, the slag on the sites is alkaline (the pH of the substrate in initial successional stages is 8-9), with a low manganese content (MnO < 20 %) and about 30 % of Si produced by upgrading standard alloy through addition of silicon waste from the iron silicon industry at the end of the ferroalloy production process (Oliveira et al., 2017).
Data collection
Fieldwork was carried out in May 2018. The Braun-Blanquet approach (Braun-Blanquet, 1964; Barkman et al., 1964; Dierschke, 1994) was used for data collection, with category 2 subdivided into 2m, 2a and 2b. Five and four relevés were collected in Sibenik and Biljane Donje, respectively. The plots were selected randomly within each site and the entire surface of the landfills was covered. The size of relevé plots was 25 m2. The
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Fig. 2: Ferro-manganese and silico-manganese slag heaps in the area of the former Electrodes and Ferroalloys Factory in the city of Šibenik (A); details of vegetation with Andrachne telephioides and Dittrichia viscosa in Šibenik (B); heaps in the village of Biljane Donje, Zadar County (C), details of vegetation with Avena barbata and Dittrichia viscosa at the top of a heap in Biljane Donje (D) (Photo: N. Jasprica, May 5, 2018).
Sl. 2: Feromanganska in silikomanganska jalovina v predelu nekdanje tovarne elektrod in železovih zlitin v Šibeniku (A); detajl vegetacije z vrstama Andrachne telephioides in Dittrichia viscosa v Šibeniku (B); jalovina v zaselku Biljane Donje v zadrskem okrožju (C), detajl vegetacije z vrstama Avena barbata and Dittrichia viscosa na vrhu jalovine v zaselku Biljane Donje (D) (Foto: N. Jasprica, 5 maj 2018)
nomenclature of plant taxa follows the Flora Croatica Database (Nikolic, 2018). The biological forms were directly verified in the field, labelled with acronyms reported by Pignatti (1982) and based on the classification by Raunkiaer (1934). Regarding chorological forms, reference was made to Jasprica et al. (2017), as well as monographs used for taxonomic nomenclature.
Taxa were associated with vegetation units (classes). The system of characterizing species (mostly for those plants that are considered 'characteristic species' of the classes) was mostly derived from Mucina et al. (2016). The nomenclature of vegetation units followed Skvorc et al. (2017). Constant taxa were defined as those with a frequency 30 % within the vegetation unit. Dominant
taxa were defined as those occurring in at least 10 % of the relevés of a vegetation unit with a cover value of 25 %.
RESULTS
There were 64 plant taxa in total (Tab. 1). The vegetation cover varied from 30 % to 80 %, while stands appeared on slopes ranging from 10° to 80°.
The landfills were dominated by Therophytes (57 %) and Hemicryptophytes (28 %). Phanerophytes and Chamaephytes occurred in equal percentages ( 5 % each).
Mediterranean floral elements (34 %), followed by a considerable share of Cosmopolitans (16 %) and
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Tab. 1: Phytosociological table of vegetation on the ferro-manganese and silico-manganese slag heaps. Abbreviations: LF = life form, FE = floral element. Life forms: Ch - chamaephytes, G - geophytes, H - hemicryptophytes, P - phanerophytes, T - therophytes. Floral elements: MED - Mediterranean; SEU - South European; EA - Euroasian; WS - Cosmopolitan; CUAD - Cultivated and adventive plants; * - Illyrian-Adriatic endemic taxon. Tab. 1: Fitosociološka preglednica vegetacije na feromanganski in slikomanganski jalovini. Okrajšave: LF = življenjska oblika, FE = floristični element. Življenjske oblike: Ch - hamefiti, G - geofiti, H - hemikriptofiti, P -fanerofiti, T - terofiti (enoletnice). Floristični elementi: MED - sredozemski, SEU - južnoevropski, EA - evrazijski, WS - kozmopoliti, CUAD - gojene in adventivne rastline, * - ilirsko-jadranski endemit.
Date and location of the relevés/ Datumi in lokalitete popisov: May 5, 2018. Rels. 1-5, Šibenik: Rel. 1. X = 5571400, Y = 4845052; Rel. 2. X = 5571390, Y = 4845085; Rel. 3. X = 5571443, Y = 4845104; Rel. 4. X = 5571441, Y = 4845092; Rel. 5. X = 5571431, Y = 4845006. Rels. 6-9. Biljane Donje, near Zadar: Rel. 6. X = 5538978, Y = 4883653; Rel. 7. X = 5538952, Y = 4883659; Rel. 8. X = 5538959, Y = 4883693; Rel. 9. X = 5538978, Y = 4883713.
		Relevé No.	1	2	3	4	5	6	7	8	9	
		Locality	Šibenik					Biljane Donje				
		Plot size (m2)	25	25	25	25	25	25	25	25	25	
		Aspect	N	NE		NE	NE	N	S	W	W	
LF	FE	Slope (°)	10	55		70	80	70	70	40	80	
		Vegetation cover(%)	70	50	70	40	30	60	80	80	80	
		Total number of taxa	20	16	10	17	17	17	12	21	16	o/ /o
Chenopodietea												
T	SEU	Avena barbata Pott ex Link	3	1		+	+	1	3	2a	2m	88
T	MED	Echium plantagineum L.	+		2a			+	3	+	+	66
H	MED	Reseda alba L.		+				+	1	+	+	55
T	MED	Bromus madritensis L.	1			+	+					33
T	MED	Desmazeria rigida (L.) Tutin	+					+		+		33
T	MED	Aegilops neglecta Req. ex Bertol.		+			+			+		33
H	MED	Carduus pycnocephalus L.				+		+		r		33
T	MED	Lophochloa cristata (L.) Hyl.	2a							+		22
T	MED	Aegilops triuncialis L.	+							+		22
T	MED	Crepis sancta (L.) Babc.				+					+	22
T	SEU	Geranium purpureum Vill.					2a				+	22
T	MED	Medicago orbicularis (L.) Bartal.								+	+	22
T	MED	Sonchus asper (L.) Hill ssp. glaucescens (Jord.) Ball		+								11
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T	MED	Urospermum picroides (L.) Scop. ex F.W.Schmidt									r	11
Festuco-Brometea												
H	EA	Melica ciliata L.		+	+	1	+	2b	+			66
T	EAF	Arenaria leptoclados (Reichenb.) Guss.	+							r		22
H	*	Centaurea spinosociliata Seenus		+						+		22
H	SEU	Sanguisorba minor Scop. ssp. muricata Briq.			+	+						22
H	SEU	Lactuca viminea (L.) J. et C. Presl						+			r	22
H	MED	Tragopogon porrifolius L.						+				11
T	MED	Lomelosia brachiata (Sm.) Greuter et Bürdet (= Trenastelma palaestinum)							1			11
Artemisietea vulgaris												
H	MED	Dittrichia viscosa (L.) Greuter		2a	2a	1		2b	1	2b		66
H	EA	Chondrilla juncea L.				+	+			+	+	44
H	WS	Reseda lutea L.			+	+	+					33
H	EA	Picris hieracioides L.						+				11
T	WS	Galium aparine L.									+	11
H	EA	Cirsium vulgare (Savi) Ten.									r	11
Sedo-Scleranthetea												
T	WS	Medicago minima (L.) Barta	+	+						3		33
T	WS	Cerastium pumilum Curtis ssp. glutinosum (Fries) Jalas	+							+		22
T	EA	Petrorhagia prolifera (L.) P. W. Ball ex Heywood		+						+		22
T	MED	Valantia muralis L.				r						11
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Ch	SEU	Sedum ochroleucum Chaix					+					11
Lygeo sparti-Stipetea tenacissimae												
H	MED	Reichardia picroides (L.) Roth.					r	+			r	33
T	SEU	Vulpia ciliata Dumort	2m					+				22
H	MED	Piptatherum miliaceum (L.) Coss.		3		+						22
H	MED	Brachypodium retusum (Pers.) P. Beauv.		+								11
Papaveretea rhoeadis												
T	CUAD	Papaver rhoeas L.					r	+	+		1	44
T	WS	Senecio vulgaris L.						r		r	+	33
T	EAF	Veronica arvensis L.	+									11
G	WS	Convolvulus arvensis L.				2a						11
Sisymbrietea												
T	EA	Geranium rotundifolium L.	+	+								22
T	MED	Sisymbrium orientale L.	+	+								22
T	WS	Erodium cicutarium (L.) E Her.	+									11
T	WS	Xanthium strumarium L.							r			11
Stipo-Trachynietea distachyae												
T	MED	Linaria simplex (Willd.) DC.	+	1	2m	1	+	2m	+			77
Ch	MED	Andrachne telephioides L.			4	+	r		r	+	4	66
T	MED	Psilurus incurvus (Gouan) Schinz et Thell	+									11
Quercetea ilicis												
P	MED	Juniperus oxycedrus L. ssp. oxycedrus				+						11
P	MED	Pinus halepensis Mill., juv.					+					11
G	MED	Asparagus acutifolius L.							r			11
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Helianthemetea guttati												
T	SEU	Crupina crupinastrum (Moris) Vis			+		+					22
T	MED	Medicago coronata (L.) Bartal.	+									11
T	MED	Minuartia mediterranea (Link.) K. Maly	+									11
Thlaspietea rotundifoliae												
H	SEU	Scrophularia canina L. ssp. bicolor (Sibth. et Sm.) Greuter				1						11
T	MED	Crucianella latifolia L.					2m					11
Digitario sanguinalis-Eragrostietea minoris												
T	MED	Heliotropium europaeum L.		+	+	+		+	+	+	+	77
Koelerio-Corynephoretea canescentis												
T	EA	Minuartia hybrida (Vill.) Schischkin in Komarov	+									11
Asplenietea trichomanis												
Ch	MED	Aurinia sinuata (L.) Griseb.					2a					11
Rhamno-Prunetea												
P WS Rosa canina L. . . . . r .									. . . 11			
Molinio-Arrhenatheretea												
H	WS	Plantago lanceolata L.								+		11
Others												
T	CUAD	Conyza canadensis (L.) Cronquist	+	+								22
		Fumaria sp.			+							11
		Daucus sp.						+				11
		Anthemis sp.								r		11
Euroasian plants (13 %), dominated on the landfills. Two non-indigenous species were noted: Papaver rhoeas and Conyza canadensis. The latter species is considered invasive in Croatia (Nikolic et al., 2014). Centaurea spinosociliata was defined as an endemic taxon.
The highest number of taxa belonged to the Cheno-podietea (14 taxa), followed by Festuco-Brometea (7), Artemisietea vulgaris (6) and Sedo-Scleranthetea (5). The number of taxa in the relevés ranged between 12 and 21 (average 16). The classes Digitario sanguinalis-
Eragrostietea minoris, Koelerio-Corynephoretea canes-centis, Asplenietea trichomanis, Rhamno-Prunetea and Molinio-Arrhenatheretea were represented by one taxon each, mostly with a low cover or frequency.
The dominant taxa were as follows: Avena barbata, Echium plantagineum, Medicago minima, Piptatherum miliaceum and Andrachne telephioides. Constant taxa were: Avena barbata, Echium plantagineum, Reseda alba, Bromus madritensis, Melica ciliata, Dittrichia viscosa, Chondrilla juncea, Reseda lutea, Medicago
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minima, Reichardia picroides, Papaver rhoeas, Senecio vulgaris, Andrachne telephioides, Linaria simplex and Heliotropium europaeum.
DISCUSSION
In the present study, spontaneous vegetation on seven-year-old slag heaps consisted of a relatively low number of taxa. Although we did not study vegetation dynamics, emergence of fast growing annual plant taxa and biennial hemicriptophytes was expected in the first few years, as established in similar studies (Rehounkova et al., 2011, and references therein). Transport of dia-spores from the surrounding landscape, mainly through zoochory and anemochory, is among the factors governing the development of plant communities in the initial stages of succession (Vankova & Kovar, 2004). Seeds of plants are sometimes also carried into the heaps by humans during the heaping process.
No bryophytes were found in our study, contrarily to the findings of Grgic & Lakusic (1987), who investigated succession processes on spoil heaps in Bosnia and Herzegovina. This may be generally attributed to the warm and dry Mediterranean climate and/or specific physical and chemical properties of steel slag in a slag heap.
In our case, ruderals and weeds (Chenopodietea, Artemisietea vulgaris) and taxa of the dry open habitats (Festuco-Brometea, Sedo-Scleranthetea) were dominant. In this study, contrary to the findings of Lakusic et al. (1977), who described some plant associations in the heaps (Sedo-Scleranthetea), no characteristic set of taxa was established. The most common taxa from the sites studied were also found in the urban ruderal communities of the surroundings, both in the cities of Sibenik and Zadar (Milovic, 2002; Milovic & Mitic, 2012) and their
environs (Jasprica et al., 2017). In general, but not studied here, the presence of the surrounding vegetation and variations in the species pool could also play a role in the different floristic composition and subsequent community transitions on the sites (Vukicevic & Avdalovic, 1982; Grgic & Lakusic, 1987; Otto et al., 2006).
Both the low number and low cover of woody taxa appear to indicate an early successional stage in the process of the development of natural vegetation. Steel slag is highly reactive and when exposed to rainwater it is known to release ecotoxic metals into the surrounding water bodies and soils (Meng & Liu, 2000; Oliveira et al., 2017). These biotopes may thus host only a fraction of the potential colonizers (Heckenroth et al., 2016).
In summary, this study adds to the base of information on the structure of vegetation communities on industrial waste deposits in the Mediterranean climate. Nevertheless, given the relatively small area studied and low number of relevés, the results should be considered in the context of anthropogenic influences occurring as a generalized phenomenon throughout the Mediterranean Basin and elsewhere. Taking into account the origin, properties and locations of this waste material, we recommend removing the heaps from the area and undertaking soil remediation according to Croatian law, EU standards and obligations.
ACKNOWLEDGEMENTS
The authors thank Steve Latham (UK) for improving the English and Massimo Terzi for Italian translation of the abstract. Thanks are also extended two anonymous reviewers whose observations improved the quality of the final version of the manuscript.
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Nenad JASPRICA et aL: SPONTANEOUS VEGETATION ON SLAG HEAPS IN SOUTHERN CROATIA, 93-102
SPONTANA VEGETACIJA NA JALOVINAH V JUŽNI HRVAŠKI
NenadJASPRICA
Institute for Marine and Coastal Research, University of Dubrovnik, P.O. Box 83, HR-20000 Dubrovnik, Croatia
e-mail: nenad.jasprica@unidu.hr
Marija PANDŽA
Primary School Murterski Škoji, Put Škole 8, HR-22243 Murter, Croatia
Milenko MILOVIC
"Antun Vrančic" Grammar School, Put Gimnazije 64, HR-22000 Šibenik, Croatia
POVZETEK
Fitosociološka raziskava spontane vegetacije na sedemletni feromanganski in silikomanganski jalovini v južni Hrvaški je pokazala prevladovanje ruderalnih rastlin in plevelov (Chenopodietea, Artemisietea vulgaris) ter vrst odprtih habitatov (Festuco-Brometea, Sedo-Scleranthetea). Omejena pokrovnost gozdnih taksonov kaže na zgodnji stadij sukcesije v procesu razvoja naravne vegetacije. Avtorji priporočajo odstranjevanje jalovin z obravnavanega območja in pričetek remediacije prsti v skladu s hrvaško zakonodajo, evropskimi standardi in zahtevami.
Ključne besede: fitosociologija, ruderalna vegetacija, industrijski odpadki, sredozemsko podnebje, Dalmacija,
vzhodni Jadran
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R., D. lakushenko, J. Pallas, F.J.A. Daniels, E. Bergmeier, A. Santos Guerra, N. Ermakov, M. Valachovič, J.H.J. Schaminée, T. Lysenko, Y.P. Didukh, S. Pignatti, J.S. Rodwell, J. Capelo, H.E. Weber, A. Solomeshch, P. Di-mopoulos, C. Aguiar, S.M. Hennekens & L. Tichy (2016): Vegetation of Europe: Hierarchical floristic classification system of vascular plant, bryophyte, lichen, and algal communities. Appl. Veg. Sci., 19, Suppl. 1, 3-264.
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received: 2019-01-03	DOI 10.19233/ASHN.2019.11
LE LAMIACEAE DELLA FLORA ITALIANA: DISTRIBUZIONE REGIONALE E CONSIDERAZIONI FITOGEOGRAFICHE
Amelio PEZZETTA
Via Monteperalba 34 - 34149 Trieste e-mail: fonterossi@libero.it
SINTESI
Con Lamiaceae si indica un'importante famiglia della flora italiana, ampiamente conosciuta e studiata. Il presente lavoro riporta l'elenco di tutte le entità segnalate in Italia, analizza la loro distribuzione geografica regionale, individua i principali pattern distributivi, presenta un'analisi fitogeografica e cerca di discutere le origini e movimenti migratori sulla base di dati bibliografici. Nel territorio nazionale sono segnalati 272 taxa infragenerici. La distribuzione regionale è alquanto discontinua: solo 15 taxa sono presenti in tutte le regioni; 8 in tutte le regioni continentali (comprendendo in alcuni casi anche la Sicilia o la Sardegna); gli altri si distribuiscono in una o poche regioni, anche in modo disgiunto. Prevale il contingente mediterraneo, seguito da quello endemico. Dalla letteratura consultata emerge che ci sono ancora incertezze e differenze di interpretazione riguardo le origini della famiglia, generi e specie e, dei movimenti migratori seguiti per colonizzare le regioni italiane.
Parole chiave: Lamiaceae, check-list, distribuzione regionale, biogeografia, origini
LAMIACEAE OF THE ITALIAN FLORA: REGIONAL DISTRIBUTION AND FITOGEOGRAPHIC CONSIDERATIONS
ABSTRACT
With Lamiaceae is indicted an important family of Italian flora, widely known and studied. The present work reports the list of all the entities reported in Italy, analyzes their regional geographical distribution, identifies the main distribution patterns, presents a phytogeographic analysis and tries to explain origins and migratory movements on the basis of bibliographic data. In the national territory 272 infrageneric taxa are reported. The regional distribution of the various taxa is somewhat discontinuous: only 15 taxa are present in all regions; 8 in all continental regions (including in some cases also Sicily or Sardinia), the others are distributed in one or a few regions, even in a disjointed way. The Mediterranean contingent prevails, followed by the endemic one. From the literature consulted it emerges that there are still uncertainties and opinions on the origins of the family, genera and species and the migratory movements that brought them to colonize the Italian regions.
Key words: Lamiaceae, check-list, regional distribution, biogeography, migrations, origins
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INTRODUZIONE
La famiglia delle Lamiaceae Martinov comprende 245 generi con 7886 specie (The Plant List, ultimo accesso 1-12-2018) ed e caratterizzata da piante erbacee, lianose, arbustive e raramente arboree con fiori dalla forma bila-biata. Harley et al. (2004) la ripartisce in 7 subfamiglie:
-	Ajugoideae Kost. che con circa 1100 specie e presente in tutti i continenti tranne l'Antartide;
-	Lamioideae Harl. comprendente 57 generi e circa 1190 specie e, sebbene abbia una distribuzione cosmopolita, solo poche specie non vivono in Africa ed Eurasia;
-	Nepetoideae (Dum.) Luerss. costituita da circa 112 generi e 3600 specie a distribuzione cosmopolita;
-	Prostantheroideae Luerss., endemica dell'Australia, con 16 generi e circa 280 specie;
-	Scutellarioideae Prantl con 5 generi e circa 380 specie a distribuzione subcosmopolita;
-	Symphorematoideae Briq., endemica delle zone tropicali e subtropicali dell'Asia (India, Sri Lanka, sud-est asiatico e Malesia occidentale) che comprende 3 generi con circa 30 specie;
-	Viticoideae Briq. che comprende da 6 a 10 generi e circa 400 specie distribuite in modo preponderante nelle zone tropicali e subtropicali del mondo.
Recentemente Li et al. (2016) e Li & Olmstead (2017) hanno descritto altre 5 subfamiglie: Cymarioideae, Peronematoideae, Premnoideae, Callicarpoideae e Tectonoideae.
Le Lamiaceae sono presenti in una vasta gamma di habitat e più diffuse nelle seguenti zone della terra: il Bacino del Mediterraneo, Asia (centrale, sud-occidentale, Cina e regione indomalesiana), l'Africa subsahariana e il Madagascar, l'Australia e il continente americano (Hedge 1992; Harley et al. 2004). Alcune piante sono coltivate e utilizzate dall'uomo a fini ornamentali, in cucina, pro-fumeria, liquoreria, farmacia e nella medicina popolare.
È obiettivo del presente studio fornire una visione comprensiva sulla distribuzione delle specie apparte-nenti alla famiglia delle Lamiaceae presenti nel territorio italiano, e chiarire i fenomeni migratori che ne hanno determinato la diffusione.
MATERIALI E METODI
La nomenclatura e la distribuzione dei taxa presenti seguono: Celesti-Grapow et al. (2010), Bartolucci et al. (2018), http://dryades.units.it/floritaly/ e successivi aggiornamenti riportati in bibliografía.
Per l'assegnazione dei tipi corologici (Tab. 1) si è seguito Pignatti (2018), tranne vari taxa cui è stato asse-
Fig. 1: Classificazione gerarchica delle regioni italiane in base alla somiglianza tra le distribuzioni dei singoli taxa di Lamiaceae. I numeri da 1 a 20 sono le regioni italiane: 1: Valle D'Aosta; 2: Piemonte; 3: Lombardia; 4: Trentino Alto-Adige; 5: Veneto; 6: Friuli Venezia-Giulia; 7: Liguria; 8: Emilia Romagna; 9: Toscana; 10: Marche; 11: Umbria; 12 Lazio; 13: Abruzzo; 14: Molise; 15: Campania; 16: Puglia; 17: Basilicata; 18: Calabria; 19: Sicilia; 20: Sardegna. Sl. 1: Hierarhična ureditev italijanskih regij na podlagi podobnosti med posameznimi taksoni ustnatic (Lamiaceae). Številke od 1 do 20 so italijanske regije: 1: Dolina Aoste; 2: Piemont; 3: Lombardija; 4: Trentinsko - Zgornje Poa-dižje; 5: Benečija; 6: Furlanija-Julijska krajina; 7: Ligurija; 8: Emilija Romanja; 9: Toskana; 10: Marke; 11: Umbrija; 12 Lacij; 13: Abruci; 14: Molize; 15: Kampanija; 16: Apulija; 17: Bazilikata; 18: Kalabrija; 19: Sicilija; 20: Sardinija.
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Tab. 1: Distribuzione regionale delle Lamiaceae della flora italiana. (1) da Bartolucci et al. (2018). Tab. 1: Regionalna razširjenost ustnatic v italijanski flori. (1) povzeto po Bartolucci et al. (2018).
	Taxa	Totale taxa della	Percentuale Lamiaceae	Lamiaceae	Lamiaceae
Regioni italiane	totali	flora regionale (1)	sulla flora regionale	endemiche	esclusive
Valle d'Aosta	63	2333	2,7	-	-
Piemonte	100	3535	2,8	-	2
Lombardia	110	3429	3,2	-	3
Trentino Alto Adige	105	3504	3,0	2	5
Veneto	105	3338	3,1	2	1
Friuli Venezia Giulia	107	3147	3,4	1	5
Liguria	114	3080	3,7	2	4
Emilia Romagna	117	2843	4,1	1	2
Toscana	129	3400	3,8	3	3
Marche	105	2540	4,1	4	1
Umbria	95	2406	3,9	4	-
Lazio	121	3047	4,0	7	-
Abruzzo	135	3216	4,2	5	3
Molise	102	2327	4,4	5	-
Campania	128	2828	4,5	12	1
Puglia	114	2577	4,4	8	2
Basilicata	107	2607	4,1	9	-
Calabria	104	2799	3,7	12	1
Sicilia	108	2787	3,9	15	17
Sardegna	77	2441	3,1	10	15
gnato un nuovo corotipo sulla base delle informazioni desunte da: Aeschimann et al. (2004), Bartolucci et al. (2018), Euro+Med Data Base (2006), Poldini (1991) e Tutin et al. (1964-80).
Al corotipo Appennino-Balcanico sono stati assegnati i taxa presenti solo nel territorio delimitato dai seguenti confini fisici (Pezzetta, 2010): a) per la Penisola Italiana, le isole e l'arco appenninico dalla Liguria all'Aspromon-te; b) per la Penisola Balcanica, Creta, le isole dell'Egeo e il territorio continentale a sud dell'asse fluviale che va dalle sorgenti della Sava alle foci del Danubio e dal Mar Nero all'Adriatico-Ionio. Al corotipo Subendemico sono stati assegnati i taxa contraddistinti da un areale che da qualche regione del territorio italiano sconfina in alcune zone dei Paesi vicini.
Al fine di avere maggiore chiarezza sui quadri distri-butivi, si è calcolato Il valore medio di presenza (Vm) nelle varie parti d'Italia (nord, centro, sud e isole), otte-nuto sommando i dati regionali/il numero delle regioni.
Per quantificare la somiglianza tra le distribuzioni dei singoli taxa nelle regioni italiane è stata condotta una classificazione numerica delle regioni stesse, su dati di presenza-assenza, utilizzando il legame medio come
algoritmo di clustering e l'indice di Soerensen come coefficiente di distanza (Fig. 1).
RISULTATI E DISCUSSIONE
L'elenco floristico comprende 272 taxa infragenerici, corrispondenti a circa il 3,3 % della flora italiana, che secondo Bartolucci et al. (2018) ammonta a 8195 taxa. Essi sono ripartiti in 40 generi, tra cui il più ricco è Salvia con 29 taxa, seguito da Teucrium con 23, Clinopodium con 21, Thymus con 19, Lamium con17, Micromeria e Nepeta con 12, Mentha con 11, Ajuga con 10, Galeopsis e Scutellaria con 9 e poi tutti gli altri con valori inferiori.
I taxa spontanei, non avventizi si ripartiscono in 5 subfamiglie che, tenendo conto delle classificazioni proposte da Harley et al. (2004), Li et al. (2016) e Li & Olmstead (2017), comprendono i seguenti generi:
1.	Viticoideae: Vitex;
2.	Ajugoideae: Ajuga, Teucrium e Clerodendrum;
3.	Scutellarioideae: Scutellaria;
4.	Lamioideae: Acanthoprasium, Ballota, Betonica, Chaiturus, Galeopsis, Lamium, Leonurus, Marru-bium, Melittis, Molucella, Phlomis e Stachys;
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5. Nepetoideae: Clinopodium, Dracocephalum, Glechoma, Hyssopus, Lavandula, Lycopus, Melissa, Micromeria, Mentha, Nepeta, Ocimum, Origanum, Perilla, Prunella, Salvia, Satureja, Thymbra, Thymus e Ziziphora.
Solo 15 specie sono presentí in tutte le regioni italiane: Ajuga reptans, Lamium amplexicuale, L. purpu-reum, Lycopus europaeus. Marrubium vulgare, Mentha aquatica subsp. aquatica, M. pulegium subsp. pulegium, M. spicata, Nepeta cataria, Prunella laciniata, P. vulgaris subsp. vulgaris, Salvia rosmarinus, Stachys annua subsp. annua, Teucrium chamaedrys subsp. chamaedrys e T. montanum.
I	seguenti taxa sono presenti in tutte le regioni peninsu-lari e in qualche caso anche in Sicilia o Sardegna: Betonica officinalis, Clinopodium nepeta subsp. nepeta, C. nepeta subsp. sylvaticum, C. vulgare subsp. vulgare, Galeopsis an-gustifolia, Lamium maculatum, Mentha longifolia e Stachys sylvatica. Le altre entità hanno una distribuzione variabile che puo comprendere una o più regioni.
La maggior presenza di taxa si registra nell'Italia settentrionale con 173 unità che corrispondono a circa il 63,6 % del totale delle lamiacee italiane. Nell'Italia Centrale (dalla Toscana all'Abruzzo) sono presenti 162 taxa (59,5 %) e nell'Italia meridionale 158 (58,1 %) e in Sicilia e Sardegna 125 (45,9 %).
II	valore medio di presenza (Vm) è più alto nell'Italia Centrale con 117,2. Nell'Italia Meridionale è di 111, nell'Italia settentrionale è di 102,6 e nelle isole 92,5.
La regione più ricca (Tab. 1) è l'Abruzzo con 135 taxa ed è seguita da: Toscana (130); Campania (128); Lazio (122), Emilia Romagna (117); Liguria e Puglia (114); Lombardia (110); Sicilia (108); Friuli Venezia Giulia e Basilicata (107); Veneto (106); Marche e Trentino Alto Adige (105); Calabria (104); Molise (102); Piemonte (100); Umbria (95); Sardegna (77); Valle d'Aosta che chiude con 63 taxa.
La classificazione (Fig. 1) mostra una maggiore affi-nità tra le regioni dello stesso settore geografico (Nord, Centro, Sud e isole). La Sicilia e la Sardegna, che dimo-strano la maggiore affinità in assoluto, sono nettamente separate dagli altri gruppi, un risultato riconducibile alle loro particolari vicende paleogeografiche. In vari settori e/o regioni, sono segnalate entità assenti in altri o che raggiungono un limite di distribuzione assoluto o circoscritto al territorio nazionale.
Nell'Italia nord-occidentale (Liguria) è presente la seguente entità stenoendemica assente in altre regioni e unica rappresentante del genere in Italia: Acantho-prasium frutescens. In una o più regione alpina centro-orientale (dalla Lombardia al Friuli Venezia Giulia) sono presenti in modo le seguenti entità assenti altrove: Salvia pratensis subsp. saccardiana, Stachys talbotii e Teucrium siculum subsp. euganeum. Nell'Italia Centrale è presente la seguente entità assente in altre regioni: Mentha requienii subsp. bistaminata. Nell' Italia Meridionale sono presenti le seguenti specie non segnalate
in altri settori della penisola: Lavandula austroapennina, Phlomis tenorei, Salvia ceratophylloides, Stachys recta subsp. tenoreana e Thymus picentinus.
I seguenti taxa sono presenti solo in Sardegna: Clinopodium sandalioticum, C. sardoum, Glechoma sardoa, Mentha requienii subsp. requienii, Micromeria cordata, Nepeta foliosa e Salvia desoleana. In Sicilia, invece sono presenti i seguenti taxa non segnalati in altre regioni: Clinopodium alpinum subsp. nebrodense, C. minae, C. raimondoi, Scutellaria rubicunda, Stachys germanica subsp. dasyanthes, Thymus praecox subsp. parvulus e T. richardii.
Le seguenti specie sono segnalate solo in una delle seguenti regioni italiane:
-	Piemonte: Galeopsis sulphurea e Scutellaria minor;
-	Lombardia: Plectranthus scutellarioides, Salvia reflexa e Stachys guillonii subsp. hyssopifolia;
-	Trentino Alto Adige: Dracocephalum moldavica, Salvia amplexicaulis, Stachys talbotii, Teucrium hircanicum e T. polium subsp. purpurascens;
-	Veneto: Teucrium siculum subsp. euganeum;
-	Friuli Venezia Giulia: Ballota nigra subsp. velutina, Clinopodium acinos subsp. villosum, C. einsele-anum, C. thymifolium, Salvia napifolia e Thymus illyricus;
-	Liguria: Acanthoprasium frutescens, Stachys rossii, Teucrium chamaedrys subsp. pectinatum e Prunella hyssopifolia;
-	Emilia Romagna: Dracocephalum parviflorum e Scutellaria albida. subsp. albida;
-	Toscana: Mentha requienii subsp. bistaminata, Salvia officinalis subsp. gallica e Stachys salisii;
-	Marche: Nepeta italica;
-	Abruzzo: Clinopodium graveolens, Mentha cervina e Thymus zygiformis;
-	Campania: Stachys recta subsp. tenoreana;
-	Puglia: Clinopodium serpyllifolium subsp. frutico-sum e Stachys cretica;
-	Calabria: Salvia ceratophylloides;
-	Sicilia: Ajuga chamaepitys subsp. suffrutescens, Clinopodium alpinum subsp. nebrodense, C. minae, C. raimondoi, Origanum onites, Salvia ca-nariensis, S. leucantha, S. microphylla, S. pinnata, Scutellaria rubicunda, Stachys germanica subsp. dasyanthes, S. perfoliata, Teucrium creticum, T. luteum, T. massiliense, Thymus praecox subsp. parvulus e T. richardii;
-	Sardegna: Clinopodium sandalioticum, C. sar-doum, Glechoma sardoa, Lamium garganicum subsp. corsicum, Mentha requienii subsp. requienii, Micromeria cordata, M. filiformis subsp. filiformis, Nepeta foliosa, Salvia desoleana, Satureja thymbra, Stachys brachyclada, S. corsica, S. germanica subsp. dasyanthes, Teucrium subspinosum e Thymus herba-barona.
I dati riportati dimostrano che le regioni insulari e quelle continentali di confine sono piu ricche di lamiacee endemiche ed assenti in altre regioni. Diverse entita
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nella penisola italiana sono a un limite assoluto del loro areale. Infatti:
-	raggiungono in Italia il limite settentrionale assoluto di distribuzione: Micromeria microphylla, Nepeta italica, Satureja montana subsp. variegata, Stachys arenaria subsp. arenaria, S. marrubiifolia, S. recta subsp. subcrenata, Thymus carstiensis, T. illyricus e T. zygiformis;
-	raggiungono in Italia il limite meridionale assoluto di distribuzione geografica: Clinopodium alpinum subsp. alpinum, C. nepeta subsp. nepeta, Draco-cephalum moldavica, Galeopsis angustifolia subsp. angustifolia, G. ladanum, Lamium garganicum subsp. corsicum, Stachys corsica e Thymus oeni-pontanus;
-	raggiungono in Italia il limite orientale assoluto di distribuzione: Ajuga chamaepitys subsp. suffrutescens, Galeopsis reuteri, Lamium flexuo-sum, Lavandula angustifolia, L. latifolia, Melittis melissophyllum subsp. albida, Mentha requienii subsp. bistaminata, M. suaveolens subsp. insularis, Micromeria marginata, Nepeta apulei, N. tuberosa. subsp. tuberosa, Prunella hyssopifolia, Stachys arenaria subsp. arenaria, S. brachyclada, S. guillonii subsp. hyssopifolia, S. heraclea, S. marrubiifolia, S. rossii, Teucrium chamaedrys subsp. pectinatum, T. lucidum, T. subspinosum, Thymus striatus subsp. acicularis e T. vulgaris subsp. vulgaris;
-	raggiungono in Italia il limite occidentale assoluto di distribuzione: Ajuga orientalis, Ballota nigra subsp. velutina, B. pseudodictamnus subsp. pseu-dodictamnus, Clinopodium suaveolens, C. thymifo-lium, Dracocephalum moldavica, Lamium bifidum subsp. balcanicum, L. flexuosum, L. garganicum subsp. striatum, Lycopus exaltatus, Marrubium incanum, M. peregrinum, Mentha microphylla, Mi-cromeria graeca subsp. fruticulosa, M. microphylla, M. thymifolia, Nepeta italica, N. nepetella subsp. nepetella, Origanum onites, Phlomis fruticosa, Salvia officinalis subsp. officinalis, S. virgata, Satureja subspicata subsp. liburnica, S. montana subsp. variegata, Scutellaria altissima, Stachys cretica, S. perfoliata, S. recta subsp. subcrenata, S. thirkei, S. tymphaea e Thymus carstiensis.
Altre entità in qualche regione raggiungono un limite distribuzionale non assoluto ma che riguarda solo il territorio peninsulare. In particolare, raggiungono il limite meridionale di distribuzione in:
-	Emilia Romagna: Clerodendrum bungej e Leonurus quinquelobatus;
-	Toscana: Ballota nigra subsp. nigra, Betonica hirsuta, Horminum pyrenaicum e Teucrium scorodonia;
-	Marche: Thymus pulegioides,
-	Lazio: Nepeta nepetella subsp. nepetella, Perilla frutescens e Teucrium botrys;
-	Abruzzo: Ajuga pyramidalis, Clerodendrum tri-chotomum, Lamium galeobdolon subsp. flavidum,
Satureja subspicata subsp. liburnica, Stachys thirkei, Teucrium scordium subsp. scordium e Thymus oenipontanus;
-	Molise: Betonica alopecuros subsp. divulsa e Salvia nemorosa subsp. nemorosa;
-	Campania: Chaiturus marrubiastrum, Clinopodium acinos subsp. acinos, C. nepeta subsp. ascendens, Galeopsis pubescens, Hyssopus officinalis subsp. officinalis, Lycopus exaltatus, Nepeta nuda subsp. nuda, Origanum vulgare subsp. prismaticum, Salvia pratensis subsp. pratensis, Scutellaria altissima, Stachys marrubiifolia, S. montana subsp. montana e S. recta subsp. recta;
-	Puglia: Ajuga genevensis, Clinopodium alpinum subsp. alpinum, C. suaveolens, Galeopsis specio-sa, Marrubium peregrinum, Scutellaria hastifolia, Stachys palustris e Thymus vulgaris subsp. vulgaris;
-	Basilicata: Ballota nigra subsp. meridionalis, La-mium album subsp. album, L. garganicum subsp. striatum, Melittis melissophyllum subsp. melis-sophyllum, Salvia verticillata subsp. verticillata, S. virgata, Stachys recta subsp. subcrenata, Thymus moesiacus e T. striatus subsp. acicularis;
-	Calabria: Betonica officinalis, Clinopodium vulgare subsp. vulgare, Galeopsis angustifolia subsp. angustifolia, G. ladanum, Glechoma hederacea, Hyssopus officinalis subsp. aristatus, Lamium bifidum subsp. bifidum, L. galeobdolon subsp. montanum, L. garganicum subsp. garganicum, L. garganicum subsp. laevigatum, L. maculatum, Lavandula au-stroapennina, Melissa officinalis subsp. officinalis, Mentha longifolia, Salvia glutinosa, S. haematodes, Satureja montana subsp. montana, Scutellaria alpina subsp. alpina, S. galericulata, Stachys arenaria subsp. arenaria, S. germanica subsp. germanica, S. germanica subsp. salviifolia, S. heraclea, S. recta subsp. grandiflora, S. tymphaea, Thymus praecox subsp. polytrichus e Ziziphora capitata subsp. capitata;
-	Sicilia: Ajuga chamaepitys. subsp. chamaepitys,
A.	iva subsp. iva, A. orientalis, A. reptans, A. te-norei, Ballota hispanica, B. nigra subsp. uncinata,
B.	pseudodictamnus subsp. pseudodictamnus, Clinopodium alpinum subsp. meridionale, C. nepeta subsp. nepeta, C. nepeta subsp. spruneri, C.
C.	nepeta subsp. sylvaticum, C. vulgare L. subsp. arundanum, Lamium amplexicaule, L. garganicum subsp. laevigatum, L. hybridum, L. purpureum, Lavandula latifolia, L. multifida, L. stoechas, Marrubium alysson, M. incanum, Melissa officinalis subsp. altissima, Melittis melissophyllum subsp. albida, Mentha aquatica subsp. aquatica, M. microphylla, M. pulegium. subsp. pulegium, M. spicata, Micromeria graeca subsp. garganica, M. graeca subsp. fruticulosa, M. graeca subsp. graeca, M. juliana, Mi. microphylla, M. nervosa, Moluccella spinosa, Nepeta cataria, Origanum majorana, O. vulgare
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subsp. vulgare, Phlomis fruticosa, P. herba-venti subsp. herba-venti, Prunella laciniata, P. vulgaris subsp. vulgaris, Salvia argentea, S. clandestina, S. microphylla, S. officinalis subsp. officinalis, S. rosmarinus, S. sclarea subsp. sclarea, S. verbenaca, Stachys annua subsp. annua, S. byzantina, S. italica, S. major, S. ocymastrum, S. romana, S. sylvatica, Teucrium campanulatum, T. chamaedrys subsp. chamaedrys, T. flavum. subsp. flavum, T. fruticans. subsp. fruticans, T. scordium. subsp. scordioides, T. siculum subsp. siculum, T. spinosum, Thymbra capitata, Thymus longicaulis subsp. longicaulis. T. spinulosus e Vitex agnus-castus.
Raggiungono il limite settentrionale di distribuzione nelle seguenti Regioni:
-	Valle d'Osta: Salvia aethiopis;
-	Piemonte: Galeopsis reuteri, Hyssopus officinalis subsp. officinalis, Lamium garganicum subsp. laevi-gatum, Lycopus exaltatus, Nepeta nepetella subsp. nepetella, N. nuda subsp. nuda, Salvia clandestina, S. nemorosa subsp. nemorosa, Satureja montana. subsp. montana e Scutellaria columnae subsp. columnae;
-	Lombardia: Ballota nigra subsp. uncinata, Gale-opsis segetum, Lamium bifidum subsp. bifidum, L. hybridum, Salvia rosmarinus, S. verbenaca, Stachys arvensis, S. montana, S. recta. subsp. grandiflora e S. montana subsp. montana;
-	Trentino Alto Adige: Ajuga chamaepitys subsp. chamaepitys, A. genevensis, A. reptans, A. pyramidalis, Ballota nigra subsp. meridionalis, B. nigra subsp. nigra, Betonica hirsuta, B. officinalis, Galeopsis angustifolia subsp. angustifolia, G. bifida, G. ladanum, G. pubescens, G. speciosa, G. tetrahit, Glechoma hederacea, G. hirsuta, Horminum pyreniacum, Hyssopus officinalis subsp. aristatus, Lamium album subsp. album, L. amplexicaule, L. maculatum, L. orvala, L. purpureum, Lavandula latifolia, Leonurus cardiaca, Lycopus europaeus, Marrubium vulgare, Melittis melissophyllum subsp. melissophyllum, Mentha aquatica, M. arvensis, M. longifolia, M. pulegium subsp. pulegium, Melissa officinalis subsp. officinalis, Origanum vulgare subsp. prismaticum, Prunella laciniata, P. vulgaris subsp. vulgaris, Salvia glutinosa, S. haematodes, S. officinalis subsp. officinalis, S. pratensis. subsp. pratensis, S. verticillata. subsp. verticillata, S. viridis, Satureja hortensis, Stachys alpina subsp. alpina, S. annua subsp. annua, S. germanica. sub-sp. germanica, S. germanica subsp. salviifolia, S. montana subsp. montana, S. palustris, S. sylvatica, Scutellaria alpina subsp. alpina, S. galericulata, Thymus oenipontanus, T. praecox subsp. polytri-chus, T. pulegioides, T. pseudochamaedrys, Teucrium botrys, T. chamaedrys subsp. chamaedrys, T. montanum e T. scordium subsp. scordium;
-	Veneto: Micromeria juliana e Phlomis fruticosa;
-	Friuli Venezia Giulia: Clinopodium vulgare subsp. arundanum, Satureja montana. subsp. variegata, Stachys maritima e Thymus longicaulis subsp. longicaulis;
-	Liguria: Ajuga iva subsp. iva, A. orientalis, Lavan-dula stoechas subsp. stoechas, Micromeria graeca subsp. graeca, Stachys ocymastrum e Teucrium fruticans subsp. fruticans;
-	Emilia Romagna: Clinopodium alpinum subsp. meridionale, C. nepeta subsp. spruneri, Melissa officinalis subsp. altissima, Salvia virgata, Stachys heraclea, S. thirkei, S. tymphaea, Thymus moe-siacus, T. striatus subsp. acicularis e Ziziphora capitata subsp. capitata;
-	Toscana: Mentha suaveolens subsp. insularis, Salvia microphylla, Stachys marrubiifolia, S. major, Teucrium marum, T. siculum subsp. siculum e Thymbra capitata;
-	Marche: Betonica alopecuros subsp. divulsa, Lamium flexuosum e Teucrium flavum subsp. glau-cum;
-	Lazio: Salvia fruticosa subsp. thomasi e Thymus spinulosus;
-	Abruzzo: Ajuga chamaepitys subsp. chia, A. teno-rei, Ballota hispanica e Clinopodium suaveolens.
Tab. 2: Distribuzione delle Lamiaceae della flora italiana per tipo di habitat.
Tab. 2: Razširjenost ustnatic v italijanski flori glede na tip habitata.
Tipo di habitat	Numero taxa
Margini di boschi	5
Cespuglieti e Siepi	25
Prati e Campi coltivati	25
Boschi di varie tipologie	28
Incolti e Ruderi	71
Radure di boschi	11
Macchie e boscaglie	14
Garighe	19
Ambienti umidi	40
Prati aridi	80
Pascoli alpini e subalpini	15
Ghiaioni, Macereti e Pietraie	30
Rupi e sue fessure	61
Dune	5
Pascoli sassosi	39
Muri	7
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-	Molise: Melittis melissophyllum subsp. albida e Micromeria graeca subsp. garganica;
-	Campania: Lavandula austroapennina, Micromeria graeca subsp. consentina, M. graeca subsp. longi-flora e Stachys arenaria subsp. arenaria;
-	Puglia: Lamium garganicum subsp. garganicum, Marrubium alysson, Micromeria nervosa, Mo-luccella spinosa, Teucrium campanulatum e T. spinosum.
Per gli altri taxa non è stato possibile affermare con certezza i limiti di distribuzione.
Le Lamiaceae della flora italiana crescono in habitat molto diversi (Tab. 2). Oltre 100 taxa si rinvengono nei prati e pascoli di vario tipo (aridi, umidi, sassosi, etc.) e generalmente in ambienti aperti e soleggiati tra cui le garighe e i consorzi terofitici effimeri. Non mancano tuttavia le specie che prediligono gli habitat riparati e freschi dei boschi di varie tipologie, delle macchie e dei cespuglieti. Oltre 60 taxa si rinvengono tra le rupi, pie-traie e ghiaioni di vario tipo, ambiti inospitali ove solo pochi organismi specializzati riescono a sopravvivere.
Dalla Tabella 3 emerge che sono presenti in tutte le fasce altitudinali comprese tra il livello del mare e oltre 2400 metri, con molte entità presenti in più fasce. La maggior ricchezza si ha nella fascia che va da 100 a 900 m con 210 taxa (77,2 %). Ad altitudini maggiori e minori diminuiscono: nelle fasce tra 900-1800 m., 1800-2400 m. e oltre 2400 metri sono presenti rispetti-vamente 151, 47 e 11 taxa e in quella tra 0 e 100 metri ne sono presenti 172.
La Tabella 4 riporta i risultati dell'analisi fitogeogra-fica, con la ripartizione percentuale dei vari elementi corologici. I taxa si ripartiscono in 7 contingenti floristi-ci tra cui domina il mediterraneo con 82 taxa. Seguono i contingenti: europeo (53), endemico (49), eurasiatico (46), avventizio (31), nordico (7) e atlantico (4). Al contingente endemico appartengono entità con distribuzione molto ristretta: i taxa endemici in senso stretto (stenoendemici) presenti solo in una o più regioni italiane e i taxa subendemici. Esso dimostra innanzitutto che il territorio nazionale anche per le lamiacee è un ambito
Tab. 3: Distribuzione delle Lamiaceae in base all/altitudine.
Tab. 3: Razširjenost ustnatic glede na nadmorsko višino.
Altitudine in metri	Numero taxa
0-100	172
100-900	215
900-1800	151
1800-2400	47
Oltre 2400	11
di speciazioni floristiche. Inoltre: è più rappresentato in Sicilia e Sardegna con 30 taxa di cui alcuni presenti anche in altre regioni centro-meridionali; è presente con 19 taxa nell'Italia meridionale, 10 nell'Italia Centrale e 9 nell'Italia settentrionale. Per quanto riguarda gli altri contingenti floristici si ossserva quanto segue:
-	il contingente mediterraneo è più rappresentato in Sicilia e Sardegna con 56 taxa e mostra un trend decrescente dalle regioni meridionali a quelle settentrionali;
-	i contingenti avventizio, eurasiatico ed europeo hanno un trend decrescente da nord a sud;
-	il contingente nordico è rappresentato da un pari di numero di taxa da nord a sud, mentre si riduce in Sicilia e Sardegna:
-	il contingente mediterraneo-atlantico registra la maggior ricchezza nell'Italia settentrionale, se-guono Sicilia e Sardegna e poi con valori identici l'Italia centrale e meridionale.
Le origini della famiglia
Dove e quando le Lamiaceae si originarono e in quale epoca raggiunsero la penisola italiana? Nelle ere geolo-giche passate, vegetali provenienti da tutte le direzioni raggiunsero i territori emersi che oggi costituiscono l'Italia sfruttando le connessioni territoriali esistenti e/o in pre-senza di una barriera, con la dispersione a lunga distanza che affida la diffusione degli organi riproduttivi al vento, agli animali, agli uccelli, alle correnti marine e all'uomo. La ricostruzione delle ere geologiche in cui le migrazioni avvennero non è facile: ancora oggi nonostante i progres-si delle conoscenze biogeografiche permangono molti lati oscuri. Vari spunti sono stati forniti dalle ricerche di biologia molecolare e sistematica filogenetica con cui è stato possibile: 1) ricostruire gli alberi genealogici di vari taxa; 2) individuare i centri d'origine, i territori in cui sono presenti i taxa più antichi, i processi di speciazione e le rotte migratorie seguite per colonizzare varie parti del globo. Di solito, per la stima dei periodi temporali dei processi e meccanismi evolutivi si utilizza il cosiddetto orologio molecolare, che prende in considerazione i tempi medi di evoluzione di alcune sostanze proteiche. Esso si basa sul fatto che le mutazioni genetiche avvengono con frequenze generalmente costanti: tenendo conto del numero di variazioni riscontrate, è possibile stimare il tempo trascorso dal momento in cui ebbero inizio (Zuckerkandl & Pauling, 1962). In anni recenti, l'uso di nuovi algoritmi ed elaboratori più potenti ha consentito alla filogenetica molecolare di fare enormi progressi: ora è possibile elaborare ipotesi complesse sulle relazioni filogenetiche, i modelli biogeografici di dispersione, espansione, vicarianza e transizioni evolutive riguardanti gruppi che vanno da specie strettamente correlate a intere famiglie di piante.
Un gruppo di organismi più o meno affini si diversifico e assunse i propri caratteri distintivi, da un antenato
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comune presente in una o più aree geografiche definite "centri di origine". Da tali ambiti l'antico progenitore si diffuse colonizzando territori in cui talvolta s'innescano mutazioni genetiche che portano alla formazione di nuovi taxa. Di conseguenza, oltre al centro d'origine primario si possono avere altri secondari e post-secon-dari ove sono avvenuti e avvengono i processi di diver-sificazione biologica. Spesso si fa coincidere il centro di origine con il territorio in cui una famiglia di organismi viventi raggiunge la maggiore diversità, sono presenti entità con caratteristiche più ancestrali o si sono trovati reperti fossili più antichi.
Nel caso delle Lamiaceae, i reperti fossili conosciuti non consentono di individuare il centro d'origine e l'antenato da cui discendono, ma si rivelano utili per af-fermare che suoi taxa popolavano certe regioni terrestri durante precise ere geologiche. Alcuni di essi sono i se-guenti: frutti di resti di Gmelina tertiara Bande di fine del Cretaceo inizio Paleocene (circa 67-64 Ma), rinvenuti in India (Wheeler et al., 2017); polline di Nepetoideae di 49 Ma e semi di Melissa della prima metà dell'Oligoce-ne rinvenuti in Germania; polline di Ocimumpollenites indicus risalente alla prima metà dell'Eocene (circa 49 Ma) rinvenuto nella regione indiana del Rajasthan (Kar, 1996); Ajuginucula smithii Reid et Chandler e Melissa parva Reid et Chandler del medio Oligocene (circa 28,4 milioni di anni fa) rinvenuti a Bembridge Inghilterra (Martinez-Millan, 2010); resti di Teucrium sibiricum L. del Tardo Oligocene (28,4-23 Ma) rinvenuto nella Siberia occidentale (Dorofeev, 1963); frutti di Lycopus cf. antiquus Reid 1920 del Miocene rinvenuti a Nowy Sacz (Polonia) (tancucka-Srodoniowa); resti di Origanum vulgare risalenti al Medio Miocene (16-13,8 Ma), rinvenuti in Germania (Mai, 2001); resti di Stachys lati-carpa e Lamium sp. del Medio Miocene (13,8-11,6 Ma) rinvenuti in Germania (Roy & Lindqvist, 2015); frutti di Teucrium della metà del Miocene rinvenuti a Fasterholt e S0by (Danimarca) (Friis, 1985); semi di Glechoma hederacea, Lycopus sp., L. cholmechensis Wieliczk., Mentha pliocenica Dorof., Stachys cf. pliocenica Dorof., Teucrium pripiatense (Dorof.) Wieliczk. e T. tatjanae Nikit. di fine Pliocene inizio Pleistocene rinvenuti in Bielorussia (Velichkevih & Zastawniak, 2003); semi di Ajuga antiqua C. Reid & E. Reid del Pliocene-Pleistocene rinvenuti in Italia (Martinetto, 2015); semi dl Teucrium pripiatense del Pliocene rinvenuti in Germania (Mai, 2007). In conclusione i dati riportati, consentono di af-fermare che: i fossili più antichi risalgono a circa 67-64 Ma e sono stati rinvenuti in India, all'epoca un subcontinente isolato che si allontanava dalla costa orientale dell'Africa e si avvicinava all'Asia; in parte dei territori che oggi costituiscono l'Europa centro-settentrionale, le Lamiaceae erano presenti a partire da 49 Ma; la subfamiglia Nepetoidae è la più antica. Tenendo conto di tali dati si puo sostenere che in India o più in generale nel continente asiatico è situato il centro d'origine delle Lamiaceae?
Tab. 4: Corotipi delle Lamiaceae della flora italiana. Tab. 4: Horotipi ustnatic v italijanski flori.
Elementi geografici	Numero taxa	%
Endemico e Subendemico	49	18,0
Endémico	37	
Subendemico	12	
Mediterraneo	82	30,1
Eurimediterraneo	20	
Stenomediterraneo	26	
Mediterraneo-Occidentale	19	
Mediterraneo-Orientale	7	
Mediterraneo Montano	1	
Sud-Mediterraneo	1	
Nord-Est-Mediterraneo	3	
Sud-Est-Mediterraneo	1	
Sud-Ovest-Mediterraneo	3	
Nord-Ovest-Mediterraneo	2	
Eurasiatico	46	16,9
Eurasiatico s.s.	15	
Europeo-Caucasico	11	
Eurosiberiano	3	
Sud-Europeo-Sud-Siberiano.	5	
Pontico	3	
Paleotemperato	4	
Mediterraneo-Turaniano	4	
Mediterraneo-Pontico	1	
Nordico	7	2,6
Circumboreale	7	
Europeo	53	19,5
Europeo s.s.	1	
Centro-Europeo	3	
Orofita Sud-Ovest-Europeo	3	
Orof. Sud-Europeo	7	
Orofita Sud-Est- Europeo	6	
Illirico	2	
Sud-Est-Europeo	9	
Ovest-Europeo	2	
Appennino-Balcanico	17	
Est-Alpino-Dinarico	2	
Sud-Europeo	1	
Atlantico	4	1,5
Mediterraneo-Atlantico	1	
Subatlantico	3	
Avventizio	31	11,4
Avventizio	31	
Totale	272	100
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Ad avviso di Harley et al. (2004) la famiglia si origino durante il Cretaceo. Wu & Li (1982) sostengono che la famiglia è originaria della Cina meridionale o dell'Indomalesia e le subfamiglie più primitive sono le Prostanthcroideae e le Ajugoideae. Hedge (1992) invece sostiene che l'Asia centrale e Sud-Occidentale possono essere considerati centri di origine primaria da cui le lamiacee si diffusero verso altri territori ove i processi di diversificazione continuarono, tra i quali: il Bacino del Mediterraneo, l'Africa australe, l'America occidentale, le isole oceaniche e altre zone del continente asiatico. Nell'Asia sud-occidentale sono presenti 66 generi e circa 1100 specie (Hedge, 1992). Nel suo ambito l'Iran con 46 generi e 406 specie (Jamzad, 2013) e la Turchia con 47 generi e 782 specie (Celep & Dirmenci, 2017), hanno il maggior numero di taxa. Per Manafzadeh et al. (2014) la regione irano-turanica è un importante hot spot di diversità biologica-evolutiva delle xerofite da cui i generi Salvia, Nepeta, Thymus e Scutellaria si originarono e diffusero.
Ipotesi su periodi e rotte migratorie
Al fine di elaborare ipotesi attendibili sui periodi e rotte migratorie seguite dalle lamiacee per raggiungere la penisola italiana, si prenderanno in considerazione vari eventi paleogeografici che dal Terziario all'Olo-cene, si sono susseguiti contribuendo alla formazione dell'attuale assetto floristico-vegetazionale.
Le migrazioni del Terziario
Durante il Terziario, da circa 65 Ma a 2 Ma, ini-ziarono gli eventi che portarono alla formazione della penisola italiana e gli sconvolgimenti paleogeografici furono accompagnati da: la comparsa di famiglie di piante e animali, colonizzazione di nuovi territori ed estinzioni. La diffusione e formazione delle lamiacee nella penisola italiana durante il Cenozoico avvenne in tre diversi periodi: uno più antico che coinvolse generi a distribuzione paleotirrenica e paleoegeica; uno intermedio nel Messiniano; l'ultimo più recente nel Pliocene.
Nella prima fase più antica di inizio Oligocene, circa 34 Ma, la zona dove in seguito sorgerà l'Italia era occupata da un mare tropicale circondato a Ovest dal blocco iberico-provenzale cui era unita la microzolla sardo-corsa, a Nord ed Est da terre che costituivano la Dinaride e a Sud dall'Apulide o Egeide, un subcontinente comprendente territori emersi appartenenti alla Puglia attuale, la penisola balcanica e l'Anatolia. All'epoca l'arco calabro-peloritano, la Sardegna e la Corsica costituivano un unico blocco collegato alla placca europea in un'area corrispondente all'attuale Provenza-Linguadoca. Anche le Baleari e parte del Nord-Africa erano legate alla placca europea in un ambito territoriale compreso tra la Spagna meridionale e la Catalogna e facevano parte di un lungo corrugamento
detto massiccio ercinico che andava dalla Spagna sino a Vienna (Bosellino, 2005). Durante il Tardo Oligocene il territorio inizio a frammentarsi, si formarono varie microplacche tra cui quella corso-sardo-calabra che si stacco, subi una rotazione e lentamente si porto nella posizione attuale. L'arco calabro-peloritano dopo aver accompagnato alla deriva di Corsica e Sardegna, continuo a spostarsi verso sud- est (Bosellino, 2005, op. cit.). Secondo Furon (1959), invece, tra l'Oligocene e l'Eocene esisteva un subcontinente chiamato Thyrrenis o Massiccio Iberico-Tirrenico che incorporava oltre ai territori suddetti anche l'Arcipelago toscano e varie paleoisole ora unite all'Italia centrale: il Promontorio del Circeo, il Monte Argentario e le Colline Metallifere. Le connessioni territoriali tra il blocco sardo-corso, l'arcipelago toscano, l'area ligure-provenzale, le Baleari e la penisola iberica favorirono le migrazioni floristiche. In seguito le piante presenti nell'area, con il lungo isolamento geografico si diversificarono in nuove specie. A tali cause sono da attribuire le vicarianze foristiche tra le regioni peninsulari da un lato e, Nord-Africa e/o Europa occidentale dall'altro. La distribuzione di Micromeria filiformisis s.l. e Prunella hyssopifolia potrebbe riflettere quest'evento paleogeografico. Altre prove di antichi legami con la penisola iberica sono fornite dal gruppo di Thymus richardii che comprende: T. richardii Pers. subsp. richardii presente a Minorca e in alcune zone dell'ex Jugoslavia; T. richardii subsp. nitidus (Guss.) Jalas endemico dell'isola di Marettimo; T. richardii subsp. ebusitanus (Font Quer) Jalas presente a Ibiza e T. richardii subsp. vigoi Riera, Gilames & Rosselló della penisola iberica. Anche Nepeta foloisa, affine a N. multibracteata Desf. (Valsecchi & Corrias, 1973) potrebbe tetstimoniare tali antichi legami.
Durante il Miocene: 1) l'isolamento geografico dell'arco calabro-peloritano favori la formazione di vari endemismi condivisi tra Calabria e Sicilia tra cui Scutellaria columnae subsp. gussonei; 2) con la deriva delle microzolle terziarie, diverse entità mediterraneo-occi-dentali raggiunsero i territori emersi della Sicilia da cui si espansero verso altre regioni dell'Italia Meridionale.
Altre migrazioni floristiche avvennero attraverso l'Egeide, il subcontinente che univa l'Asia minore con la Grecia, il Gargano, Salento e altri territori emersi. Secondo Gridelli (1950) nel Miocene il Gargano era collegato alla Dalmazia, il Salento alla Grecia-Albania e tra le due zone esisteva un tratto di mare definito solco transegeico. Le ricerche successive (De Giuli et al., 1987; Rogl, 1999, Patacca et al., 2008), sia pur con sfumature diverse, confermano l'esistenza di ponti territoriali diretti tra varie parti emerse della Puglia e la penisola balcanica tra fine Oligocene-inizio Miocene e durante il Langhiano. Francini Corti (1966) definí paleoegeiche le specie che varcarono l'Adriatico miocenico. Tra esse: Phlomis fruticosa, Salvia triloba (sin. Salvia fruticosa) e Satureja cuneifolia. Probabilmente anche altre lamiacee di origini orientali varcarono l'Adriatico miocenico, tra
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cui gli antenati di Lamium garganicum, Micromeria gra-eca e Stachys italica che proseguirono la rotta migratoria lungo l'Appennino meridionale e raggiunsero la Sicilia.
L'epoca successiva in cui avvennero nuove ondate migratorie, speciazioni, vicarianze, etc. è il Messiniano tra 7 e 5 Ma. Nel suo corso si sollevo la soglia di Gibilter-ra, s'interruppero i collegamenti con l'oceano Atlantico, il Bacino del Mediterraneo si prosciugo a causa della forte evaporazione e si aprirono collegamenti territoriali che favorirono le migrazioni foristiche (Bocquet et al., 1978). In questo periodo si suppone esistessero ponti terrestri che univano: il Nord-Africa e la Sicilia con, da un lato Sardegna, Corsica, Liguria e Toscana e dall'al-tro con Calabria, l'Appennino e quest'ultimo con la penisola balcanica. Il clima caldo-arido che s'instauro favori la diffusione di piante steppiche, xerofile e alofite. Ad avviso di Pignatti (1994) all'epoca, piante d'origine orientale con spiccate caratteristiche xerotermofle, capaci di attecchire su suoli molto salati, raggiunsero i territori emersi della penisola italiana, percorrendo un lungo corridoio che univa il Nord-Africa con la penisola iberica, l'arco pirenaico-alpino-appenninico o il sistema sardo-corso. Bonanni (2018) sostiene che all'epoca si diffusero e differenziarono vari arbusti tra cui quelli appartenenti ai seguenti generi di lamiacee: Clinopo-dium, Hyssopus, Lavandula, Melissa, Mentha, Ocimum, Origanum, Phlomis, Satureja e Thymus.
La disgiunzione degli areali di Mentha suaveolens subsp. insularis, Teucrium marum, T. massiliense, T. subspinosum e Thymus herba-barona potrebbe essere la conseguenza sia delle derive mioceniche sia delle migrazioni foristiche del Messiniano.
Nel periodo in esame è ipotizzabile che dal Nord-Africa raggiungessero la Sicilia, la Sardegna e altre regioni peninsulari diversi taxa e loro antenati di origini mediterranee sud-occidentali tra cui: Ajuga chamaepi-tys subsp. suffrutescens, Clinopodium alpinum subsp. meridionale, Lavandula multifda, L. stoechas, Nepeta apulei, N. tuberosa subsp. tuberosa, Stachys arenaria, S. brachyclada, S. glutinosa, Teucrium fruticans, T. lucidum e l'antenato del gruppo di Teucrium siculum. Si puo ipotizzare che alcune specie del gruppo appartengano alla corrente migratoria floristica sud-occidentale che secondo La Valva (1992), durante il Cenozoico col-legava la penisola iberica con l'Africa settentrionale, l'Algeria, la Sicilia e l'Appennino meridionale. È pos-sibile che all'epoca sia esistito anche un collegamento diretto o attraverso il Nord-Africa della Sicilia con la penisola anatolica, le isole egee e/o la Grecia centrale che permise la migrazione di Ajuga orientalis, Mentha microphylla, Origanum onites, Salvia fruticosa s.l., Stachys perfoliata, Teucrium creticum e dell'antenato di Scutellaria rubicunda.
Al Messiniano o altra epoca imprecisata del Terziario potrebbero risalire le affinità floristiche esi-stenti tra le Alpi centro-occidentali e il Mediterraneo Orientale che documentano: la discendenza da ante-
nati comuni che popolavano l'Europa meridionale e il Bacino del Mediterraneo; entità orientali migrate in direzione occidentali seguendo direttrici sconosciute. A questa categoria di taxa appartengono: Micromeria marginata affine a M, croatica (Pers.) Schott presente nella penisola balcanica e il genere Acanthoprasium costituito da due specie presenti rispettivamente nelle Alpi Marittime e a Cipro, Ad avviso di Martini (1984) i taxa di Acanthoprasium si originarono da un antenato comune che nel Miocene occupava le terre emerse del Mediterraneo; la trasgressione marina post- messiniana porto all'isolamento delle popolazioni e alla loro di-versificazione.
Durante il periodo successivo del Pliocene che inizio circa 5,3 Ma e si concluse attorno a 2,5 Ma, si riapri
10	stretto di Gibilterra, il Bacino del Mediterraneo si riempi, si ebbe la progressiva formazione della penisola italiana che emerse prima come arcipelago e poi come sistema montuoso unitario, un lembo del continente Sud-Egeide si separo dalla penisola balcanica per unirsi all'Appennino meridionale e la temperatura media della terra inizio a scendere producendo un clima più secco che contribuí a trasformare la vegetazione esistente. Le foreste tropicali di laurisilve si diradarono e in varie parti furono sostituite dai boschi a sclerofille più adatti al clima arido che si era formato. Di conseguenza altre ondate migratorie e processi di diversificazione portarono alla formazione di nuovi assetti vegetazionali. In questo periodo varie entità centro-europee e nordiche iniziarono
11	processo di colonizzazione lungo la penisola italiana. La scomparsa dei ponti terrestri del Messiniano, causo l'isolamento geografico degli organismi viventi cui segui la diversificazione di piante d'origine mediterranea e di diversi taxa endemici tra cui molti appenninici. Pignatti (1994) considera Ajuga tenorei un'entità appartenente al gruppo delle specie endemiche appenniniche altomontane che si formo verso la fine del Terziario quando la catena emerse dal mare e fu colonizzata da piante provenienti da est e ovest. I reperti fossili analizzati da Martinetto (1995) confermano che durante il Pliocene, il genere Ajuga aveva colonizzato l'Italia e avvalorano l'ipotesi di Pignatti. Tra la fine del Miocene e l'inizio del Pliocene, ad avviso di Favarger & Robert (1994) dalla branca meridionale della flora arcto-terziaria si originarono vari taxa tra Horminum pyrenaicum e Stachys alopecurus.
Potrebbe essere iniziato durante il Pliocene anche il processo di diversificazione che porto alla formazione di Stachys salisii, da Borzatti De Loewenstern & Mannocci (2008) considerata un'entità apoendemica originatasi per poliploidizzazione da un taxon diploide diffuso nelle zone vicine del complesso sardo-corso e dell'Arcipelago Toscano. Stachys salisii e l'entità simile S. corsica hanno notevoli affinità con taxa di origine orientale. Il loro antenato probabilmente nel Messinia-no raggiunse i territori emersi della penisola italiana e durante il Pliocene inizio a diversificarsi.
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Le migrazioni pleistoceniche
Nel Pleistocene ci fu un'alternanza di periodi glacia-li freddi e fasi calde che influenzarono profondamente la biodiversità del Mediterraneo. Durante le fasi fredde: la temperatura media delle zone temperate era di circa 10° inferiore a quella attuale; lungo la penisola italiana, il limite delle nevi perenni toccava 1300 metri d'altitu-dine; il livello marino si abbasso; si connessero tra loro territori ora separati dal mare: la Sicilia con la Calabria, la Sardegna con la Corsica, varie isole dell'Arcipelago toscano con la terraferma e vaste zone appartenenti alle due penisole circumadriatiche. A causa di cio si produssero estinzioni di specie terziarie, accantonamenti, formazione di nuove specie, disgiunzioni e nuove ondate migratorie. Nei paesaggi frammentati delle zone continentali e delle isole mediterranee s'innesco la speciazione allopatrica tramite selezione e/o deriva genica (Thompson, 2005). Le migrazioni floristiche met-tendo in contatto piante di diverse origini, favorirono l'allopoliploidia ossia l'ibridazione tra specie seguita da poliploidia. Gli ibridi superando la condizione di steri-lità, iniziarono a riprodursi e si diffusero conquistando nuovi territori. A tal proposito, secondo letswaart (1980), tra fine Pliocene e il Pleistocene vari taxa del genere Origanum, migrarono, vennero in contatto, s'ibridarono e formarono nuove specie.
La sopravvivenza di molti organismi viventi d'origine terziaria avvenne in aree definite centri di rifugio. Ad avviso di Médail & Diadema (2009) nel Bacino del Mediterraneo ne sono individuabili 52 di cui 32 nel settore occidentale, 19 in quello orientale e 8 nel territorio italiano (Alpi Marittime, Sardegna, Alpi Apuane, Gargano, Campania, Appennino Meridionale, Calabria e Sicilia). Secondo Ozenda (1994) le zone di rifugio in Italia erano costituite dalla punta del Salento, la Sardegna, la Sicilia e la fascia costiera tirrenica dal Lazio alla Calabria. Nello stesso periodo la larghezza del Canale di Sicilia si ridusse a circa 40-50 Km rispetto agli attuali 145 Km e probabilmente questo fatto favori la dispersione a lunga distanza di piante provenienti dal continente africano.
Secondo Tomaselli & Gualmini (2000) durante l'era glaciale, attraverso il raccordo fisco tra l'Appennino settentrionale e le Alpi Occidentali, esistevano relazioni fitogeografche che permisero le migrazioni foristiche di taxa orofili ovest-europei, alpino-occidentali e al-pino-appenninici da Nord-Ovest a Sud-Est nei periodi freddi e in direzione opposta in quelli caldi. Altri studi (Negri, 1928; Corti, 1956) hanno dimostrato che in più fasi del Quaternario varie entità atlantico-occidentali, attraversando i valichi a bassa quota delle Alpi Marittime e dell'Appennino settentrionale raggiunsero il Piemonte e poi proseguirono verso altre regioni. A questa categoria potrebbe appartenere Teucrium scorodonia.
All'epoca la linea di costa tra le penisole italiana e balcanica si trovava qualche centinaio di chilometri più a sud di quella attuale e poteva congiungere le
città di Ancona e Zara. Nel territorio più a sud, varie isole dalmate erano inglobate alla terraferma, le opposte sponde circumadriatiche erano più vicine ed esistevano territori emersi. Si presume che la maggiore vicinanza delle sponde e i ponti terrestri che si erano instaurati, favorirono i movimenti migratori che portarono in Italia specie appennino-balcaniche e generalmente orientali. Una specie che usufruï di tali connessioni fu Salvia officinalis. Ad avviso di Radosavljevic et al. (2015), la regione costiera dell'Adriatico orientale, oltre che centro d'origine del taxon, durante il Wurm fu anche un'area di rifugio da cui ripartirono i ripopolamenti dei territori vicini. A loro avviso anche l'Appennino meridionale in cui le popolazioni di Salvia officinalis sono caratterizzate un numero notevole di alleli, poteva co-stituire un'area di rifugio. Probabilmente le popolazioni di Salvia officinalis e di altre specie tra cui Hyssopus officinalis subsp. aristatus, Marrubium incanum, Stachys recta subsp. subcrenata, S. recta subsp. grandiflora e Thymus praecox subsp. polytrichus raggiunsero la penisola italiana seguendo più rotte migratorie: la via carsica nord-adriatica e un ponte terrestre più a sud.
Le seguenti entità appennino-balcaniche presenti solo nelle regioni centro-meridionali, invece, potrebbero esse-re migrate in direzione occidentale percorrendo un'unica rotta migratoria: Lamium bifidum subsp. balcanicum, L. garganicum s.l., Micromeria graeca s.l., Stachys thirkei, S. tymphaea, Thymus striatus s.l. e T. zygiformis.
Durante qualche fase calda del Pleistocene o nell'O-locene, attraverso il collegamento tra il Carso triestino e la penisola balcanica raggiunsero il Friuli Venezia Giulia: Ballota nigra subsp. velutina, Clinopodium aci-nos subsp. villosum, C. einseleanum, C. thymifolium, Micromeria juliana, Salvia napifolia, Satureja montana. subsp. variegata, S. subspicata subsp. liburnica e Thymus illyricus.
Ai periodi interglaciali freddi del Pleistocene è da at-tribuire la migrazione nella penisola della componente microtermica nordica ed eurasiatica della flora italiana cui appartengono le seguenti lamiacee: Clinopodium vulgare, Galeopsis bifida, Glechoma hederacea, Lycopus exaltatus, Mentha arvensis, Prunella vulgaris, Scutellaria galericulata, Stachys palustris e S. sylvatica. Durante gli interglaciali caldi, invece, raggiunsero la penisola entità tipiche degli ambienti steppici.
Le migrazioni oloceniche
L'Olocene inizio circa 11700 anni fa e fu caratte-rizzato da un vistoso aumento della temperatura e del livello marino, l'arretramento delle linee costiere e dei ghiacciai alpini, l'espansione dei relitti terziari sopravvissuti in stazioni di rifugi, la diffusiome di entità di diverse origini geografiche e la formazione di nuovi taxa. In questo periodo l'uomo inizio la domesticazione di piante e animali, svolgendo un importante ruolo nella trasformazione del paesaggio.
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Dopo l'era glaciale, due distinte ondate migratorie interessarono le regioni dell'Italia settentrionale. La prima che si sviluppo in più fasi seguendo una direttrice est-ovest attraverso un corridoio padano o il margine inferiore delle Alpi, porto diverse piante pontiche, me-diterraneo-orientali ed est-europee sino alle regioni oc-cidentali della penisola. È probabile che alcune specie proseguissero i movimenti migratori anche in direzione sud. La seconda ondata che era stata preceduta da altre simili nel Pleistocene, attraverso i bassi valichi delle Alpi Marittime e dell'Appennino permise l'ingresso nelle regioni peninsulari di elementi atlantici, mediterraneo-o-cidentali e ovest-europei. Nello stesso periodo dai rifugi dell'Italia meridionale partirono ondate migratorie in direzione settentrionale. Circa 10000 anni fa, secondo Pignatti (2018) Dracocephalum austriacum raggiunse le Alpi. Ad avviso di Poldini (1989) dopo il Wurm, il Carso litoraneo fu ripopolato da entità illiriche provenienti dall'immediato retroterra balcanico.
La diffusione diretta o indiretta delle piante nell'O-locene fu favorita anche dall'uomo che in diverse regioni peninsulari era presente circa 50000 anni fa. In generale l'uomo con l'attività agricola, il pascolo, gli incendi, la costruzione d'infrastrutture di trasporto e di edifici da un lato provoca la rarefazione di piante autoctone e dall'altro favorisce l'introduzione di piante estranee che si adattano facilmente agli ambienti artifi-ciali ricavati dai disboscamenti effettuati. Molte piante potrebbero essere state diffuse anche con il commercio marittimo, tra cui Satureja thymbra che ad avviso di Pignatti (2018) potrebbe essere stata introdotta in Italia dai Fenici. Nel Bacino del Mediterraneo in cui le lamiacee hanno il più importante centro di diversità, si sono sviluppate antiche civiltà e gli uomini per millenni hanno modificato gli habitat, influenzando la distribuzione delle piante, i loro modelli evolutivi, flussi genici, processi differenziazione e la dispersione dei semi (Thompson, 2005). Secondo Pignatti (1994), l'impatto umano sulla flora ha provocato un aumento del grado di ploidia in diverse specie e variazioni mor-fologiche, tra cui quelle osservate nel genere Acinos (ora inserito in Clinopodium).
Molte lamiacee coltivate da oltre 5000 anni si sono spontaneizzate, conquistando nuovi territori. Esistono papiri egizi del 2800 a.C. che indicano gli usi medicamentosi di erbe come il basilico, la lavanda, la
maggiorana, la menta e la salvia che all'epoca potevano essere coltivate e si diffusero a causa dell'uomo.
Si puo presumere che le seguenti lamiacee coltivate da almeno 2000 anni, si siano spontaneizzate: Ballota pseudodictamnus, Leonurus cardiaca, Stachys rosmarinus e specie appartenenti ai generi Lavandula, Melissa, Mentha, Ocimum, Origanum, Salvia, Satureja e Thymus. In periodi piu recenti, in alcuni casi negli ultimi 2-3 secoli, la flora italiana si e arricchita di altri taxa coltivati e naturalizzati appartenenti ai generi: Caryopteris, Clerodendrum, Dracocephalum, Elsholtzia, Lamium, Lavandula, Leonurus, Lycopus, Nepeta, Perilla, Physostegia, Plectranthus, Salvia, Scutellaria, Stachys e Teucrium.
Modalita di dispersione
Durante la loro evoluzione le lamiacee hanno adot-tato accorgimenti anatomico-strutturali che facilitano la dispersione e il trasporto. Alcuni taxa hanno semi che per le loro ridotte misure o per particolari caratteristiche anatomiche, possono essere facilmente trasportati dalle correnti aeree. Altri sono diffusi dagli animali con due diversi modi: 1) hanno semi carnosi che sono mangiati e poi dispersi con gli escrementi; 2) sono costituiti da superfici vischiose, meccanismi di aggancio con setole e uncini o sono inclusi in parti spinose che facilitano l'adesione al corpo (Bouman & Meeuse1992).
I semi di alcune specie dei generi Ajuga, Lamium, Stachys e Teucrium, dopo il distacco dalla pianta, in un primo tempo possono essere trasportati dal vento a brevi distanze e poi sono dispersi dalle formiche.
Alcuni taxa della tribu Menthae hanno adottato i seguenti accorgimenti morfologici che facilitano la dispersione a lunga distanza: ali, peli apicali e squame sui semi, calici gonfiati e altri accorgimenti anatomici (tumbleweed che prevede il trasporto dell'intera pianta) per la dispersione con il vento, spine per la dispersione epizocora, "sacche" di flottazione e la myxospermia, osservabile anche nella maggior parte delle Nepetoideae, che consiste nella secrezione di sostanze mucillaginose da parte semi o frutti per facilitare l'attaccamento al corpo degli animali e il trasporto con le correnti idriche. In generale, la diffusione biogeografica della tribu Mentheae avvenne sfruttando i ponti terrstri mentre sono piu rari attraverso le barriere terrestri o idriche (Drew & Systma, 2012).
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USTNATICE (LAMIACEAE) V ITALIJANSKI FLORI: REGIONALNA RAZŠIRJENOST IN
FITOGEOGRAFSKI POMISLEKI
Amelio PEZZETTA
Via Monteperalba 34 - 34149 Trieste e-mail: fonterossi@libero.it
POVZETEK
Družina ustnatic (Lamiaceae) je pomembna in dobro raziskana v italijanski flori. V pričujočem delu avtor poroča o seznamu vseh vrst v Italiji, analizira njihivo regionalno geografsko razširjenost, prepoznava glavne vzorce razširjenosti, predstavlja rezultate fitogeografske analize in poskuša razpravljati o izvoru in selitvenih premikih na temelju bibliografskih podatkov. Na italijanskem ozemlju se pojavlja 272 infrageneričnih taksonov. Regionalna razširjenost je bolj ali manj nesklenjena: samo 15 taksonov je prisotnih v vseh regijah (upoštevaje v nekaterih primerih tudi Sicilijo in Sardinijo); drugi so razširjeni v eni ali nekaj regijah, tudi v obliki disjunkcij. Prevladujejo sredozemske vrste, sledijo jim endemiti. Na podlagi pregledane literature je razvidno, da še vedno obstajajo nejasnosti in razlike glede interpretacije izvora družine, rodov in vrst ter selitvenih premikov pri naseljevanju italijanskih regij.
Ključne besede: Lamiaceae, popis vrst, regionalna razširjenost, biogeografija, izvor
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SITOGRAFIA
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received: 2019-04-03	DOI 10.19233/ASHN.2019.12
OCCURRENCE OF GIANT TUN, TONNA GALEA (LINNAEUS, 1758) (GASTROPODA: TONNIDAE) IN THE MARINE WATERS OFF SLOVENIA
(NORTHERN ADRIATIC SEA)
Manja ROGELJA
Aquarium Piran, Academic, Electronics and Maritime High School, Bolniska ulica 11, 6330 Piran, Slovenia
Lovrenc LIPEJ
Marine Biology Station, National Institute of Biology Piran, Fornace 41, SI-6330 Piran, Slovenia
e-mail: lovrenc.lipej@nib.si
ABSTRACT
On 1st December 2018 a fisherman caught a specimen of the giant tun Tonna galea (Linnaeus, 1758) in the bottom trammel net for flounders, approximately 1 Nm outside the town of Izola. The net was placed on a muddy bottom at 20 m of depth. This is the second record of T. galea in the Slovenian waters (Gulf of Trieste, northern Adriatic Sea). Another specimen (the first one) was previously reported in October 2015 in the waters off Piran. By including T. galea in the checklist of Slovenian marine malacofauna, at least 370 gastropod species were up to date recorded in the Slovenian part of the Adriatic Sea.
Key words: Giant tun, Tonna galea, marine malacofauna, Gulf of Trieste, northern Adriatic Sea
PRESENZA DI DOGLIO, TONNA GALEA (LINNAEUS, 1758) (GASTROPODA: TONNIDAE), IN ACQUE MARINE AL LARGO DELLA SLOVENIA (ADRIATICO
SETTENTRIONALE)
SINTESI
Il 1° dicembre 2018 un esemplare del gigantesco doglio Tonna galea (Linnaeus, 1758) e stato catturato con una rete da posta, il tramaglio, a circa 1 Nm dalla cittadina di Izola. La rete e stata posizionata su fondo fangoso a 20 m di profonditá. Questo e il secondo ritrovamento di T. galea nelle acque slovene (Golfo di Trieste, Adriatico settentrionale). Un altro esemplare (il primo) e stato segnalato a ottobre 2015 nelle acque di Pirano. Includendo T. galea nella lista della malacofauna marina slovena, almeno 370 specie di gasteropodi sono state registrate nella parte slovena dell'Adriatico.
Parole chiave: Doglio, Tonna galea, malacofauna marina, Golfo di Trieste, Adriatico settentrionale
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INTRODUCTION
Tonna galea (Linnaeus, 1758) is a large gastropod, widespread in the Atlantic and Pacific Oceans and in the Mediterranean Sea (de Simone, 1995). It is the second largest Mediterranean gastropod, which could reach more than 29 cm in size (Katsanevakis et al., 2008). It mainly inhabits sandy and muddy sediments and sea-grass meadows (Katsanevakis et al., 2008). It is a carnivore which preys on sea cucumbers such as Holothuria tubulosa, H. forskali, H. poli and H. sanctori (Toscano et al., 1992; Francour, 1997), other echinoderms and mol-lusks. The basic life history of this species deserved only scarce scientific interest and many aspects of its biology and ecology still remains unknown (Doxa et al., 2011). Nowadays, this giant gastropod is endangered mostly by artisanal fishermen and collectors (Tunesi et al., 2006). It is a rare and protected species according to Annex II of the Bern convention (Council of Europe, 1979) and the Protocol of the Barcelona convention (Annex II) (European Community, 1999; UL RS, 2002). However, it is still sporadically collected in many Greek areas by divers (Katsanevakis et al., 2008) as a food delicacy or for shell collectors (Tunesi et al., 2006; Russo & Perini, 2016). The aim of this paper is to present data on the occurrence of this giant gastropod in the Slovenian part of the Adriatic Sea.
MATERIAL AND METHODS
Two individual giant tuns were found in recent years in the Slovenian part of the Adriatic Sea. The first was recorded on 24th October 2015 close (200 m distance northward) to the diffuser of the pipeline of the sewage outfall near Piran and the second on 1st December 2018 one Nm outside the town of Izola (45° 33' 20.9'' N; 013°
Fig. 1: Specimen of Tonna galea, caught in the waters off Izola (Slovenia), kept in the Piran Aquarium (Photo: M. Rogelja).
Sl. 1: Primerek velikega sodca, ujetega v vodah okoli Izole (Slovenija) v piranskem akvariju (Foto: M. Rogelja).
38' 19.6'' E). Both individuals were caught accidentally as by-catch in the bottom trammel net. In the first case the giant tun was kept in the Aquarium Piran still alive and then moved to the Shell museum Piran where it is now part of the exhibited collection. A note on this record was mentioned in the Piran municipal bulletin by Simič (2015).
In the second case, the specimen was caught in a trammel net for flounders, placed on muddy bottom at 20 m of depth overnight. The specimen was deposited still alive in the Piran Aquarium into a 3.400 l aquarium tank with sandy bottom (Fig. 1). The giant tun was photographed and the shell measured with a calliper to the nearest millimetre (Fig. 2). The specimen is housed in the collection of the Aquarium Piran.
RESULTS AND DISCUSSION
The species was easily recognized through external morphological characters such as shell, which is spiral in shape and globose, resembling a barrel. The colour is pale brown and homogenous. Shell aperture is large with its outside border damaged. The surface of the shell is covered with wide spiral ribs (Cossignani & Ardovini, 2011). Head and the muscular foot are rather large and beige coloured with irregular dark brown spots. The shell measured 155 mm and the oral aperture is 145 mm wide. The giant tun collected in 2015 measured 190 mm.
Published data on the occurrence of Tonna galea are very scarce in the Adriatic Sea. Stefano Chiereghin considered this species as very rare in the northern Adriatic already two centuries ago (Chiereghin, 2001). According to Coen (1933, 1937; in: Russo & Perini, 2016) T. galea, a species which used to be rather common, seems to face the threat of extinction.
More recently the giant tun was recorded in Montenegro (Petovic et al., 2017), in Croatia (e.g. Zavodnik et al., 2006) and in Italy (Cossignani et al., 1992). Even more rare is considered in its northern part. In fact, the majority of available faunistic surveys on mollusks or invertebrates did not mention this species for areas of northern Adriatic Sea (e.g. Zavodnik & Kovačic, 2000; Zavodnik et al., 2005; Kučic, 2016). In the eastern northern Adriatic, there are only few published records on this species. A specimen of T. galea, collected in August 1965 in waters off the island of Lošinj, is housed in the collection of the Natural History Museum of Rijeka (Croatia) (http://www.prirodoslovni.com/inventarna/). Another one was mentioned by Zavodnik et al. (2006) for the island of Pag. Other available data are known from local newspapers or social media. Those are dealing on cases of illegal hunting of giant tuns in the waters off Novigrad (Klobučar Opačak, 2013) and of finding of a specimen, stranded on a beach in Rovinj (Orlovic Radic, 2016) which was after released back into the sea. In their comprehensive survey of mollusks in the Gulf
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of Trieste, Vio & De Min (1996) mentioned an empty shell caught by a fisherman in waters off Savudrija (Istria peninsula), but without any precise data. In the western part of the north Adriatic Sea T. galea was recently found in waters of Caorle (Venezia), when a juvenile specimen was caught by fishermen in a depth range from 25 to 30 m (Russo & Perini, 2016). Unfortunately, authors did not provide any information about the date of capture.
According to De Min & Vio (1996), at least 232 species of gastropods were recorded in the waters of Slovenia. However, authors focused their research mostly on shelled gastropods, so many seaslugs were not mentioned in their text. In a recently published monography on marine opisthobranchs in Slovenia, Lipej et al. (2018) reported 141 species. By analysing both checklists and by including T. galea in the list, at least 370 gastropod species were up to date recorded in the Slovenian part of the Adriatic Sea.
ACKNOWLEDGMENTS
Authors wish to express their gratitude to the fisherman Daniel Hrvat for the alert and the donation of the giant tun to the Aquarium Piran and to Jan Simic (Shell museum Piran) for sharing the morphological data of the first specimen.
Fig. 2: Shell of the studied specimen of Tonna galea, caught in the waters off Slovenia (Photo: M. Rogelja). Sl. 2: Lupina ujetega primerka velikega sodca, ujetega v vodah okoli Izole (Slovenija) v piranskem akvariju (Foto: M. Rogelja).
POJAVLJANJE VELIKEGA SODCA, TONNA GALEA (LINNAEUS, 1758) (GASTROPODA: TONNIDAE) V MORSKIH VODAH SLOVENIJE (SEVERNI JADRAN)
Manja ROGELJA
Akvarij Piran, Gimnazija, elektro in pomorska šola Piran, Bolniška ulica 11, 6330 Piran, Slovenija
Lovrenc LIPEJ
Morska Biološka Postaja, Nacionalni Inštitut za Biologijo, Piran, Fornače 41, SI-6330 Piran, Slovenija
e-mail: lovrenc.lipej@nib.si
POVZETEK
Prvega decembra je lokalni ribič približno 1 Nm pred Izolo v ribiško mrežo ujel primerek velikega sodca (Tonna galea). Mreža je bila postavljena v globini 20 m nad muljastim dnom. To je drugi zabeležen primer pojavljanja velikega sodca v slovenskih vodah (Tržaški zaliv, severni Jadran). Pred tem je bil en primerek te vrste (prvi zapis o pojavljanju) ujet v vodah blizu Pirana oktobra 2015. Upoštevaje nov podatek je seznam morskih polžev v slovenskem delu Jadranskega morja bogatejši še za eno vrsto in zdaj šteje najmanj 370 vrst.
Ključne besede: veliki sodec, morska malakofavna, drugi zapis o pojavljanju, Tržaški zaliv, Jadransko morje
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Russo, P. & L. Perini (2016): Ritrovamento di un esemplare vivente di Tonna galea (Linnaeus, 1758) (Gastropoda: Tonnidae) in Alto Adriatico. Alleryana, 34(1), 16-17.
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Zavodnik, D., A. Pallaoro, A. Jaklin, M. Kovačic & M. Arko-Pijevac (2005): Benthos Survey of the Senj Archipelago (North Adriatic Sea, Croatia). Acta Adriat., 46(Suppl. 2), 3-68.
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received: 2019-01-24	DOI 10.19233/ASHN.2019.13
SPATIAL DISTRIBUTION OF THREE SPECIES OF PALAEMON SHRIMP (CRUSTACEA: DECAPODA: CARIDEA) IN BADAŠEVICA RIVER
(SW SLOVENIA)
Jure JUGOVIC & Živa MUHIČ
Department of Biodiversity, Faculty of Mathematics, Natural Sciences and Information Technologies, University of Primorska,
Glagoljaška 8, 6000 Koper, Slovenia e-mail: jure.jugovic@upr.si
ABSTRACT
We investigated the presence, spatial distribution and possible co-existence of Palaemon species from Badaševica river and its draining channels. We used inverted bottles with a bait to trap the shrimp and recorded three species ("P. elegans, P. adspersus, P. antennarius) from six out of seven surveyed localities. The localities mostly differed in distance from the coastline (0-3.6 km) and salinity (3.9-36.2), while high variation was recorded in other hydrologi-cal, physio-chemical and biochemical parameters among the localities and species. P. elegans was present only at the river mouth at salinity of 33.2, while P. antennarius was predominantly found at localities in a distance more than 2 kilometres inland. P. adspersus was most common and prevailed at localities with denser vegetation. Although P. adspersus and P. elegans were both found at a single locality, their microhabitat clearly differed (P. elegans was recorded exclusively at the river mouth, P. adspersus ca. 50 metres inland). A single specimen of P. antennarius was trapped together with P. adspersus but in general their spatial and ecological segregation was well expressed. Presence of ovigerous females in brackish environment was confirmed for P. adspersus and P. antennarius. Males outnumbered females in all three species.
Key words: brackish environment, spatial segregation, co-occurrence, Palaemonidae, salinity
DISTRIBUZIONE SPAZIALE DI TRE SPECIE DI GAMBERI DEL GENERE PALAEMON (CRUSTACEA: DECAPODA: CARIDEA) NEL FIUME CORNALUNGA (SLOVENIA SUD-OCCIDENTALE)
SINTESI
Gli autori hanno studiato la presenza, la distribuzione spaziale e la possibile coesistenza di specie del genere Palaemon nel fiume Cornalunga e nei suoi canali di drenaggio. Con l'uso di bottiglie rovesce con un'esca, hanno intrappolato tre specie di gamberetti ("P. elegans, P. adspersus, P. antennarius) in sei delle sette localitá campionate. Le localitá sono posizionate a distanze differenti dalla costa (0-3,6 km), con diverse salinitá (3,9-36,2) e ampie differenze pure negli altri parametri idrologici, fisico-chimici e biochimici tra localitá e specie. P. elegans e presente solo alla foce del fiume (salinitá pari a 33.2), mentre P. antennarius e presente prevalentemente in localitá a una distanza maggiore ai 2 km verso l'entroterra. P. adspersus e piu comune, trovato prevalentemente in localitá con vegetazione piu densa. Sebbene P. adspersus e P. elegans sono stati trovati in una sola localitá, il loro microhabitat differisce chiaramente (P. elegans presente esclusivamente alla foce del fiume, metre P. adspersus a circa 50 metri di distanza verso l'entroterra). Un singolo esemplare di P. antennarius e stato trovato intrappolato insieme a P. adspersus, ma in generale la loro segregazione spaziale ed ecologica e ben espressa. La presenza di femmine ovigere in ambiente salmastro é stata confermata per P. adspersus e P. antennarius. Per tutte le specie i maschi campionati superavano in numero le femmine.
Parole chiave: ambiente salmastro, segregazione spaziale, co-occorrenza, Palaemonidae, salinitá
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INTRODUCTION
Palaemonidae are diagnosed by the size of their second chelipeds that are always larger (in some species slightly and in other extremely) than the first chelipeds (Bauer, 2004; De Grave et al., 2008; Christodoulou et al., 2016). The genus Palaemon consists of 87 species (De Grave & Ashelby, 2013; Carvalho et al., 2014; Tzomos & Koukouras, 2015), however there are only two genera and 14 species in the Palearctic region (De Grave et al., 2008; Tzomos & Koukouras, 2015). In Slovenia, five species of Palaemonidae shrimps are reported (Manning & Stevcic, 1982; Christodoulou et al., 2016), although this family is one of the most speciose within the Caridea (de Grave et al., 2008; Christodoulou et al., 2016) following the Atyidae (43 genera) with 14 genera in total (Christodoulou et al., 2016).
Among them, three species were known to penetrate rivers and channels, but only Palaemon anntenarius H. Milne Edwards, 1837 is treated as a predominantly freshwater species inhabiting lakes and rivers. Nevertheless, it can sometimes be found also in coastal brackish waters such as lagoons and estuaries in the Mediterranean basin (Holthuis, 1961; d'Udekem d'Acoz, 1999; Falciai & Palmerini, 2002; Gottstein-Matocec & Kerovec, 2002). This species is on the list of protected species in Slovenia (Decree on protected wild animal species: Anonymous, 2004). Palaemon adspersus Rathke, 1837 and Palaemon elegans Rathke, 1837 are predominantly marine species but can be found in anchialine waters, and they can sometimes co-occur (Manning & Stevcic, 1982). In Slovenia, they were found together in few localities in the areas of tidal flats, where another Palaemon species, P. xiphias (Risso, 1816) can also occur (Manning
& Stevcic, 1982). Palaemon serratus (Pennant, 1777), a fifth palaemonid species from Slovenia, is frequently reported from the coastal marine environments (Turk & Richter, 2007).
In total, there are only three small rivers with direct outflow into the Adriatic Sea in Slovenia: Dragonja at the border with Croatia in the south, Rizana outflowing into the port of Koper in the north, and Badasevica that is flowing through the artificial channel throughout its lower flow, while in its upper part it flows through agricultural landscape. Spring of Badasevica that was our focal river is at 196 m above sea level and reach the Bay of Koper after 9.5 kilometres with a gradient of only 2.07 %. In its lower part, gradient is even lower, only 0.14 % during the last 2.2 kilometres before the outflow. Owing to its torrential nature, floods were frequent in its lower part, therefore the river channel was highly changed and redirected; the river banks were walled or covered with stone blocks and many draining channels were constructed since 1950s (Plut, 1979). Badasevica had its old channel outflowing in the San Canziano bay, however an artificial new main and some side (draining) channels were constructed south of it and the river has now its main outflow in the Bay of Koper (Plut, 1979). All three main rivers of the Slovenian part of Adriatic basin potentially contribute to the pollution of the gulf of Trieste (Turk, 2016). At their estuaries, freshwater and marine systems are interacting, and anchialinae water is present. According to salinity, habitat categories can be divided in freshwater (i.e. limnetic: 0-0.5) and saline (oligohaline: 0.5-5; mesohaline: 5-15; polyhaline: 18-30; mixohaline: 30-40) environments (Jones & Hallin, 2010).
In the present study we provide the information on spatial distribution of three species of Palaemon within
Fig. 1: Geographical position of Badaševica river (arrow) in Slovenia (a) and sampling localities with proportions of sampled Palaemon species (b) (map adjusted and redrawn from Google Earth).
Sl. 1: Geografski položaj reke Badaševice (puščica) v Sloveniji (a) in vzorčna mesta s prikazanimi razmerji ujetih vrst iz rodu Palaemon (b) (prirejeno po Google Earth).
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Tab. 1: Sampling localities (S) with hydrological, biological, physio-chemical and biochemical parameters (min-max value) in Badaševica river. Tab. 1: Vzorčna mesta (S) z razponom hidroloških, bioloških, fizikalno-kemijskih in biokemijskih parametrov v reki Badaševici.
NJ
s	Ceographic coordinates	Distance of traps from the sea [m]	Channel type	Substrate	Vegetation	Tidal influence	T [°C]	Oxygen [mg/L]	Oxygen [%]	pH	Conductivity [mS/ cm]	Salinity	Nitrates [mg/L]	Chi a [|Jg/L]
1	45°32'32.8"N 1 3°43 '11.4"E	0-80	new artificial channel	silt, mud, rocks, walled	exposed, some different algae	strong	11.1-25.9	7.08-11.75	86.3-116.8	8.05-8.09	16.1-50.2	13.2-33.2	42.3-1 95.5	0.40-8.10
2	45°32'25.5"N 1 3°43 '1 4.9"E	250-300	new artificial channel	silt, mud, rocks, walled	some filamentous algae	strong	11.2-25.7	7.16-12.19	87.0-124.0	8.05-8.14	13.1-50.5	10.5-32.6	35.4-196.5	0.61-25.33
3	45°32'09.4"N 1 3°43 '45.8"E	1130-1150	new artificial channel	rocks (artificial), walled (incl. bottom)	some filamentous algae	medium	12.1-25.6	7.09-12.46	86.0-127.4	8.06-8.33	4.16-50.4	3.0-36.2	14.2-193.0	1.90-33.66
4	45°32 '23.1 "N 1 3°43 '45.3"E	780-820	draining channel	silt, mud	some phylamentous algae, Phragmites	low	11.4-25.7	9.31-11.34	102.1-130.6	7.62-8.06	16.46^2.0	6.3-12.7	40.3-130.5	1.41-33.91
5	45°32'1 6.2"N 1 3 °44' 1 2.1" E	2110-2160 (B*) 3520-3570 (SC*)	old channel	silt, mud	dense filamentous algae	low	13.5-27.1	7.81-15.34	85.3-145.8	8.15-8.20	25.20^7.4	9.5-13.7	59.1-1 73.5	3.14-34.61
6	45°32'28.7"N 1 3°44'20.3"E	2500-2550 (B) 3050-3100 (SC)	old channel	silt, mud	filamentous and other algae	low	1 7.8-28.9	15.34-21.72	1 75.4-227.2	8.33-8.70	27.1-45.6	15.7-33.9	68.6-151.0	4.41-16.78
7	45°31 '48.0"N 1 3°44'40.0"E	2550-2610	old channel	silt, mud, concrete, small rocks, walled	algae in periphyton	none	10.0-28.4	6.16-11.80	78.5-125.3	7.80-8.30	0.63-38.4	3.9-22.7	0.94-138.5	3.66-41.71
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a single river system (Badasevica in SW Slovenia) and discuss possible environmental factors influencing their spatial distribution.
MATERIAL AND METHODS
Specimens were collected with trapping at seven localities (Fig. 1) of Badasevica river and its draining channels from the outflow (locality 1) to artificial barrier 2.6 km inland (locality 7) (Fig. 1, Tab. 1). Locality 7 was situated below a two metres high artificial dam, hence no traps were set upstream from the dam. Three plastic bottles (volume 1.5 l) with inverted opening were used per locality and the distance from the sea of each trap was measured (Tab. 1). Crushed mussels (Mytillus gal-loprovincialis) and chicken meat were used as bait and trapping lasted for four days during four sampling sessions in spring 2017. Samples were collected once per month in middle March, April, May and June. Sampling localities were georeferenced using a GPS and phys-icochemical water quality parameters (dissolved oxygen (mg*L-1), oxygen saturation (%), water temperature (°C), conductivity (mS*cm-1), and pH) were measured using a Portable multiparameter Aquaprobe AP-200 with a GPS Aquameter (Aquaread AP 2000). At each locality, sediment type and tidal influence (strong, medium, low, none) were assessed by naked eye (Tab. 1). Samples of water were transferred into the laboratory and chlorophyll a (jg*L-1) was measured shortly afterwards. Salinity was calculated from water temperature and conductivity. Distance from the sea was measured from orto-photo maps for each sampling locality as a range of distances between the three traps.
Specimens were identified using the Olympus SZX7 stereomicroscope with a built-in camera. The identification key of Gonzalez-Ortegon & Cuesta (2006) was used for species identification. Presence of ovigerous females and male-female ratio were checked. Nomenclature follows De Grave & Ashelby (2013).
RESULTS
Main observations and measurements on the hy-drological and physio-chemical parameters at seven sampling localities are compiled in Tab. 1. Altogether, three species were sampled during the study from localities 1-6, while no animals were recorded at locality 7 (Fig. 1, Tab. 2). Most animals were collected in April and May with 52.6 % and 31.6 % of the total sample size, respectively, while in March and June only 7.9 % of the total sample size in each of those months was collected. Palaemon adspersus was most commonly sampled (69.7 % of sampled animals) and was found at four localities (1-4; see Tab. 2).
At locality 4, where only P. adspersus was recorded, animals counted for 50.0 % of the total sample size. The ranges of chemical parameters measured at each sam-
pling day and locality overlap among the three species, however, oxygen levels (concentration and saturation) were bit higher at locality 6 (and sometimes at locality 5) than at the other localities. Moreover, the distance from the sea and salinity greatly differ among the localities (Tab. 1). With time (i.e. consecutive sampling periods), P. adspersus was recorded progressively further from the coastline (Tab. 2). While it was recorded from localities 1, 2 and 4 (50-820 metres from the coastline) in March, it was found at localities 2, 3 and 4 (250-1150 metres inland) in April, and only at localities 3 and 4 (780-1150 metres inland) during May and June. P. elegans (5.3 % of total sample) was found only in one (outermost) of the three traps at the river mouth (locality 1) where salinity at the sampling day was 33.2, which is almost as high as salinity reported for the northern Adriatic Sea (ap-prox. 38-39, e.g. Grbec et al., 2007). P. adspersus was recorded together with P. elegans at locality 1, however it was found there in another trap that was set 50 m from the river mouth, at salinity of 13.2. In total, P. adspersus was found 50-1150 m inland, at salinity range 3.2-36.2. P. antennarius (25.0 % of total sample size) was found at longest distance from the sea, i. e. at two localities (5, 6) that are situated more than 2 kilometres from the coastline, with salinity range 19.0-30.9. Nevertheless, a single specimen of P. antennarius was found also at locality 2 (ca. 300 metres from the coastline) together with P. adspersus at salinity 10.5. As in P. adspersus, recordings of P. antennarius progressed further inland with time (Tab. 2). While the species was recorded at locality 2 in March, it was later recorded only from localities 5 (April, May; ca. 2.1 kilometres from the coastline) and 6 (June; ca. 2.5 kilometres from the coastline).
During April and May, presence of ovigerous females was confirmed for P. adspersus (2 and 5 females at localities 2 and 4, respectively) and P. antennarius (4 females at locality 5) but not for P. elegans. Males outnumbered females in all three species (100 % of males in P. elegans, 75.0 % in P. antennarius and 78.4 % in P. adspersus).
DISCUSSION
We report on a presence and spatial segregation of three Palaemon species (P adspersus, P. elegans, P. antennarius) in Badasevica river and channels nearby. Nevertheless, P. adspersus and P. elegans are frequently reported from the same environments (Berglund & Bengtsson 1981; tapinska & Szaniawska 2006; Janas 2013). In estuaries with a low tidal influence both can inhabit meadows of Zostera marina, however, Berglund (1980; 1982) reports that in a latter case P. adspersus is more abundant, possibly due to larger body size in comparison to P. elegans. Moreover, a spatial co-occurence of three species of Palaemon, P. antennarius, P. adspersus and P. varians with an ecological niche separation within Phragmites australis was reported by Dolmen et al. (2004). In this case, P. adspersus and P. elegans occurred
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Tab. 2: A list of species per each sampling locality (S), sampling date (month, in roman numerals) and number of sampled shrimps together with physio-chemical and biochemical parameters measured at each successful sampling. Tab. 2:. Seznam vrst po vzorčnih mestih (S) s podatki o datumu vzorčenja (mesec, označeno z rimskimi številkami) in številu zbranih kozic ter vrednostmi fizikalno-kemijskih in biokemijskih parametrov ob vsakem uspešnem vzorčenju.
S	Species	Month	No.	T ra	Oxygen [mg/L]	Oxygen [%]	PH	Conductivity [mS/cm]	Salinity	no3 [mg/L]	Chlorophyll a [pg/L]
1	P. adspersus	III	1	11.1	10.44	94	8.09	16.08	13.2	42.3	8.10
	P. elegans	V	4	20.5	9.17	101.3	8.08	45.7	33.2	144.5	3.67
2	P. adspersus	III	1	11.2	10.23	92.1	8.14	13.1	10.5	35.4	25.33
		IV	2	16.2	12.19	124	8.13	35.9	27.8	104.5	4.42
	P. antennarius	III	1	11.2	10.23	92.1	8.14	13.1	10.5	35.4	25.33
3	P. adspersus	IV	4	16.4	12.46	127.4	8.33	4.97	3.2	26.1	18.92
		V	5	20.4	10.50	111.2	8.13	49.8	36.2	123.5	1.90
		VI	1	25.6	7.09	86.0	8.06	50.4	32.6	193.0	2.88
4	P. adspersus	III	3	11.4	11.34	102.9	8.06	16.5	13.4	40.3	18.03
		IV	26	16.8	9.91	102.1	7.95	27.3	20.3	77.1	33.91
		V	8	24.4	9.31	110.6	7.99	42.0	27.3	96.7	1.41
		VI	1	25.7	10.76	130.6	7.62	34.2	21.1	131.5	5.88
5	P. antennarius	IV	8	19.6	7.82	85.3	8.17	42.5	30.9	120.5	34.61
		V	7	25.9	8.68	106.0	8.15	31.2	19.0	79.2	3.14
6	P. antennarius	VI	4	28.9	15.72	202.2	8.33	39.8	23.3	151.0	15.11
in a microhabitat with lower and P. varians with higher density of P. australis (Dolmen et al., 2004). On the other hand, where a tidal influence is strong, P. adspersus and P. elegans in most cases select different microhabitats (Dolmen et al., 2004). In our case, selection of different microhabitats of the two species would be in line with observations of a strong tidal influence at our localities; whereas P. elegans was found only at the final point of the riverine mouth, P. adspersus occupied brackish part of the river up to approx. one kilometre from the coastline. Both species usually prefer well aerated systems with salinity higher than 15 (mostly polyhaline and mixohaline environments) (Barnes, 1994; Dolmen et al., 2004).
Despite that there are records of occurrence of P. elegans below 6.5 of salinity from the Baltic sea (mesohaline to oligohaline waters; Dolmen et al., 2004; tapinska & Szaniawska, 2006), both species are euryha-line, however in Badaševica only P. adspersus was found in a wide range of salinity (oligohaline to mixohaline). During our study, P. elegans was found only in mixohaline water. Berglund & Bengtsson (1981) reported that P. elegans is more prone to hypoxy than P. adspersus. In our case, oxygen levels were similar for a locality with P. elegans and for localities with P. adspersus. Therefore, we cannot see the oxygen as a factor influencing spatial segregation of the two species in our case. Both species are mainly nocturnal (Berglund 1980; Hagerman &
Ostrup, 1980; Guerao & Abello, 1996; Janas & Baran-ska, 2008), however pronounced nocturnal activity is usually less stressed in P. adspersus (Berglund, 1980; Hagerman & Ostrup, 1980). Since P. elegans is not a habitat specialist, more prone to hypoxia, more active and quicker in feeding than P. adspersus, it can occupy sites that are not preferential for stronger and larger P adspersus (Berglund & Bengtsson, 1981). Especially when found in marine environments, P. adspersus prefers meadows of marine flowering plants (e.g. Posidonia, Zostera, Cymodocea) (Manent & Abella-Gutierrez, 2006), while P. elegans can be abundant also at sandy and unprotected bottom (Berglund & Bengtsson, 1981). This could be in line with our case as the environment at the site with P. elegans was open and unprotected. Moreover, we recorded P. adspersus only at localities where dense vegetation was present. It should be noted that P. adspersus was by far most abundant at the end of a draining channel at locality 4 (73.1 % of a P. adspersus sample) with densest vegetation. Since it has been reported that P. adspersus rather avoid open spaces since it can be quickly detected by the predators owing to its large size, this locality seemingly offers this species an optimal habitat and reproduction site, and is probably lacking shrimp predators. Moreover, at the localities closest to the coastline (1, 2), shrimps were found only at the beginning of the sampling period (at locality 1, a
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single specimen in March, and at locality 2, a single and two specimens in March and April, respectively). No additional animals were found there during the continuation of the sampling period (May, June), and a species reached a peak of abundance in April at locality 4 (50.0 % of a P. adspersus sample).
P. anntenarius represented 25.0 % of the total sample size and was found in two localities where neither of the above mentioned species occurred. P. antennarius is reported to be oligohaline species that inhabits freshwater to brackish environments with muddy bottom. Most commonly it is mentioned as a true freshwater species (Dalla Via, 1987; Gottstein-Matočec et al., 2006; Ana-stasiadou et al., 2009, 2014; Christodoulou et al., 2016). During our study it was found in mesohaline and poly-haline waters and always above 15 of salinity, however, this is not contradicting its euryhaline nature as Dalla Via (1987) reports that it can be found at a wide range of salinity from 5 to 30. This species can adapt to quick salinity changes by metabolic adjustment if the changes in salinity are short-termed, while at higher salinities (>19) oxygen uptake strongly increases. Populations that inhabit brackish environments with higher salinity can adapt up to approximately 25 of salinity but in the same time brackish populations cannot easily adapt to low salinities (Dalla Via, 1987). This is in line with our results as this species was found at the range of salinity above 10.5 (but even higher than reported in literature, up to 30.9) and most abundant at the two localities (5, 6) with highest oxygen levels. Gottstein-Matočec et al., 2006 reported that P. antennarius shows higher reproductive success in environments with stable salinity, however during the reproductive period brackish waters were preferred (Dalla Via, 1987; Gottstein-Matočec et al., 2006) over waters with lower salinity in delta of Neretva (SE Croatia). Sheltered bays with stable environment (low tidal influence, stable salinity, warm temperature, abundance of food) and muddy bottom can therefore be optimal for the reproduction of the species, such as probably at localities 5 and 6 in our case where it was recorded after the beginning of its breeding season in April. Nevertheless, a single specimen of P. antennarius was found before the breeding season in March also at locality 2 in the main channel of the Badaševica river, in this case together with P. adspersus. We failed to find the data on a sympatric occurrence of those two species in the literature, so we think this co-occurence was coincidetial. However, we cannot exclude the option that P. antennarius can occasionally be present in the main channel of the river, possibly due to drift or active spreading of the species.
Sex ratio in our samples strongly deviates towards males and this contradicts the reports for all three species where females are usually more abundant (Gottstein-Matočec et al., 2006; tapinska & Szaniawska, 2006;
Manent & Abelle-Gutierrez, 2006). P. adspersus for which a reproductive period lasts from March to August (Guerao & Ribera, 1995; Manent & Abella-Gutierrez, 2006) females were frequently noticed to lay eggs in shallow coastal marine waters (Barnes, 1994; Guerao & Ribera, 1999; Glamuzina et al., 2014). Nevertheless, we noticed some ovigerous females in the river channel itself (28.6 % of all ovigerous females at locality 2), however, it is possible that some of them move towards the sea for egg laying which could cause their deficit upstream. Since most of ovigerous P. adspersus females (71.4 %) were found at locality 4 it is also possible that ovigerous females seek for protected and well-hidden places where they remain for the most of time. Hence, their trapping probability could be lower than for males and estimated sex ratio is then biased towards males. In P. antennarius, reproductive period lasts from April until August with a maximum in June (Gottstein-Matocec et al., 2006). This is in line with our data for Slovenian mesohaline and poly-haline environments, while no conclusions can be made on unusual sex ratio in P. antennarius (but see above for P. adspersus) and P. elegans. For the latter, a small sample size may prevent a more accurate conclusion.
CONCLUSIONS
In this study we reported on a well expressed spatial and ecological segregation among three species of Pal-aemon in a brackish environment of a river Badasevica. The following conclusions can be made:
1.	P. elegans and P. adspersus select different habitats near the river outflow that is under a strong tidal influence (P elegans occupies more exposed rocky bottom at higher salinity at the final point of the outflow, and P. adspersus is present at a microsite with lower salinity in a better protected river channel only few tens of meters inland);
2.	P. antennarius and P. adspersus seem to be ecologically and spatially well separated as the vast majority of P. adspersus was found in a drainage channel and upper the river channel with dense vegetation (mostly macrophytes), and P. antennarius was found predominantly at sites more than 2 kilometres inland with low tidal influence in a well aerated water;
3.	Presence of ovigerous females was confirmed for P. adspersus and P. antennarius.
ACKNOWLEDGEMENTS
Authors thank Felicita Urzi for help in a laboratory, Martina Jeklar for help on the field and Domen Trkov for useful information on distribution of Palaemon shrimps in the area of Koper. Authors also thank two anonymous referees for constructive comments on the manuscript.
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PROSTORSKA RAZPOREDITEV TREH VRST KOZIC IZ RODU PALAEMON (CRUSTACEA: DECAPODA: CARIDEA) V BADAŠEVICI (JZ SLOVENIJA)
Jure JUGOVIC & Živa MUHIČ
Department of Biodiversity, Faculty of Mathematics, Natural Sciences and Information Technologies, University of Primorska,
Glagoljaška 8, 6000 Koper, Slovenia e-mail: jure.jugovic@upr.si
POVZETEK
Preiskovali smo prisotnost, prostorsko razporeditev in možnost sobivanja vrst iz rodu Palaemon v reki Badaševici in njenih odvodnih kanalih. Za pasti smo uporabili plastenke z navznoter obrnjenim ustjem. Zabeležili smo tri vrste ("P. elegans, P. adspersus, P. antennarius) s šestih od sedem preiskovanih vzorčnih mest. Vzorčna mesta so se najbolj razlikovala po oddaljenosti od morja (0-3.6 km) in slanosti (3.9-36.2), pri ostalih beleženih hidroloških, fizikalno--kemijskih in biokemisjkih parametrih pa smo zabeležili veliko stopnjo variabilnosti tako med vzorčnimi mesti kot vrstami kozic. P. elegans smo zabeležili le na ustju reke pri slanosti 33.2, P. antennarius pa smo skoraj izključno našli le na vzorčnih mestih, ki so od morja oddaljena več kot 2 km. P. adspersus je bila najštevilnejše zastopana vrsta in se je pojavljala v velikem številu predvsem na lokacijah z gosto vegetacijo. Čeprav smo P. adspersus in P. elegans našli na istem vzorčnem mestu ob izlivu reke v morje, smo opazili, da se izbira njunega mikrohabitata razlikuje (P. elegans smo našli neposredno na izlivu reke v morje, P. adspersus pa smo zabeležili prb. 50 m po toku navzgor). P. antennarius smo le enkrat (en osebek) našli na eni od vzorčnih mest skupaj s P. adspersus, a je bila sicer prostorska in ekološka ločitev med vrstami jasno vidna. Prisotnost ovigerih samic smo potrdili za vrsti P. adspersus in P. antennarius. Samci so bili pri vseh treh vrstah številnejši od samic.
Ključne besede: somorno okolje, prostorska ločitev, sobivanje, Palaemonidae, slanost
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received: 2019-03-22	DOI 10.19233/ASHN.2019.14
ABIOTIC PARAMETERS IN TUNIS SOUTHERN LAGOON AFTER AN ENVIRONMENTAL RESTORATION AND STATUS OF MACROBENTHIC BIOCENOSIS (NORTHERN TUNISIA, CENTRAL MEDITERRANEAN SEA)
Khadija OUNIFI BEN AMOR & Mohamed Mourad BEN AMOR
Laboratoire de Biodiversité, Biotechnologie et Changements Climatiques, Faculté des Sciences de Tunis, Université Tunis El Manar, Tunis Tunisie. Institut National des Sciences et Technologies de la Mer, port de pêche, 2025 La Goulette, Tunisia
Jamila BEN SOUISSI
Institut National Agronomique de Tunisie, 43 Avenue Charles Nicolle, cité Mahrajène 1082, Tunis Tunisie.
e-mail: ounifikhadija@yahoo.com
ABSTRACT
Tunis Southern Lagoon was previously polluted by anthropogenic activities which needed a thorough environmental restoration, achieved during September 2001. The aim of the work is to reveal the positive changes of the abiotic parameters and their role on the biodiversity of the lagoon. Ecological measures carried out during a 24-months period (from October 2014 to September 2016) at 3 fixed stations, showed an improvement in water quality, confirming the positive impact of the restoration project. An overview of the macrobenthic biocenosis evolution is also discussed in the present work.
Key words: Eutrophication, restoration, improvement, water quality, biodiversity
PARAMETRI ABIOTICI NELLA LAGUNA MERIDIONALE DI TUNISI DOPO IL RESTAURO AMBIENTALE E STATO DELLA BIOCENOSI MACROBENTONICA (TUNISIA SETTENTRIONALE, MEDITERRANEO CENTRALE)
SINTESI
In passato la Laguna méridionale di Tunisi è stata contaminata da varie attività antropogeniche e pertanto neces-sitava di un accurato restauro ambientale, effettuato nel settembre 2001. L'articolo vuole evidenziare i cambiamenti positivi dei parametri abiotici e il loro ruolo sulla biodiversità della laguna. Le misure ecologiche effettuate nel corso di un periodo di 24 mesi (da ottobre 2014 a settembre 2016) in 3 stazioni fisse, hanno mostrato un miglioramento della qualità dell'acqua, confermando l'impatto positivo del progetto di restauro. Nel presente lavoro viene anche presentata una revisione dell'evoluzione della biocenosi macrobentonica.
Parole chiave: eutrofizzazione, restauro, miglioramento, qualità dell'acqua, biodiversità
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INTRODUCTION
In the last decades, Tunis Southern Lagoon was polluted by local anthropic activities which induced dystrophic crises together with destruction of benthic communities (Ben Souissi, 2002; Chakroun, 2004), due to the fact that this lagoon poorly communicated with the sea. Water renewal was low, and a hyper-eutrophication and contamination by toxic heavy metals occurred in this brackish restricted area. An environmental rehabilitation of the lagoon was decided by Tunisian authorities to limit eutrophication and contamination by toxic industrial discharges. The project also aims to improve biodiversity and gradually restore fishery activities in the lagoon (Ben Souissi et al. 2015). The project of restoration was conducted between April 1998 and July 2001 by the Society for Research and Promotion of Tunis (SEPTS) and the consortium (LAC SUD 2000) (Vandenbroek and Ben Charrada 2001). The environmental restoration focused the enlargement the depth of the canal joining the lagoon to the sea and installing a hydraulic system allowing frequent renewal of the waters of the lagoon and the elimination of areas of water stagnation. The main objective of this study consists to analyze the new ecological status of this
Fig. 1: A. Map of Tunisia pointing out the site of Tunis Southern Lagoon (TSL) located in the north. B. Tunis Northern Lagoon (TNL) separated from Tunis Southern Lagoon by a navigation channel (NC).1-3 sampling stations in TSL.
Sl. 1: A. Zemljevid Tunizije z označeno južno tuniško laguno (TSL) na severu. B. Severna tuniška laguna je od južne omejena s plovnim kanalom (NC). 1-3 Vzorčeval-ne postaje v TSL.
ecosystem based on 2 years of measurements locally carried out. An overview on its macrobenthic flora and the fishing interest fauna is discussed in this paper to point out the impact of ecological restoration on the biological environment.
MATERIAL AND METHODS
The Lagoon of Tunis is separated in two areas by a navigation canal (Fig. 1). Tunis Southern Lagoon extends over an area of 720 ha with an almost regular depth of about 2.4 m. It appears as an ellipse stretching in a SW-NE direction, between 36°46'47''and 36°48'00''N and 10°12'22'' and 10°16'41''E. Its shores have been excavated and protected by large rocky blocks. Three sampling stations are located in the lagoon and indicated by; Station 1 located to the east of the lagoon near the bay of Tunis, station 2 in the middle and station 3 in the west (Fig. 1). To access to these stations, a flat bottom boat suitable for navigation in the lagoon was used, the analyses consist of monthly measurements carried out in situ and in the laboratory during a 24 months from October 2014 to September 2016.
Temperature, salinity, pH, and dissolved oxygen were monthly measured at approximately 10 cm below the surface using a salinometer (WTW.LF 197), a pH meter (WTW. pH 197) and oximeter (WTW.OXI 197) calibrated beforehand. Turbidity was measured using a Secchi disk. In the laboratory, chemical analyzes of total nitrogen and phosphorus were analyzed in the laboratory by means of a photometric method which uses, as reagents, kits tests previously prepared by the supplier of the equipment. The basic tool of the photometric method is a photometer Photolab S12 type WTW equipped with a thermoreactor CR3000 type WTW. The chlorophyll-a was determined using the spectrophotometric method of Lorenzen (1967) and following Parsons et al. (1984), the analysis of the latter must be initiated rapidly (within 3 hours after sampling). The main results of two years of measurements are presented below. Data on macrobenthic fauna and flora were based on a compilation of published articles, thesis, surveys and our own observations in the last decade.
RESULTS
Temperature - The total average of 2 years of measurements is 20. 3 °C, the minima recorded vary between 9.8 and 11.8 °C and the maxima between 26.6 and 28 °C (Fig. 2). Temperatures recorded in station 1, near the Gulf of Tunis, show a slightly higher thermal gradient (1°C) compared to the other stations. This gradient is explained by the discharges of electric central near the water inlet to the lagoon, which discharge about 60 m3s-1 of hot water. This difference is more appreciable in winter than in summer.
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—•—ST1 --■- 5T2 —ST3
Months
Fig. 2: Water temperatures in the Tunis southern lagoon (from October 2014 to September 2016) Sl. 2: Temperatura vode v južni tuniški laguni (od oktobra 2014 do septembra 2016).
Salinity - The salinity in the lagoon is homogeneous. The mean value recorded during our study period is 37.5. The lowest exceptional salinities were 31.3 and 34.1 recorded respectively in September 2015 and February 2016 (Fig. 3). These values are recorded as a result of rainfall that caused storm water to enter the lagoon from the banks. The maximum salinity has reached a value of 39 recorded in July 2016 due to high temperatures that enhanced evaporation in the lagoon. With the exception of these values, salinity has varied with an annual gradient that usually does not exceed 1. This is mainly due to the rapid renewal of the lagoon water, which makes the effect of evaporation relatively low.
Fig. 4: Water pH in the Tunis southern lagoon (from October 2014 to September 2016). Sl. 4: pH vode v južni tuniški laguni (od oktobra 2014 do septembra 2016).
Transparency - The average transparency of the water in the lagoon is about 2.0 m (Fig. 5). The lowest transparency values are recorded in station 1, which is largely influenced by the water in coming from the Gulf of Tunis. From station 2, the visibility conditions change and the influence of the gulf decreases considerably, the transparency is therefore better. The western part of the lagoon (ST3) represents the most transparent zone because it is less influenced by the gulf; moreover, it is constantly invaded by caulerpes, having roots sunk in the sediment, with a tendency to fix the materials on the bottom.
Monihs
Fig. 3: Water salinity in the Tunis southern lagoon (from October 2014 to September 2016). Sl. 3: Slanost v južni tuniški laguni (od oktobra 2014 do septembra 2016).
pH - The mean pH recorded in the southern lagoon over the period from October 2014 to September 2016 is 8.3, the maximum value is 9 while the minimum is 7.85 (Fig. 4). The relatively low values recorded in summer 2015 are mainly due to the exceptional warmth occurred during this period, which accelerate the fermentation and mortality of macroalgae inducing a relatively low pH. During the period of algal growth, the release of CO2 tends to increase this parameter.
Fig. 5: Monthly fluctuations of Transparency (m) in the Tunis southern lagoon (from October 2014 to September 2016).
Sl. 5: Mesečna nihanja prozornosti (m) v južni tuniški laguni (od oktobra 2014 do septembra 2016).
Dissolved Oxygen - The dissolved oxygen contents range from 70 to 130%. The average of the two years of measurements in the lagoon is 90% (Fig. 6). The maximum values observed are due to the production of oxygen by photosynthesis of macroalgae and the minimum values observed are probably due to the mineralization of organic matter resulting from the mass mortality of nitrophilic algae.
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-1-5T1 -«-5T2 —*—STB
Fig. 8: Monthly fluctuations of total phosphorus (fag/l) in the Tunis southern lagoon (from October 2014 to September 2016).
Sl. 8: Mesečna nihanja koncentracij celokupnega fosforja (fag/l) v južni tuniški laguni (od oktobra 2014 do septembra 2016).
Fig. 6: Monthly fluctuations of dissolved Oxygen (%) in the Tunis southern lagoon (from October 2014 to September 2016).
Sl. 6: Mesečna nihanja koncentracij raztopljenega kisika (%) v južni tuniški laguni (od oktobra 2014 do septembra 2016).
Total Nitrogen - The average total nitrogen concentration over the two years is 674 pg/l. An extreme value of 1378 pg/l was recorded in November 2015 (Fig. 7). This rate coincided with the massive mortality of mac-roalgae in this month since the organic form of nitrogen constitutes about 89% of total nitrogen.
Total phosphorus - The total phosphorus content range from 9 to 93 |jg/l with an average of 32.7 |jg/l (Fig. 8). The peaks are due either to the mortality of the macroalgae or to the action of the floods and rains that preceded the periods of these peaks and which brought large quantities of phosphate nutrients into the lagoon.
Chlorophyll-a - The Chlorophyll-a allow us to assess the degree of eutrophication of the water, in the Tunis southern lagoon, chlorophyll-a concentration varies from 0.28 to 14.88 jg/l (Fig. 9). The average of the two years relatively low at 2.5 jg/l.
Fig. 9: Monthly fluctuations of Chlorophyll a (fag/l) in the Tunis southern lagoon (from October 2014 to September 2016).
Sl. 9: Mesečna nihanja koncentracij klorofila a (fag/l) v južni tuniški laguni (od oktobra 2014 do septembra 2016).
DISCUSSION
Prior the lagoon's ecological rehabilitation, the average monthly salinity ranged between 31 and 48.9 (Ben Souissi 2002), between 37 and 38.3, after environmental restoration. This comparison indicated that the euryhalin character of the lagoon is changed into "marinization" sensu Zaouali and Baeten (1983). High levels of dissolved oxygen in water trend towards an eutrophication, and to date since the end of environmental restoration, no dystrophic crisis was observed; the dissolved oxygen levels oscillate around the saturation point (Hermi & Aissa (2002); Chakroun, 2004). Monthly pH averages were saw-tooth fluctuations between 8.11 and 9.49 and may even reach very alkaline pH values as a result of spills of various chemical pollutants (Ben Souissi 2002). This parameter currently has a spatiotemporal stability since the minimum value did not drop below 8 and the maximum value did not exceed 8.4.
Based on the key parameters of eutrophication indicators: total phosphorus and chlorophyll-a, expressed as annual averages, the eutrophication status of the Tunis Southern Lagoon waters can be outlined. The report of
■5T1 - - - ST2 —ST3
Months
Fig. 7: Monthly fluctuations of total nitrogen (fag/l) in the Tunis southern lagoon (from October 2014 to September 2016).
Sl. 7: Mesečna nihanja koncentracij celokupnega dušika (fag/l) v južni tuniški laguni (od oktobra 2014 do septembra 2016).
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these concentrations on the abacus following the model proposed by the OCDE (1982) showed that the waters of the Tunis southern lagoon are mesotrophic with a probability of 54% versus the hypereutrophic state observed before the restoration with a probability of 70% (Jouini et al., 2005).
The restoration of the lagoon displayed a high increase of biodiversity, with occurrence of species of phanerogams and seaweed of marine origin. Among new established vegetation in the lagoon were found the endemic caulerpe Caulerpa prolifera (Forsskal) J.V.Lamouroux, 1809, and the brown algae Cysto-seira barbata (Stackhouse) C.Agardh, 1820 indicator of a healthy ecosystem (Ben Souissi et al., 2015). Prior to restoration, the benthic macroflora was exhibited a very low biodiversity characteristic from eutrophic eu-ryhalin and eurytherm facies dominated by Ulva rigida C.Agardh, 1823, typical of lagoon environments (Ben Souissi, 2002; Shili et al., 2002).
The lagoon azoic during its restoration was progressively invaded by several species, among them were found immigrants from Indo-Pacific origin established since autumn 2001 in the area with the start-up of locks and the restoration of communication with the sea (Gulf of Tunis) and the lagoon itself (Ben Souissi et al., 2003).
The current malacological fauna of the lagoon is comprised 50 species of molluscs, 2 Polyplacophora, 28 gastropods (especially nudibranchs), 17 bivalves and 3 cephalopods versus only 29 species recorded before restoration (Eteres et al. 2011). Of these 50 species, 5 are allochthonous having an Indo-Pacific origin. The best instance is Fulvia fragilis (Forsskal & Niebuhr, 1775), which colonized and invaded the entire lagoon, with presence of juveniles and specimens up to 60 mm in width (Rifi et al., 2011; 2013).
Therefore, new activities have been developed such as the collection of mussel on artificial rocky banks of the lagoon and fishery of cephalopod species such as common cuttlefish Sepia officinalis Linnaeus, 1758 and musky octopus Eledone moschata (Lamarck, 1758).
A diversity of carcinological fauna was displayed in the lagoon comprising 44 crustacean species (19 decapods, 11 isopods, 10 amphipods, 3 barnacles and a single stomatopod) were recorded versus 29 before the ecological rehabilitation of the lagoon. Of these 44 species, 31 are autochthonous and 13 allochthonous (Ounifi Ben Amor et al. 2017). The presence of some species seems not to be transient since several of them were well established in the area (Ounifi Ben Amor et al., 2015; 2016a; 2016b).
The ichthyofauna is also much diversified and concomitantly allowed the resumption of fishing activities in area. Eight species of elasmobranch and more than 70 teleost species are recorded in the lagoon (Mejri et al., 2004; Ben Souissi et al., 2005). A survey carried out in 2014 among fishermen operating regularly in the lagoon shows that the local ichthyofauna included more than 90 species (Ben Souissi et al. 2015).
The physicochemical and trophic analyzes carried out before and after the restoration of Tunis southern lagoon, display a high water quality, stability and an improvement in edaphic environment of the lagoon. This homogenization observed after the ecological restoration is the consequence of an important exchange between the lagoon and the Gulf of Tunis. Such exchange and the absence of water stagnation in some areas have led to a marked disappearance of nitrophilous algae versus the reappearance of marine species. The successful settlement of these latter in Tunis southern lagoon revealed the evident improvement of the lagoon waters.
ABIOTSKI PARAMETRI V TUNIŠKI JUŽNI LAGUNI PO OKOLJSKI OBNOVI IN STATUS MAKROBENTOŠKIH BIOCENOZ (SEVERNA TUNIZIJA, OSREDNJE SREDOZEMSKO MORJE)
Khadija OUNIFI BEN AMOR & Mohamed Mourad BEN AMOR
Laboratoire de Biodiversité, Biotechnologie et Changements Climatiques, Faculté des Sciences de Tunis, Université Tunis El Manar, Tunis Tunisie. Institut National des Sciences et Technologies de la Mer, port de pêche, 2025 La Goulette, Tunisia
Jamila BEN SOUISSI
Institut National Agronomique de Tunisie, 43 Avenue Charles Nicolle, cité Mahrajène 1082, Tunis Tunisie.
e-mail: ounifikhadija@yahoo.com
POVZETEK
Južna tuniška laguna se je soočala z onesnaženjem zaradi antropogenih dejavnosti, zato je prišlo septembra 2001 do okoljske obnove. Namen tega prispevka je obelodaniti pozitivne spremembe v abiotskih dejavnikih in njihovo vlogo glede biodiverzitete v laguni. Ekološke meritve, ki so potekale v 24-mesečnem obdobju (od oktobra 2014 do septembra 2016) na 3 stalnih postajah, so pokazale izboljšanje kvalitete vode in s tem potrdile pozitivni učinek projekta obnove. Avtorji v delu razpravljajo tudi o makrobentoških biocenozah.
Ključne besede: evtrofikacija, obnova, izboljšanje, kvaliteta vode, biodiverziteta
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REFERENCES
Ben Souissi, J. (2002): Impact de la pollution sur les communautés macrobenthiques du lac sud de Tunis avant sa restauration environnementale. Thèse de Doctorat. Biologie. Faculté des Sciences de Tunis, 267 pp.
Ben Souissi, J., M. Rezig & J. Zaouali (2003): Appearance of invasive species in the southern lake of Tunis. p. 911-922. In: Proceedings of the Sixth International Conference on the Mediterranean Coastal Environment. MEDCOST 03, 7-11 October, 2003. Ravenna, Italy.
Ben Souissi, J., H. Méjri, J. Zaouali, A. El Abed, M. Ben Salem, O. Guélorget & C. Capapé (2005): Teleost species recorded in Tunis Southern Lagoon after environmental restoration (Northern Tunisia, Central Mediterranean. Annales, Ser. Hist. Nat., 15(2), 157-164.
Ben Souissi, J., M. Rifi, R. Ben Charrada & J. Zaouali (2015): La lagune de Tunis: Un exemple de dépollution réussie ? In: Daumali X. and Centemeri L. (Eds). Pollution industrielle en Méditerranée. Maison Méditerranéenne des Sciences de l'Homme (France), 353-367.
Chakroun, R. (2004): Réponse de la macrofaune invertébrée benthique à l'état de dégradation du milieu: Cas du "lac" sud de Tunis et de la lagune de Ghar El-Melh. Thèse Doctorat. Biologie. Faculte des Sciences de Bizerte, 341 pp.
Eters, E., K. Ounifi Ben Amor, M. Ben Salem & J. Ben Souissi, (2011): Faune malacologique actuelle de la lagune sud de Tunis (Tunisie Septentrionale), In 2ème Congrès franco-maghrébin de zoologie et 4èmes Journées franco-tunisiennes de Zoologie, Zarzis, nov. 2010, Paris, Société Zoologique de France. Bull. Soc. Zool. Fr, p. 136.
Hermi, M & P. Aissa, (2002): Impact de l'anthropisation du lac sud de Tunis (Tunisie) sur la structure automnale des peuplements de Nématodes libres. Bull Inst Nat Sc Tec Mer Sal, 29, 77-85.
Jouini, Z., R. Ben Charrada & M. Moussa (2005): Caractéristiques du Lac Sud de Tunis après sa restauration. Mar. Life, 15(1-2), 3-11.
Lorenzen, CJ. (1967): Determination of chlorophyll and pheopigments by spectrophotometric equations. Limnology and Oceanography 12, 343-346.
Méjri, H., J. Ben Souissi, J. Zaouali, A. El Abed, Y. Vergne, O. Guélorget & C. Capapé (2004): On the recent occurrence of elasmobranch species in Tunis Southern lagoon (Northern Tunisia, Central Mediterranean) Annales, Ser. Hist. Nat., 15(2), 143-155.
OCDE (OECD) (1982): Eutrophisation des eaux. Méthodes de surveillance, d'évaluation et de lutte, Organisation de Coopération et de Développement Economiques, Paris, 164 pp.
Ounifi Ben Amor, K., M. Rifi & J. Ben Souissi (2015): Description, reproductive biology and ecology of the Sphaeroma walkeri (Crustacea: Isopoda) alien species from the Tunis southern Lagoon (Northern Tunisia: Central Mediterranean). Annales, Ser. Hist. Nat., 25(1), 35-44.
Ounifi Ben Amor, K., M.M. Ben Amor & J. Ben Souissi (2016a): Annotated list of crustacean species recorded in the Tunis Southern Lagoon (Northern Tunisia, Central Mediterranean). Annales, Ser. Hist. Nat., 26 (1), 55-70.
Ounifi Ben Amor, K., M. Rifi, R. Ghanem, I. Draeif, J. Zaouali & J. Ben Souissi (2016b): Update of alien fauna and new records from Tunisian marine waters. Medit. Mar. Sci., 17(1), 124-143.
Ounifi Ben Amor, K., M.M. Ben Amor, M. Rifi & J. Ben Souissi (2017): Diversity of crustacean species from Tunis Southern Lagoon (Central Mediterranean) after an ecological restoration. Cah. Biol. Mar., 58(1), 49-57.
Parsons, TR & CM. Maita Lalli (1984): A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, 173 pp.
Rifi, M., J. Ben Souissi & J. Zaouali (2013): Statut écologique du bivalve invasif Fulvia fragilis (Forsskâl in Niehbur, 1775) dans les eaux tunisiennes. Deuxième Conférence internationale Biodiversité et sécurité alimentaire. Hammamet, 26-28 Avril, p. 65.
Rifi, M., G. Le Pennec, M. Ben Salem & J. Ben Souissi (2011): Reproductive strategy of the invasive cockle Fulvia fragilis in the Bay of Tunis (Tunisia). J. Mar. Biol. Assoc. UK, 91(7), 1465-1475.
Shili, A., E.B. Trabelsi & N.B. Maïz (2002): Seasonal dynamics of macro-algae in the South Lake of Tunis. J. Coast. Conserv., 8(2), 127-134.
Vandenbroeck, J & R. Ben Charrada (2001): Restoration and development project of south Lake of Tunis and its shores. Terra Aqua, 85, 1-20.
Zaouali, J & S. Baeten (1983): Impact de l'eutrophisation dans la lagune de Tunis (Partie Nord). 2c partie: analyse de correspondance. Rapp. Comm. Inter. Mer Médit., 28(6), 327-332.
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PROTECTING ADRIATIC BIODIVERSITY IN KOTOR: THE CONGRESS ADRIBIOPRO 2019
An international conference on the protection of the biodiversity of the Adriatic Sea was held from 7th to 10th April 2019 in the town of Kotor, a small coastal pearl listed as a UNESCO World Heritage Site. The conference was organized by the Institute of Marine Biology of the University of Montenegro. It was the final event of the project "Marine Biodiversity Conservation Center 'Boka Aquarium' - MonteAqua", aiming to gather all relevant national and regional stakeholders, as well as to secure closer regional cooperation in the Adriatic region. During the four days filled with various activities, participants from 16 countries delivered 92 presentations covering 9 different topics: marine biodiversity conservation, conservation of coastal and marine areas, preventing marine pollution, rare and endangered species in the Adriatic Sea, invasive and alien marine species, roles of aquaria, sustainable use of marine resources, marine biotechnology, and freshwater biodiversity conservation.
The event opened with an exhibition by the talented underwater photographers Ivana Orlovic Kranjc and Janez Kranjc titled "Hidden Beauty of the Sea". The photographs portraying the rich and colourful underwater world of the Adriatic Sea were a lovely introduction into two days of interesting presentations and panel discussions.
In her introductory speech, Professor Durdica Perovic, Vice Rector of the University of Montenegro, stated that the results of the conference would be used in shaping future marine science priorities and policies in Montenegro and other Adriatic countries. With the main focus of the conference being biodiversity and its protection, a lot of emphasis was put on some current issues that pester the global oceans, such as unsustainable use of resources, marine pollution and non-indigenous species, as well as certain local problems characteristic of the Adriatic Sea. On a more operational note, the participants pointed out some deficits, such as the lack of experts in taxonomy, especially in the younger generation, as well as the growing need for cooperation among Adriatic countries.
Many excellent contributions were presented, abstracts of which can be viewed at the website of the 'Aquarium Boka' Marine Biodiversity Conservation Center	(http://www.aquariumboka.ucg.ac.me/
wp-content/uploads/201 9/04/AdriBioPro2019-BookAbstracts-20190408.pdf). Among eminent researchers, Academician Professor Dr. Gordan
Fig. 1: Panel discussion with esteemed marine biologists on the topic: Why Adriatic biodiversity matters (photo: Institute of marine biology Kotor).
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Fig. 2: The participants of the first AdriBioPro conference (photo: Institute of marine biology Kotor).
Karaman, an expert in amphipod taxonomy, presented his lifelong study of these crustaceans, which yielded descriptions of several new species from the Bay of Kotor. A special focus was put on the issue of mass mortality of the Mediterranean endemic bivalve Pinna nobilis caused by a protozoan parasite. An international group of researchers presented their experience and lessons learned from this occurrence and the measures taken so far to counteract it. The word of the conference had reached as far as Lebanon; in fact, the marine scientists from this country presented an interesting study of the Lebanese population of the endangered, yet still heavily exploited common guitarfish.
Many interesting speeches were given, priorities and policies were discussed, but like in many similar occasions, even more valuable connections and collaborations were probably made during the array
of social activities. The conference dinner held on the Wednesday evening was one of them. We had a unique opportunity to see a glimpse of rich Montenegrin cultural heritage through the performance of local folklore dancers, while enjoying Montenegrin food and wine. In my opinion, the conference was a success and more such occasions would be appreciated in the Adriatic region in the future.
Ana Fortič
Morska biološka postaja Piran, Nacionalni inštitut za biologijo
MORSKA BIOLOŠKA POSTAJA PIRAN C^f^ MARINE BIOLOGY STATION PIRAN	Moi9
144
IN MEMORIAM
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IN MEMORIAM, 147-148
IN MEMORIAM OF FABIO PERCO (1946-2019)
In the middle of February 2019, more than 300 people paid their last respects to Dr Fabio Perco at the cemetery of Santa Anna in Trieste. Fabio was an esteemed biologist, an outstanding ornithologist and a very warm person, who left a profound mark on the creation, protection, management and popularisation of many Italian natural sites of immense importance, such as the northern Adriatic lagoons, the coastal limestone cliffs and Trieste's karstic environment. He was actively involved in the creation of the Skocjan Inlet Nature Reserve on the Slovenian coast. In short, I can surely say he dedicated his entire life to nature conservation.
Carcharhinus limbatus (drawing Fabio Perco).
Fabio was a truly gifted artist, who was certainly bestowed his artistic talent at birth, for his father Dino was an excellent illustrator, as were Fabio's brothers and daughters. Fabio was a master wildlife painter, able to produce exquisite illustrations of birds and other animals. The birds in his paintings are realistic and authen-
tic, always depicted in their natural habitats, but with a fairy tale touch. Some of his masterpieces of lagoon avifauna are on display at the centre of the Škocjanski Zatok Nature Reserve in Koper. His magnificent art was undoubtedly inspired by his love for nature, especially the animal kingdom.
He planned and brought to realisation many nature conservation projects. His efforts were crucial in the creation of several coastal protected areas, such as the Regional Nature Reserve "Isola della Cona". This popular ornithological and naturalist site has won numerous awards at national and international levels. Fabio was also a promotor for the establishment of a centre for white storks at the Oasis of Quadris near Fagagna del Friuli and in charge of the establishment of a lakeside feeding station for vultures at Cornino near Udine. Unfortunately, he did not manage to bring to life another brilliant project of his, whose goal was to reintroduce the white-tailed eagle (Haliaetus albicilla) into the province of Friuli Venezia Giulia.
Fabio was also a gifted writer, publishing articles on a variety of topics dealing with ornithology, nature conservation and protected areas, especially the wetlands. He was a dedicated man who gathered his inspiration from his family, so it is not surprising that he published many books in co-authorship with his close relatives. He dedicated a lot of his time to researching birds of prey and owls. In fact, Fabio studied natural sciences at the University of Trieste, obtaining his Master of Science title with a thesis on the goshawk (Accipiter gentilis) in the Trieste Karst. My favourite book by Fabio is a monograph about owls and birds of prey entitled I rapaci, conoscerli e proteggerli (WWF Italia, 1976), which he co-wrote with his father Dino and his brother Franco, also a skilled illustrator and writer. He also produced a book on the fauna of the impressive limestone cliffs of Duino together with his daughter Nicoletta (Fauna della Riserva naturale Falesie di Duino, 2011), with illustrations created by his daughter Elena. Among the many
Carcharías taurus and Odontaspis ferox (drawing Fabio Perco).
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vulture (Il grifone in Italia e nel mondo, 1996) co-authored with Fulvio Genero and Bruno Dentesani (1996), deserve special mention.
I regret to have known Fabio for only a few years; still, I can say that our meetings were very fruitful for me. I learned so much from him, heard so many stories and enjoyed every single moment that I spent with him in his karstic realm of Sgonico. The possibility and privilege to exchange opinions with such an erudite and discussing topics of terrestrial and marine biology, nature conservation, history and etymology, is something I will never forget. He was a skilled narrator who could present a topic in a very interesting and detailed manner.
But above all, I will remember Fabio as a genuinely warm person, a good friend with a great sense of humour, and an eternal discoverer of the secrets of nature. We will remain surrounded by his legacy in the wetlands of either side of the Gulf of Trieste...
Lovrenc Lipej
other monographs that Fabio penned, the amazing study dealing with vultures, which he published with Gianni Benassi (Gli avvoltoi, 1985), and the one on the griffon
Fabio Perco (photo: Natasa Salaja).
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NAVODILA AVTORJEM
1.	Revija ANNALES (Anali za istrske in mediteranske študije Series, Historia Naturalis) objavlja izvirne znanstvene in pregledne članke z naravoslovnimi vsebinami, ki obravnavajo posebnosti različnih podpodročij sredozemskega naravoslovja: morska biologija in ekologija, ihtiologija, geologija s paleontologijo, krasoslovje, oljkar-stvo, biodiverziteta Slovenije, varstvo narave, onesnaževanje in varstvo okolja, fizična geografija Istre in Medite-rana idr. Vključujejo pa tudi krajše znanstvene prispevke o zaključenih raziskovanjih., ki se nanašajo na omenjeno področje.
2.	Sprejemamo članke v angleškem, slovenskem in italijanskem jeziku. Avtorji morajo zagotoviti jezikovno neoporečnost besedil, uredništvo pa ima pravico članke dodatno jezikovno lektorirati.
3.	Članki naj obsegajo do 48.000 znakov brez presledkov oz. 2 avtorski poli besedila. Članek je mogoče oddati na e-naslov annales@mbss.org (zaželjeno) ali na elektronskem nosilcu (CD) po pošti na naslov uredništva.
Avtor ob oddaji članka zagotavlja, da članek še ni bil objavljen in se obvezuje, da ga ne bo objavil drugje.
4.	Naslovna stran članka naj vsebuje naslov članka, ime in priimek avtorja (avtorjev), ime in naslov inštitucije, kjer je (so) avtor(ji) zaposlen(i) oz. domači naslov in naslovom elektronske pošte (samo prvi oz. korespondenčni avtor).
5.	Članek mora vsebovati povzetek in izvleček. Izvleček je krajši (cca. 10 vrstic) od povzetka (cca. 30 vrstic).
V izvlečku na kratko opišemo namen, metode dela in rezultate. Izvleček naj ne vsebuje komentarjev in priporočil.
Povzetek vsebuje opis namena in metod dela ter povzame analizo oziroma interpretacijo rezultatov. V povzetku ne sme biti ničesar, česar glavno besedilo ne vsebuje. V povzetku se avtor ne sklicuje na slike, tabele in reference, ki so v članku.
6.	Avtorji naj pod izvleček članka pripišejo ustrezne ključne besede (največ 6). Zaželjeni so tudi angleški (ali slovenski) prevodi izvlečka, povzetka, ključnih besed, podnapisov k slikovnemu in tabelarnemu gradivu. V nasprotnem primeru bo za prevode poskrbelo uredništvo.
7.	Glavni del besedila naj vključuje sledeča poglavja: Uvod, Material in metode, Rezultati, Razprava ali Rezultati in razprava, Zaključki (ali Sklepi), Zahvala (če avtor želi), Literatura. Dele besedila je možno oblikovati v podpoglavja (npr. Pregled dosedanjih objav v Uvodu, Opis območja raziskav v Material in metode). Podpisi k slikam so priloženi posebej za poglavjem Literatura.
8.	Tabele avtor priravi posebej na ločenih straneh v programu Word, tako kot rokopis, jih zaporedno oštevilči in opremi z naslovom - kratkim opisom. V glavnem delu besedila se sklicuje na tabele tako, da jih na ustreznem mestu označi z npr. "(Tab. 1)".
9.	Slikovno gradivo (grafi, zemljevidi, fotografije, table) avtor posreduje v ločenih datotekah (jpeg, tiff) z najmanj 300 dpi resolucije pri želeni velikosti. Največja velikost slikovnega gradiva je 17x20 cm. Vsa potrebna dovoljenja za objavo slikovnega gradiva (v skladu z Zakonom o avtorski in sorodnih pravicah) priskrbi avtor sam in jih predloži uredništvu pred objavo članka. Slike je potrebno tudi podnasloviti in zaporedno oštevilčiti (glej točko 7). V glavnem delu besedila se avtor sklicuje na slike tako, da jih na ustreznem mestu označi z npr. "(Sl. 1)".
10.	Bibliografske opombe, s čimer mislimo na citat
-	torej sklicevanje na druge publikacije, sestavljajo naslednji podatki v oklepaju: avtor in leto izida; npr. (Novak, 2007). Če sta dva avtorja, se izpišeta oba (Novak & Kranjc, 2001), če so trije ali več pa se izpiše samo prvi, ki mu sledi okrajšava et al. (Novak et al., 1999). Več citatov je med seboj ločenih s podpičjem in si sledijo kronološko
-	z naraščajočo letnico izdaje, npr. (Novak et al., 1999; Adamič, 2001; Kranjc & Zupan, 2007). Osebno informacijo (ustno, pisno) izpišemo prav tako v oklepaju z navedbo kratice imena in priimka posredovalca informacije, za vejico pa dodamo "osebno sporočilo", npr. (J. Novak, osebno sporočilo).
11.	Celotni bibliografski podatki so navedeni v poglavju Literatura v abecednem vrstnem redu. Pri tem avtor navede izključno dela, ki jih je v članku citiral. Če ima isti avtor več bibliografskih podatkov, se najprej kronološko izpišejo tisti, kjer je edini avtor, sledijo dela v soavtorstavu še z enim avtorjem in dela v soavtorstvu z več avtorji. Imena revij, v katerih so izšla citirana dela, se izpišejo okrajašano (splošno priznane okrajšave revij). Članki, ki še niso bili publicirani, se lahko citirajo le, če so bili dokončno sprejeti v tisk, pri čemer se na koncu bibliografskega podatka doda beseda "v tisku". Člankov, ki so šele bili poslani v recenzijo, se ne sme citirati.
Primeri navajanje različnih tipov bibliografskih podatkov:
članki v revijah: Klock, J.-H., A. Wieland, R. Seifert & W. Michaelis (2007):
Extracellular polymeric substances (EPS) from cyanobac-terial mats: characterisation and isolation method optimisation. Mar. Biol., 152, 1077-1085.
Knjige in druge neserijske publikacije (poročila, diplomska dela, doktorske disertacije): Wheeler, A. (1969): The fishes of the British Isles and North-West Europe. McMillan, London, 613 p.
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Poglavje v knjigi: McEachran, J. D. & C. Capapé (1984): Myliobatidae. In: Whitehead, P. J. P., M. L. Bauchot, J.-C. Hureau, J. Nielsen & E. Tortonese (eds.): Fishes of the North-eastern Atlantic and the Mediterranean, Vol. 1. Unesco, Paris, pp. 205209.
12. Drugo: latinski izrazi kot npr. in vivo, in situ, e.g., i.e., ter rodovna (Myliobatis sp.) in vrstna (Myliobatis aqui-la) imena se izpišejo v fontu italic. Kadarkoli je možno, se uporabljajo enote iz sistema SI (Système international d'unités).
13. Prvi odtis člankov uredništvo pošlje avtorjem v korekturo. Avtorji so dolžni popravljeno gradivo vrniti v enem tednu. Besedilo popravljamo s korekturnimi znamenji, ki jih najdemo na koncu Slovenskega pravopisa (2001), Ljubljana, ZRC SAZU, 24-25.
Širjenje obsega besedila ob korekturah ni dovoljeno. Druge korekture opravi uredništvo.
14. Za dodatna pojasnila v zvezi z objavo člankov je uredništvo na voljo.
UREDNIŠTVO
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ISTRUZIONI PER GLI AUTORI
1.	La rivista ANNALES (Annali per gli studi istriani e mediterranei, Series Historia Naturalis) pubblica articoli scientifici originali e compendii dai contenuti scientifi-ci relativi ai vari settori della storia naturale e pertinen-ti l'area geografica del Mediterraneo: biologia marina, ecologia, ittiologia, geologia, paleontologia, carsologia, olivicoltura, biodiversità della Slovenia, tutela della natura, inquinamento e tutela dell'ambiente, geografía fisica dell'Istria e del Mediterraneo ecc. La rivista pubblica anche articoli scientifici brevi relativi a ricerche concluse pertinenti a tali settori.
2.	La Redazione accetta articoli in lingua inglese, slo-vena e italiana. Gli autori devono garantire l'ineccepibi-lità linguistica dei testi, la Redazione si riserva il diritto di una revisione linguistica.
3.	Gli articoli devono essere di lunghezza non su-periore alle 48.000 battute senza spazi, ovvero 2 fogli d'autore. Possono venir recapitati all'indirizzo di posta elettronica annales@mbss.org (preferibilmente) oppure su supporto elettronico (CD) per posta ordinaria all'indirizzo della Redazione.
L'autore garantirá l'originalità dell'articolo e si impe-gnerà a non pubblicarlo altrove.
4.	Ogni articolo deve essere corredato da: titolo, nome e cognome dell'autore (autori), denominazione ed indirizzo dell'ente di appartenenza o, in alternativa, l'indirizzo di casa, nonché l'indirizzo di posta elettronica (solo del primo autore o dell'autore di corrispondenza).
5.	I contributi devono essere corredati da un riassunto e da una sintesi. Quest'ultima sarà più breve (cca. 10 ri-ghe) del riassunto (cca 30 righe).
Nella sintesi si descriveranno brevemente lo scopo, i metodi e i risultati delle ricerche. La sintesi non deve contenere commenti e segnalazioni.
Il riassunto riporterà in maniera sintetica lo scopo, i metodi delle ricerche e l'analisi ossia l'interpretazione dei risultati. Il riassunto non deve riferirsi alle tabelle, figure e alla bibliografía contenuta nell'articolo.
6.	Gli autori sono tenuti ad indicare le parole chiave
adeguate (massimo 6). Sono auspicabili anche le tradu-zioni in inglese (o sloveno) della sintesi, del riassunto, delle parole chiave, delle didascalie e delle tabelle. In caso contrario, vi provvederà la Redazione.
7.	Il testo principale deve essere strutturato nei se-guenti capitoli: Introduzione, Materiali e metodi, Risul-tati, Discussione o Risultati e discussione, Conclusioni, Ringraziamenti (se necessari), Bibliografía. Il testo puo
essere strutturato in sottocapitoli (ad es. sottocapitolo Rassegna delle pubblicazioni nell'Introduzione; sottocapitolo Descrizione dell'area di ricerca nel capitolo Materiali e metodi). Le didascalie devono essere presentate separatamente, a seguito del capitolo Bibliografía.
8.	Le tabelle saranno preparate in forma elettronica come il manoscritto (formato Word) e allegate in fogli se-parati alla fine del testo. Gli autori sono pregati di con-trassegnare ogni tabella con un numero e il titolo ossia una breve descrizione. Nel testo la tabella viene richia-mata come segue: (Tab. 1).
9.	Il materiale gráfico (grafici, carte geografiche, fotografíe, tavole) va preparato in formato elettronico (jpeg
0	tiff) e consegnato in file separati, con una definizione di 300 dpi alla grandezza desiderata, purché non ecceda
1	17x20 cm. Prima della pubblicazione, l'autore provve-dera a fornire alla Redazione tutte le autorizzazioni ri-chieste per la riproduzione del materiale grafico (in virtu della Legge sui diritti d'autore). Tutto il materiale grafico deve essere accompagnato da didascalie (vedi punto 7) e numerato.. Nel testo i grafici vengono richiamati come segue: (ad es. Fig. 1).
10.	I riferimenti bibliografici (citazioni) richiamano un'altra pubblicazione (articolo). La nota bibliografica, riportata nel testo, deve contenere i seguenti dati tra parentesi: cognome dell'autore, anno di pubblicazione, ad es. (Novak, 2007). Se gli autori sono due, verranno indicati entrambi (Novak & Kranjc, 2001), nel caso di tre o piu autori verra indicato soltanto il primo, seguito dall'abbreviazione et al. (Novak et al., 1999). Vari riferimenti bibliografici in una stessa nota vanno divisi dal punto e virgola e segnalati in ordine cronologico, ad. es. (Novak et al., 1999; Adamič, 2001; Kranjc & Zupan, 2007). La testimonianza (orale, scritta) verra indi-cata tra parentesi con l'abbreviazione del nome e con il cognome di chi l'ha trasmessa, seguiti dalla virgola e la dicitura "informazione personale", ad es. (J. Novak, informazione personale).
11.	La bibliografía completa va inserita in ordine alfabetico nel capitolo Bibliografía. L'autore indichera esclusivamente i lavori e le edizioni citati nell'articolo. Se si citano piu lavori dello stesso autore, verranno indicati prima in ordine cronologico i lavori in cui l'autore appare solo, poi quelli in cui l'autore compare assieme ad un secondo coautore, seguiti infine da quelli in cui egli compare tra piu coautori. I nomi delle riviste in cui sono pubblicati i lavori citati saranno indicati nella forma abbreviata (abbreviazioni ufficialmente riconosciute). Gli articoli inediti si possono citare soltanto se sono in corso di pubblicazione, facendo loro seguire la dicitura "in corso di pubblicazione". Gli articoli, non ancora recensiti non possono essere citati.
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Esempio di lavoro bibliográfico:
Articoli in riviste: Klock, J.-H., A. Wieland, R. Seifert & W. Michaelis (2007): Extracellular polymeric substances (EPS) from cyanobacterial mats: characterisation and isolation method optimisation. Mar. Biol., 152, 1077-1085.
Libri ed altre pubblicazioni non periodiche (relazioni, tesi di laurea, dissertazioni di dottorato): Wheeler, A. (1969): The fishes of the British Isles and North-West Europe. McMillan, London, 613 p.
Capitoli di libro: McEachran, J. D. & C. Capapé (1984): Myliobatidae. In: Whitehead, P. J. P., M. L. Bauchot, J.-C. Hureau, J. Nielsen & E. Tortonese (eds.): Fishes of the North-eastern Atlantic and the Mediterranean, Vol. 1. Unesco, Paris, pp. 205-209.
12.	Altro: Le espressioni latine come ad es. in vivo, in situ, e.g., i.e., i nomi dei generi famiglie (Myliobatis sp.) e delle specie (Myliobatis aquila) si scrivono con il caratte-re italic. Quando possibile saranno utilizzate le unità del sistema SI (Système international d'unités).
13.	Gli autori ricevono le prime bozze di stampa per la revisione. Le bozze corrette vanno quindi rispedite entro una settimana alla Redazione. In questa fase, i testi cor-retti con segni adeguati (indicazioni in merito si trovano alla fine della pubblicazione "Slovenski pravopis" (2001), Ljubljana, ZRC SAZU, 24-25, non possono essere più am-pliati. La revisione delle bozze è svolta dalla Redazione.
14.	La Redazione rimane a disposizione per eventuali chiarimenti.
LA REDAZIONE
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INSTRUCTIONS TO AUTHORS
1.	The journal ANNALES (Annals for Istrian and Mediterranean Studies, Series Historia Naturalis) publishes original scientific and review articles in the field of natural studies related to the specifics of various subfields of Mediterranean natural studies: marine biology and ecology, ichthyology, geology with paleontology, karst studies, olive growing, biodiversity of Slovenia, nature protection, pollution and environmental protection, physical geography of Istria and the Mediterranean, etc. It also publishes short scientific papers on completed research projects related to the above-mentioned sub-fields.
2.	The articles submitted can be written in the English, Slovene or Italian language. The authors should ensure that their contributions meet acceptable standards of language, while the editorial board has the right to have them language edited.
3.	The articles should be no longer than 48,000 characters (spaces excluded) or 32 typewritten double-spaced pages. They can be submitted via e-mail annales@mbss.org (preferably) or regular mail, with the electronic data carrier (CD) sent to the address of the editorial board.
Submission of the article implies that it reports original unpublished work and that it will not be published elsewhere.
4.	The title page should include the title of the article, the name and surname of the author(s), their affiliation (institutional name and address) or home address, and e-mail address (of the first author or the corresponding author only).
5.	The article should contain the summary and the abstract, with the former (c. 30 lines) being longer than the latter (c. 10 lines).
The abstract contains a brief description of the aim of the article, methods of work and results. It should contain no comments and recommendations.
The summary contains the description of the aim of the article and methods of work and a brief analysis or interpretation of results. It can contain only the information that appears in the text as well. It should contain no reference to figures, table and citations published in the main text.
6.	Beneath the abstract, the author(s) should supply appropriate keywords (max 6) and, if possible, the English (or Slovene) translation of the abstract, summary, keywords, and captions to figures and tables. If unprovided, the translation will be provided by the editorial board.
7. The main text should include the following chapters: Introduction, Material and Methods, Results, Discussion or Results and Discussion, Conclusion, Acknowledgement (not obligatory), References. Individual parts of the text can form a sub-chapter (e.g. Survey of Previous Studies under Introduction; Description of Research Area under Material and Methods). Captions to figures should appear on a separate page beneath References.
8.	Each table should be submitted on a separate page in Word programme (just like the main text). It should be numbered consecutively and supplied with the title -brief description. When referring to the tables in the main text, use the following style: (Tab. 1).
9.	Illustrative matter (diagrams, maps, photographs, plates) should be submitted as separate files (in jpeg or tiff format) and saved at a minimum resolution of 300 dpi per size preferred, with the maximum possible publication size being 17x20 cm. Prior to publication, the author(s) should obtain all necessary authorizations (as stipulated by the Copyright and Related Rights Act) for the publication of the illustrative matter and submit them to the editorial board. All figures should be captioned and numbered consecutively (cf. Item 7). When referring to the figures in the main text, use the following style: (Fig. 1).
10.	Bibliographic notes or citations - i.e. references to other articles or publications - should contain the following data: author and year of publication, e.g. (Novak, 2007). If there are two authors, include both surnames (Novak & Kranjc, 2001); if there are more than two authors, include the surname of the first author followed by a comma and the abbreviation et al. (Novak et al., 1999). If there is more than one reference, separate them by a semicolon and list them in ascending chronological order, e.g. (Novak et al., 1999; Adamic, 2001; Kranjc & Zupan, 2007). When citing information obtained through personal communication (oral, written), provide the initial letter of the name and full surname of the informant followed by a comma and the phrase personal communication, e.g. (J. Novak, personal communication).
11.	The entire list of bibliographic data should be published under References in alphabetical order. The author(s) should list only the works cited in the article. If you are listing several works by the same author with some of them written in co-authorship, first list those written by the author him/herself, then those written in co-authorship with another author, and finally those written in co-authorship with more than one author, with the entries listed in chronological order. The names of journals in which the works cited were published should be abbreviated (cf. list of official journal abbreviations). Unpublished articles can be cited only if they have been
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approved for publication, which should be indicated by adding the phrase in press to the end of the relevant bibliography entry.
Some examples of how to cite different types of bibliographical data:
Articles published in serial publications: Klock, J.-H., A. Wieland, R. Seifert & W. Michaelis (2007): Extracellular polymeric substances (EPS) from cyanobacterial mats: characterisation and isolation method optimisation. Mar. Biol., 152, 1077-1085.
Books and other non-serial publications (reports, diploma theses, doctoral dissertation): Wheeler, A. (1969): The fishes of the British Isles and North-West Europe. McMillan, London, 613 p.
Chapters published in a book: McEachran, J. D. & C. Capape (1984): Myliobatidae. In: Whitehead, P. J. P., M. L. Bauchot, J.-C. Hureau, J. Nielsen & E. Tortonese (eds.): Fishes of the North-eastern Atlantic and the Mediterranean, Vol. 1. Unesco, Paris, pp. 205-209.
12.	Miscellaneous: Latin phrases such as in vivo, in situ, e.g., i.e., and names of genera (Myliobatis sp.) and species (Myliobatis aquila) should be written in italics. Whenever possible, use the SI units (Système international d'unités).
13.	The authors are sent the first page proofs. They should be returned to the editorial board within a week. When reading the proofs, the authors should use the correction signs listed at the end of the book Slovenski pravopis (2001), Ljubljana, ZRC SAZU, 24-25.
It is not allowed to lengthen the text during proofreading. Second proof-reading is done by the editorial board.
14.	For additional information regarding article publication contact the editorial board.
EDITORIAL BOARD
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KAZALO K SLIKAM NA OVITKU
SLIKA NA NASLOVNICI:
Kriptobentoške vrste rib so slabo raziskana skupina manjših rib, ki so vseskozi skrite v skrivališčih. Med njimi so tudi mnoge vrste rib prisesnic. Na fotografiji je veliki prisesnik (Lepadogaster lepadogaster), ki je razmeroma pogosta vrsta bibavičnega pasu. (Foto: D. Trkov)
Sl. 1: Nekateri prisesniki si za domovanje izberejo zelo nenavadna bivališča, kot so mrtve ostrige, ostanki leščurjev ali pa oklepi mrtvih rakovic. To velja za vrsto prisesnika Apletodon incognitus, o kateri je še vedno zelo malo znanega. (Foto: D. Trkov)
Sl. 2: Afriški kostorog (Stephanolepis diaspros) je lesepska selivka, ki se je marsikje v vzhodnem Sredozemskem morju že uveljavila. Vzdolž tunizijske obale poročajo o množičnem pojavljanju. (Foto: L. Lipej) Sl. 3: Morski sodec (Tonna galea) je drugi največji morski polž v Sredozemskem morju. Pred kratkim so to redko in ogroženo vrsto prvič našli tudi v slovenskem delu Jadranskega morja. (Foto: M. Rogelja)
Sl. 4: Velikega prisesnika (Lepadogaster candolii) najdemo pod večjimi ploščatimi kamni v zgornjem infralitoralu. Pojavlja se globlje od pikastega prisesnika, poleg tega pa ga najdemo pod kamni na morskih travnikih. (Foto: D. Trkov)
Sl. 5: Navadni sklat (Squatina squatina) je ena izmed najbolj ogroženih vrst morskih psov v Sredozemskem morju, marsikje pa je celo že izginil. Novejša opazovanja in sprejeti naravovarstveni ukrepi dajejo upanje, da mu bo vseeno uspelo preživeti. (Foto: L. Kastelic)
Sl. 6: Kozica Palaemon elegans je pogosta vrsta v slovenskem delu Jadrana. V raziskavi prostorske razporeditve in sobivanja različnih kozic v reki Badaševici in pritokih se je pojavljala le v ustju reke. (Foto: B. Mavrič)
INDEX TO IMAGES ON THE COVER
FRONT COVER:
Cryptobenthic fish fauna is an under-researched group of small-sized fish living hidden in their shelters virtually all the time. Among them there are many clingfish species. The shore clingfish (Lepadogaster lepadogaster) on the photograph is a rather common intertidal species. (Photo: D. Trkov)
Fig. 1: Certain clingfish choose very peculiar shelters, such as dead oysters, remains of noble shells or even carapaces of dead crabs. One of these is Apletodon incognitus, a still poorly investigated species. (Photo: D. Trkov) Fig. 2: The reticulated leatherjacket (Stephanolepis diaspros) is a Lessepsian migrant already established in some areas of the eastern Mediterranean Sea. This species is reported to be present in high numbers along the Tunisian coast. (Photo: L. Lipej)
Fig. 3: The giant tun (Tonna galea) is the second largest Mediterranean gastropod. Recently, this rare and endangered
species has also been reported from the Slovenian part of the Adriatic Sea. (Photo: M. Rogelja)
Fig. 4: The Connemara clingfish (Lepadogaster candolii) inhabits spaces under big flat stones in the upper infralittoral
stage. It occurs deeper than shore clingfish and can also be found in seagrass meadows. (Photo: D. Trkov).
Fig. 5: The angel shark (Squatina squatina) is among the most endangered shark species in the Mediterranean,
known to be already absent from certain areas. New records and adopted nature conservation measures are giving
some hope for its survival. (Photo: L. Kastelic)
Fig. 6: The rockpool shrimp Palaemon elegans is a common species in the Slovenian part of the Adriatic Sea. In a research studying the distribution and coexistence of different shrimp species in the Badasevica River and its tributaries, this species was only present at the river mouth. (Photo: B. Mavric)
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Inštitut
IRR S
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