Metadata of the chapter that will be visualized online

Metadata of the chapter that will be visualized online Chapter Title

Alien Benthic Algae and Seagrasses inthe Mediterranean Sea and Their Connection to Global Warming

Copyright Year

2013

Copyright Holder

Springer Science+Business Media Dordrecht

Corresponding Author

Family Name

Hoffman

Particle Given Name

Razy

Suffix

Abstract

Division

The Mina and Everard Goodman Faculty of Life Sciences

Organization

Bar-Ilan University

Address

Ramat Gan, 52900, Israel

Email

[email protected]

Nearly 140 alien benthic-algae taxa and one seagrass invader species were reported found in the Mediterranean Sea since the beginning of the twentieth century. Some caused major changes in the community structure and function of marine flora and fauna. Most non-indigenous species reached the Mediterranean due to anthropogenic activities. The opening of the Suez Canal, along with the increase of marine transportation and mariculture, enabled alien invasion from the Atlantic, Indian, and Pacific Oceans. Alien algae from the Atlantic Ocean probably invade the Mediterranean via the Straits of Gibraltar through cargo ships (through ballast water or attached to the hulls). Shellfish transfer is the most important vector for introducing alien seaweed from the Far East into the western Mediterranean. Global warming raised the surface water temperature, especially in the eastern Mediterranean Basin; therefore, it plays an important role in facilitating settlement establishment and the spread of alien algae and seagrasses from the tropical Atlantic, Indian, and Pacific Oceans in the Mediterranean. The control and reduction of marine invasions are also discussed.

Alien Benthic Algae and Seagrasses in the Mediterranean Sea and Their Connection to Global Warming Razy Hoffman

5

Alien Invasion in the Mediterranean

6

More than 50 years ago, the English zoologist and ecologist Charles Sutherland Elton claimed that the spread of invasive species should be treated as one of the great historical convulsions in the world’s fauna and flora (Elton 1958; Perrings 2010). Since then, invasion phenomena increased rapidly and invasive species became a major threat to fauna, flora, and even many ecosystems all over the world (Lowe et al. 2000). As studies indicated that in many cases invasion was not reversible, it is sometimes regarded as an irreversible type of pollution by certain scientists who study this phenomenon (Boudouresque and Verlaque 2005; Perrings 2010). Biological invasion is the result of species introduction. An Introduced established species must meet four criteria: (1) it colonizes a new area where it did not previously occur; (2) the extension of its range is directly or indirectly linked to human activity; (3) there is no geographical continuity between its native area and the new area; and (4) new generations of the nonnative species are born in situ without human assistance, thus constituting self-sustaining populations (Boudouresque et al. 2005). The significance of invasive species (also known as alien, exotic, nonindigenous, introduced, or nonnative species) in marine ecosystems worldwide has been highlighted and discussed intensively in recent years from ecological, environmental, and economic points of view (Wilcove et al. 1998; Dukes and Mooney 1999; Pimental et al. 2000; Davis et al. 2001; Streftaris et al. 2005). These invasive species often rapidly adapt to their new environments (Huey et al. 2000; Mooney and Cleland 2001), increase in abundance due to high proliferation (Richardson et al. 2000; Kolar and Lodge 2001; Colautti and MacIsaac 2004), play conspicuous roles

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R. Hoffman (*) The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan 52900, Israel e-mail: [email protected]

1 2

10

3

4

in the recipient ecosystems, and sometimes even displace keystone species (Boudouresque and Verlaque 2002) and, therefore, threaten native biological diversity (IUCN 2002). Some of these species can become economically harmful and sometimes even threaten human health (EPA 2001; Hoffman and Dubinsky 2010). The Success of invaders is, however, far from predictable (Richardson et al. 2000). Some studies indicated that only a small fraction of aliens become established, and generally nearly 1 % of these become pests (Williamson 1996). About 6 % of the total species reported so far from the Mediterranean Sea are aliens and the overall inconceivable number of these non-indigenous species has almost reached 1,000, with 718 alien species reported from the eastern Mediterranean Sea, 328 from the western Mediterranean, 267 from the central Mediterranean, and 171 from the Adriatic Sea (Zenetos et al. 2010). The origins of these alien are mainly from the Indian, Pacific or Atlantic Oceans (Zenetos et al. 2005, 2008; Hoffman and Dubinsky 2010). The Mediterranean Sea has experienced a massive ­invasion of hundreds of marine alien species [of Indo-Pacific origin], including Protozoa (Forminifera), algae, Polychaeta, Crustacea, Mollusca, Miscellaneous Invertebrata (Arthropoda Pycnogonida, Bryozoa, Chaetognatha, Chordata Ascidiacea, Cnidaria, Ctenophora, Echinodermata, Porifera, Sipuncula, Nematoda, and Platyhelminthes), and fish species, over a period of only 142 years since the opening of the Suez Canal in Egypt in November 1869 (Goren and Aronov 2002; Galil 2006a; Hoffman and Dubinsky 2010; Zenetos et al. 2010). This invasion is called Lessepsian migration and takes place mostly from the Red Sea to the Mediterranean. However, several species migrated in the opposite direction (anti-Lessepsian migration) (Golani and Ben-Tuvia 1995; Golani et al. 2002). The factors that facilitated the mainly northward transport to the Mediterranean were well described by Por (1971, 1978), who claimed that high salinity and high ­temperature (probably also as a result of global warming) in the Levant Basin of the Mediterranean increase the chances of success of Red Sea invaders. The fact that the Red Sea

S. Goffredo and Z. Dubinsky (eds.), The Mediterranean Sea: Its history and present challenges, DOI 10.1007/978-94-007-6704-1_10, © Springer Science+Business Media Dordrecht 2013

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R. Hoffman 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105

106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126

contains far more species when compared with the temperate fauna in the Mediterranean also contributes to the predominance of Red Sea organisms among Lessepsian migrants. The fact that Indo-Pacific organisms show more versatile adaptation to various ecological niches helps them compete successfully with Mediterranean species and occupy vacant ecological niches as well (Por 1971). It is now estimated that nearly 60 % of the alien species in the Mediterranean Sea passed through the Suez Canal (Zenetos et al. 2010). Other reasons for the northern transport that support species migration are the winds and the northward water current leading from the southern end of the canal to its northern end (Hoffman and Dubinsky 2010). International maritime traffic also plays a very important role (as a transportation vector), conveying marine species all around the world through ships’ ballast water (Nehring 2002, 2005; Streftaris et al. 2005) or attached to ships’ hull fouling (Boudouresque and Verlaque 2010; Hoffman and Dubinsky 2010; Zenetos et al. 2010). Cargo ships pass through the Suez Canal and introduce aliens into the eastern Mediterranean. The invasion of alien species to the western and central Mediterranean is a bit different. Although some alien species spread from the eastern to the central and western Mediterranean or arrived by ship directly from the Indo-­ Pacific, other alien species entered the western Mediterranean from the Atlantic Ocean through the Straits of Gibraltar. Moreover, many alien species in the central and especially the west Mediterranean arrived through shellfish transfer and mariculture (Boudouresque et al. 2011).

 lien Algae and Seagrasses in the A Mediterranean Sea During the twentieth century, the number of exotic alien marine macroalgal species found in the Mediterranean Sea nearly doubled every 20 years (Richardson et al. 2000; Boudouresque and Verlaque 2002). One hundred and thirty nine alien benthic alga and seagrass taxa from the Mediterranean Sea have been identified and reported so far (Table 10.1). Of these, 6 belong to the Cyanobacteria, 23 to the Chlorophyta, 81 to the Rhodophyta, 28 to Ochrophyta, and 1 is a seagrass species (Halophila stipulacea), belonging to the Tracheophyta phylum (Table 10.1). The highest numbers of these alien were reported from the western and eastern Mediterranean, with 92 and 78 taxa, respectively, while lower numbers were found in the central Mediterranean and Adriatic Sea, with 57 and 49 taxa, respectively (Zenetos et al. 2010; Table 10.1). According to Streftaris and Zenetos (2006), 19 of these alien species have caused obvious biodiversity damage and are included in the list of the 100 worst invasive species in the Mediterranean (European Environmental Agency 2007),

which means that 20 % of the worst alien species in the Mediterranean are marine macrophytes! However, the list of invasive seaweed species has grown and today (in 2012) we are talking about 21–29 species of marine macrophytes (seaweeds and seagrass) that should be regarded as invasive (see Table  10.1 and Zenetos et al. 2010). These invaders show negative effects on local Mediterranean marine flora and, therefore, threaten its diversity. Rhodophyta phylum contributes the highest percentage (~60 %) of the reported alien algal taxa entering the Mediterranean (Fig. 10.1), however, distribution data for the indigenous Mediterranean seaweeds from the Chlorophyta, Rhodophyta, and Ochrophyta phyla (Fig. 10.2a) are very close to the percentages established for the alien seaweed taxa found in the Mediterranean (Fig. 10.2b). Consequently, Rhodophyta does not appear to be more efficient in introduction events than the other two groups (Hoffman and Dubinsky 2010). The vast majority of alien algae and seagrasses found in the Mediterranean so far are of natural Indo-Pacific origin and are naturally dispersed from there. The Atlantic Ocean contributed much less alien algae to the Mediterranean (Fig. 10.3). This picture is also clear when we compare the origins of alien seaweeds in the eastern (Fig. 10.4a), western (Fig. 10.4b), and central Mediterranean (Fig. 10.4c) and even the Adriatic Sea (Fig. 10.4d). Some alien algal species found in the Mediterranean are of Indo-Pacific and also Atlantic origin, as seen in Figs. 10.3 and 10.4. It is difficult to determine whether these species arrived from the Indo-Pacific or the Atlantic Oceans. The main vectors that transport alien algae and seagrasses to the Mediterranean (Fig. 10.5) are shellfish transfer, shipping, and the Suez Canal (natural Lessepsian migration). However, a few alien seaweed species were released to the Mediterranean from aquariums or fishing baits. For 17 % of the alien algae, the vector of introduction is unknown. For 7 % of the alien algae, the vector of introduction is controversial (Zenetos et al. 2010 and Table 10.1). The most famous invasive seaweeds in the Mediterranean Sea are probably Caulerpa taxifolia (killer algae), Caulerpa racemosa var. cylindracea (Grape Caulerpa), Codium fragile subsp. fragile (Dead man’s finger), the invasive strain of Asparagopsis taxiformis (Limu kohu), Colpomenia peregrina, Sargassum muticum (Jap weed), Undaria pinnatifida (Wakeme, Asian kelp), and Womersleyella setacea. These are regarded as the worst invasive (Streftaris and Zenetos 2006). C. taxifolia (Chlorophyta), which was accidentally released to the Monaco Mediterranean shore from the Oceanographic Museum of Monaco public aquaria in 1984 (Meinesz 1999; Meinesz et al. 2001), spread rapidly to France, Italy, Spain, Croatia, Albania, Tunisia (Streftaris and Zenetos 2006; Zenetos et al. 2010), and probably to other

127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 179

10  Alien Benthic Algae and Seagrasses in the Mediterranean Sea and Their Connection to Global Warming Table 10.1  List of alien benthic algae and seagrasses reported to be found in the Mediterranean Sea [AU1]

Alien Taxon Cyanobacteria Ocillatoriaceae Lyngbya anomala (C.B. Rao) Umezaki & Watanabe1 Oscillatoria bonnemaisonii (P.L. Crouan & H.M. Crouan) P.L. Crouan & H.M. Crouan ex Gomont2 Oscillatoria miniata (Zanardini) Hauck ex Gomont3 Phormidiaceae Coleofasciculus chthonoplastes (Gomont) M. Siegesmund, J.R. Johansen & T. Friedl2 Microcoleus chthonoplastes (Mertens) Zanardini2,4 Trichodesmium erythraeum Ehrenberg ex Gomont3 Chlorophyta Boodleaceae Boodlea composita (Harvey) F. Brand5 Caulerpaceae Caulerpa distichophylla Sonder6 C. mexicana Sonder ex Kützing5,6,7 C. racemosa var. cylindracea (Sonder) Verlaque, Huisman & Boudouresque6,7 C. racemosa var. lamourouxii f. requienii (Montagne) Weber-van Bosse5,6,7 C. racemosa var. turbinata (J. Agardh) Eubank6,7 C. scalpelliformis (Brown ex Turner) C. Agardh5,6,7 C. taxifolia (M. Vahl) C. Agardh6,7 Cladophoraceae Cladophora herpestica (Montagne) Kützing6,7 C. hutchinsioides Hoek & Womersley6 C. patentiramea (Montagne) Kützing6,7 Codiaceae Codium arabicum Kützing5,8 C. fragile subsp. fragile (Suringar) Hariot6,7 C. parvulum (Bory ex Audouin) P.C. Silva5,6,8,9 C. taylorii P.C. Silva5,6,7 Dasycladaceae Batophora sp.6 Neomeris annulata Dickie5,6,7 Derbesiaceae Derbesia boergesenii (Iyengar & Ramanathan) Mayhoub6,7 D. rhizophora Yamada6,7 Udoteaceae Boodleopsis sp.5 Ulvaceae Ulva fasciata Delile6,7 U. pertusa Kjellman6,7 Ulvaria obscura (Kützing) P. Gayral ex C,Bliding6,7 Rhodophyta Acrochaetiaceae Acrochaetium codicola Børgesen6,7 A. robustum Børgesen6,7 A. spathoglossi Børgesen6,7 A. subseriatum Børgesen6,7

Vector

t1.1

Origin

Status

t1.2 t1.3 t1.4

? ?

IP27 IP&At27

? ?

t1.5

?

IP27

?

t1.8

?

At&IP27

?

t1.10 t1.11

? ?

At&IP27 IP27

? ?

t1.12

t1.6 t1.7 t1.9

t1.13 t1.14 t1.15

?

IP27

CA5

SH? SC7 AQ,SH7

IP6 IP6 IP6

IN6 ES5,6 IN24

t1.18

SC7

IP6

ES6,7

t1.22 t1.23

SC7 SC7 AQ7

IP6 IP6 IP6

QU6 ES6 IN24

t1.24

SC7 ? SC,SH7

IP6 IP6 IP6

ES6 ES6 IN6

SH8 SH,OY7 SH8 SC

IP8 IP6 IP8 IP6

ES8 IN24 IN8,9 ES5,6,7

? SC7

At6 IP6

QU6 ES6

SC7 OY7

IP6 IP6

CA6 ES6

SC

IP27

CA6

OY7? OY7 OY7

IP6 IP6 IP6

ES6 IN6 ES6

t1.16 t1.17 t1.19 t1.20 t1.21

t1.25 t1.26 t1.27 t1.28 t1.29 t1.30 t1.31 t1.32 t1.33 t1.34 t1.35 t1.36 t1.37 t1.38 t1.39 t1.40 t1.41 t1.42 t1.43 t1.44 t1.45 t1.46 t1.47 t1.48 t1.49

SH,OY7 SC7 SC7 SC7

IP&At6 IP6 IP6 IP6

ES6 CA6 CA6 CA6 (continued)

t1.50 t1.51 t1.52 t1.53

R. Hoffman Table 10.1 (continued) t1.54 t1.55 t1.56 t1.57 t1.58 t1.59 t1.60 t1.61 t1.62 t1.63 t1.64 t1.65 t1.66 t1.67 t1.68 t1.69 t1.70 t1.71 t1.72 t1.73 t1.74 t1.75 t1.76 t1.77 t1.78 t1.79 t1.80 t1.81 t1.82 t1.83 t1.84 t1.85 t1.86 t1.87 t1.88 t1.89 t1.90 t1.91 t1.92 t1.93 t1.94 t1.95 t1.96 t1.97 t1.98 t1.99 t1.100 t1.101 t1.102 t1.103 t1.104

Alien Taxon Areschougiaceae Sarconema filiforme (Sonder) Kylin5,6,7,10 S. scinaioides Børgesen6,7 Bangiaceae Porphyra yezoensis Ueda6,7 Bonnemaisoniaceae Asparagopsis armata Harvey6,7 A. taxiformis (Delile) Trevisan de Saint-Léon5,6,7,10 Bonnemaisonia hamifera Hariot6,7 Callithamniaceae Aglaothamnion feldmanniae Halos6,7 Caulacanthaceae Caulacanthus okamurae Yamada6 Ceramiaceae Acrothamnion preissii (Sonder) E.M. Wollaston6,7 Antithamnion amphigeneum A.J.K. Millar6,7 A. hubbsii E.Y. Dawson6 A. nipponicum Yamada & Inagak6,7 Antithamnionella boergesenii (Cormaci & G. Furnari) Athanasiadis6,7 A. elegans (Berthold) J.H. Price & D.M. John6,7 A. spirographidis (Schiffner) E.M. Wollaston6,7 A. sublittoralis (Setchell & Gardner) Athanasiadis6,7 A. ternifolia (J.D. Hooker & Harvey) Lyle6,7 Ceramium bisporum D.L. Ballantine6,7 C. strobiliforme G.W. Lawson & D.M. John6,7 Corallinaceae Lithophyllum yessoense Foslie6,7 Cystocloniaceae Hypnea anastomosans Papenfuss, Lipkin & P.C. Silva6,22 H. cornuta (Kützing) J. Agardh5,6,7,10 H. flagelliformis Greville ex J. Agardh6,7 H. flexicaulis Yamagishi & Masuda6 H. spicifera (Suhr) Harvey5,11 H. spinella (C. Agardh) Kützing5,6,7 H. valentiae (Turner) Montagne6,7 Dasyaceae Dasya sessilis Yamada6,7 Heterosiphonia japonica Yendo6 Delesseriaceae Apoglossum gregarium (E.Y. Dawson) M.J. Wynne6,7 Nitophyllum stellato-corticatum Okamura6,7 Galaxauraceae Galaxaura rugosa (J. Ellis & Solander) J.V. Lamouroux5,6,7,11,12 Gigartinaceae Chondrus giganteus f. flabellatus Mikami6,7 Goniotrichaceae Goniotrichiopsis sublittoralis G.M. Smith6,7 Gracilariaceae Gracilaria arcuata Zanardini6,7 G. vermiculophylla (Ohmi) Papenfuss6

Vector

Origin

Status

SC7 SC7

IP6 IP6

IN5,10 ES6

OY7

IP6

ES6

SH7 SC,SH7 SH7

IP6 IP6 IP6

IN24 IN24 ES6

SH7

At6

ES6

SH7

IP6

ES6

SH7 SH7 SH? OY7 SH?7

IP6 IP6 IP6 IP7 IP6

IN24 ES6 ES6 ES6 CA6

SH7 SH7 SH7 SH7 SH7 SH?7

IP7 IP6 IP6 IP7 At6 At6

CA6,7 ES6 ES6 ES6 CA7 CA7

OY7

IP6

IN6

SC22 SC7 SC7 SH? SC11 SH?7 SC,SH7

IP6 IP7 IP6 IP6 IP27 IP&At6 IP6

ES6 ES6 ? ES6 ES5 ES6 ES6

OY7 OY7

IP6 IP6

ES6 IN6

SH7 OY7

IP6 IP6

ES6 ES-IN6,7

SH8,10

IP&At10

IN8

OY7

IP6

ES-IN6,7

SH7

IP6

ES6

SC7 OY23

IP6 IP6

CA6 IN6 (continued)

10  Alien Benthic Algae and Seagrasses in the Mediterranean Sea and Their Connection to Global Warming Table 10.1 (continued) Alien Taxon Halymeniaceae Grateloupia asiatica S. Kawaguchi & H.W. Wang6,7 G. lanceolata (Okamura) Kawaguchi6,7 G. minima P.L. Crouan & H.M. Crouan6 Grateloupia patens (Okamura) S. Kawaguchi & H.W. Wang6,7 G. subpectinata Holmes6,7 G. turuturu Yamada6,7 Liagoraceae Ganonema farinosum (J.V. Lamouroux) K.C. Fan & Yung C. Wang6,7,10 Nemalion vermiculare Suringar6,7 Lomentariaceae Lomentaria flaccida Tanaka6 L. hakodatensis Yendo6,7 Phyllophoraceae Ahnfeltiopsis flabelliformis (Harvey) Masuda6,7 Plocamiaceae Plocamium secundatum (Kützing) Kützing6,7 Rhodomelaceae Acanthophora najadiformis (Delile) Papenfuss5,6,7,10 Chondria coerulescens (J. Agardh) Falkenberg6,7 C. curvilineata F.S. Collins & Hervey6,7 C. pygmaea Garbary & Vandermeulen6,7 Herposiphonia parca Setchell6,7 Laurencia caduciramulosa Masuda & Kawaguchi6,7 L. okamurae Yamada6,7 Lophocladia lallemandii (Montagne) F. Schmitz6,7 Neosiphonia harveyi (J.W. Bailey) M.S. Kim, H.G. Choi, Guiry & G.W. Saunders6,13 Osmundea oederi (Gunnerus) G. Furnari14,6 Polysiphonia atlantica Kapraun & J.N. Norris6,7 P. fucoides (Hudson) Greville6,7 P. morrowii Harvey6,7 P. paniculata Montagne6,7 P. stricta (Dillwyn) Greville6 Pterosiphonia tanakae S. Uwai & M. Masuda6,7 Symphyocladia marchantioides (Harvey) Falkenberg6,7 Womersleyella setacea (Hollenberg) R.E. Norris6,7 Rhodophysemataceae Rhodophysema georgei Batters6,7 Rhodymeniaceae Botryocladia madagascariensis G. Feldmann6,7 Chrysymenia wrightii (Harvey) Yamada6,7 Rhodymenia erythraea Zanardini6,7 Solieriaceae Agardhiella subulata (C. Agardh) Kraft & M.J. Wynne6,7 Solieria dura (Zanardini) F. Schmitz6,7 S. filiformis (Kützing) P.W. Gabrielson6,7 Stylonemataceae Goniotrichiopsis sublittoralis G.M. Smith6,7

Vector

Origin

Status

OY7 OY7 OY? OY7 OY7 OY7

IP6 IP6 IP6 IP6 IP6 IP6

ES6 IN25 ES6 CA6,7 ES6 IN24

SC10

IP6

ES26

t1.113 t1.114

OY7

IP6

ES6

t1.115

OY? OY7

IP6 IP6

CA6 ES6

OY7

IP6

IN25

?

IP&At6

ES6

SC7 OY7 SH7 SC7 OY7 SH7 OY7 SC,SH7 SH7

IP6 At6 At6 IP6 IP6 IP6 IP6 IP6 IP6

IN5,10 IN25 ES6 ES6 ES6 ES6 ES6 IN24 IN25

t1.124

OY14,SH OY,SH7 FB7 OY7 ? ? OY7 SH7 SH7

At6 At6 At6 IP6 IP6 At6 IP6 IP6 IP6

CA6 CA6 ES6 ES6 ES6 ES6 IN25 ES6 IN24

t1.134

OY7

IP&At6

CA6

SH7 OY7 SC,SH7

IP6 IP6 IP6

ES6 ES6 CA6

OY7 SC7 ?

IP&At6 IP6 At6

ES6 CA6 ES6

SH7

IP6

t1.105 t1.106 t1.107 t1.108 t1.109 t1.110 t1.111 t1.112

t1.116 t1.117 t1.118 t1.119 t1.120 t1.121 t1.122 t1.123 t1.125 t1.126 t1.127 t1.128 t1.129 t1.130 t1.131 t1.132 t1.133 t1.135 t1.136 t1.137 t1.138 t1.139 t1.140 t1.141 t1.142 t1.143 t1.144 t1.145 t1.146 t1.147 t1.148 t1.149 t1.150 t1.151 t1.152 t1.153

ES6 (continued)

t1.154

R. Hoffman Table 10.1 (continued) t1.155 t1.156 t1.157 t1.158 t1.159 t1.160 t1.161 t1.162 t1.163 t1.164 t1.165 t1.166 t1.167 t1.168 t1.169 t1.170 t1.171 t1.172 t1.173 t1.174 t1.175 t1.176 t1.177 t1.178 t1.179 t1.180 t1.181 t1.182 t1.183 t1.184 t1.185 t1.186 t1.187 t1.188 t1.189 t1.190 t1.191 t1.192 t1.193 t1.194 t1.195 t1.196 t1.197 t1.198 t1.199 t1.200 t1.201

Alien Taxon Wrangeliaceae Anotrichium okamurae Baldock6,7 Griffithsia corallinoides (Linnaeus) Trevisan6,7 Pleonosporium caribaeum (Børgesen) R.E. Norris7,15 Ochrophyta Alariaceae Undaria pinnatifida (Harvey) Suringar6,7 Chordaceae Chorda filum (Linnaeus) Stackhouse6,7 Chordariaceae Acrothrix gracilis Kylin6,7 Botrytella parva (Takamatsu) Kim6,7 Cladosiphon zosterae (J. Agardh) Kylin6,16 Corynophlaea crispa (Harvey) Kuckuck17 Halothrix lumbricalis (Kützing) Reinke6,7 Leathesia marina (Lyngbye) Decaisne6,7 Punctaria tenuissima (C. Agardh) Greville6,7 Microcoryne ocellata Strömfelt18 Microspongium globosum Reinke19 M. tenuissimum (Hauck) A.F. Peters6 Sphaerotrichia firma (Gepp) A.D. Zinova6,7 Desmarestiaceae Desmarestia viridis (O.F. Müller) J.V. Lamouroux16 Dictyotaceae Padina antillarum (Kützing) Piccone6 P. boergesenii Allender & Kraft5,6,7 P. boryana Thivy5,6,7 Rugulopterix okamurae (E.Y. Dawson) Hwang, Lee & Kim6,7 Spatoglossum variabile Figari & De Notaris6,7 Stypopodium schimperi (Buchinger ex Kützing) Verlaque & Boudoresque5,6,7,8 Ectocarpaceae Ectocarpus siliculosus var. hiemalis (P.L. Crouan & H.M. Crouan) Kuckuck6,7,20 Fucaceae Fucus spiralis Linnaeus6,7 Laminariaceae Saccharina japonica (Areschoug) C.E. Lane, C. Mayes, Druehl & G.W. Saunders6,7 Pylaiellaceae Pylaiella littoralis (Linnaeus) Kjellman6,16 Sargassaceae Sargassum muticum (Yendo) Fensholt Setchell6,7 Scytosiphonaceae Colpomenia peregrina Sauvageau6,7 Compsoma saxicola (Kuckuck) Kuckuck21 Scytosiphon dotyi M.J. Wynne6,7

Vector

Origin

Status

SH7 OY7 SH,OY7

IP6 IP&At6 At7

CA6 ES6 CA7

OY7

IP6

IN24

OY7

IP&At6

ES6

OY7 ? ? ? OY7 OY7 OY7 ? ? ? OY7

IP&At6 IP6 At6 At27 IP&At6 IP&At6 At6 At27 At27 At6 IP6

ES6 ES6 ES6 ? ES6 ES6 ES6 ? ? ES6 ES6

?

IP&At6

IN25

? SC7 SC7 OY7 SC7 SC7

IP6 IP6 IP6 IP6 IP6 IP6

CA6 IN5 CA-ES5,6 CA6 CA6 IN8,24

?

At6

ES6

FB7

At6

CA6

OY7

IP6

CA6

?

IP&At6

ES6,25

OY7

IP6

IN24

SH7 ? OY7

IP6 At27 IP6

ES6 ? ES6 (continued)

[AU2]

10  Alien Benthic Algae and Seagrasses in the Mediterranean Sea and Their Connection to Global Warming Table 10.1 (continued) Alien Taxon Magnoliophyta Hydrocharitaceae Halophila stipulacea (Forsskål) Ascherson6,7

Vector

Origin

Status t1.202 t1.203

SC16,SH?

IP6

IN24

Abbreviations of probable vectors of introduction: SH marine shipping (ballast water, ship fouling, and anchors), SC Suez Canal, AQ aquarium, OY oyster and clam aquaculture, and FB fishing bait. Abbreviations of probable origins of alien and natural dispersal: IP Indo-Pacific (Pacific and/ or I ndian Oceans, including the Red Sea), At Atlantic. Abbreviations of the status of the establishment of alien species in the Mediterranean: QU questionable, CA casual, ES established, and IN invasive (localized or widespread, and a possible threat to flora and biodiversity) 1 Reference: Kurt et al. (2001) 2 Reference: Taskin et al. (2001) 3 Reference: Taskin et al. (2008) 4 According to Guiry and Guiry (2011) this species is now regarded as Coleofasciculus chthonoplastes (Gomont) M. Siegesmund, J.R. Johansen & T. Friedl 5 Hoffman et al. (submitted) 6 Reference: Zenetos et al. (2010) 7 Reference: Boudouresque and Verlaque (2010) 8 Reference: Hoffman et al. (2011) 9 Reference: Israel et al. (2010) 10 Reference: Hoffman and Dubinsky (2010) 11 Reference: Aleem (1993) 12 Reference: Hoffman et al. (2008a) 13 Boudouresque and Verlaque (2010) probably identified this species as Polysiphonia harveyi J.W. Bailey 14 Reference: Serio et al. (2008) 15 According to Wynne (2005) and Guiry and Guiry (2011) this species is now regarded as Spongoclonium caribaeum (Børgesen) M.J. Wynne 16 Reference: Verlaque et al. (in press) 17 Reference: Taskin (2006) 18 Reference: Taskin et al. (2010) 19 Reference: Ozturk et al. (2006) 20 According to Guiry and Guiry (2011) this taxon is now regarded as Ectocarpus siliculosus (Dillwyn) Lyngbye 21 Reference: Taskin et al. (2007) 22 Lipkin (1972a) identified this species as H. esperi Bory de Saint-Vincent 23 Reference: Sfriso et al. (2010) 24 Reference: Streftaris and Zenetos (2006) 25 Reference: Boudouresque et al. (2011) 26 Based on Israeli national herbariums catalogs and 2011 unpublished surveys 27 Reference for distribution: Guiry and Guiry (2011)

Fig. 10.1 Distribution of alien algae by phyla: blue sector represents Cyanobacteria, green – Chlorophyta, red – Rhodophyta, and yellow – Ochrophyta

Mediterranean shores. It is often called the “killer algae” since it is predominant in many underwater habitats, oppresses the local marine flora, and causes very serious ecological problems by dramatically decreasing biodiversity in native marine ecosystems (Gravez et al. 2001). C. racemosa is a very old invader in the Mediterranean; however, this species has several subspecies and variants. C. racemosa var. cylindracea was first observed in the early 1990s in Libya. This taxon spread rapidly throughout most of the Mediterranean Sea, occupied a wide range of habitats, and developed extensive populations. Its rapid invasion of the Mediterranean deeply changed phytobenthic community structure (Piazzi et al. 2001) and decreased seaweed diversity (Gravez et al. 2001) at many locations. Studies of the

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Fig. 10.2  Distribution of seaweeds by phyla: (b) native species in the Mediterranean (Boudouresque 2003; Zenetos et al. 2010) (b) alien taxa in the Mediterranean (Table 10.1). Green sector represents Chlorophyta, red – Rhodophyta, and yellow – Ochrophyta

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from Japan (Scagel 1956; Harries et al. 2007; Boudouresque and Verlaque 2010). C. fragile subsp. fragile was first observed in the Mediterranean Sea in 1946 as C. fragile subsp. tomentosoides (van Goor) P.C. Silva (Boudouresque and Verlaque 2010; Zenetos et al. 2010). This species (and S. muticum too) also expands the dispersal of from Japan to the east Pacific, the north Atlantic and the North Sea, however; it has also been reported as being found in the south Pacific and South African shores (Chapman 1999). In some north Atlantic shores of America, this invader was found to grow at very high densities and damage the natural kelp forests and its Fig. 10.3  General distribution of all alien algae reported to be found in ecosystem (Provan et al. 2005). the Mediterranean so far by their geographical origin. Red sector repreAsian kelp (U. pinnatifida) was first reported seen in the sents Indo-Pacific origin, yellow – Atlantic origin, and blue – Indo-­ Mediterranean Sea in 1971 at the Thau lagoon (France), Pacific and Atlantic origin (Modified from Zenetos et al. 2010 and which is identified as a hotspot to invaders introduced Table 10.1) through shellfish transfer (Uwai et al. 2006; Boudouresque and Verlaque 2010). U. pinnatifida also invaded the south effects of C. racemosa on local flora showed that the total and east Pacific as well as the north Atlantic coasts (Uwai percentage of cover and diversity of the indigenous flora and et al. 2006). fauna was lower in invaded areas when compared with the A. taxiformis was first reported seen in the Mediterranean control areas, where C. racemosa was absent (Piazzi and at the end of the nineteenth century; however, in 1996, a new Cinelli 2003) and, therefore, it should be regarded as a seri- strain of this species was observed for the first time. This ous threat to local marine flora, fauna, and ecosystems in the Indo-Pacific variant acted extremely invasive and spread rapMediterranean (Verlaque et al. 2004; Streftaris and Zenetos idly to all parts of the Mediterranean Sea (Boudouresque and 2006). Verlaque 2010; Zenetos et al. 2010). S. muticum, U. pinnatifida, and C. fragile subsp. fragile C. peregrine is an old-time invader since 1918 were introduced into the Mediterranean through shellfish (Boudouresque and Verlaque 2010). This brown puffy (filled transfer (Boudouresque and Verlaque 2010). These three with air) seaweed, which probably arrived from the Pacific species (especially S. muticum and C. fragile subsp. fragile) Ocean, is often called the oyster thief (also the nickname of also expand dispersal across the globe and became global C. fragile subsp. fragile) since it tends to grow on oyster threats to marine ecosystems all over the world. shells, lifting the oysters floating away from the seabed and S. muticum is a very successful invasive species (Critchley causing problems to oyster farmers, who lose some of their et al. 1990). It is native to the waters around Japan and the harvests. northwest Pacific, where it is an ecologically insignificant W. setacea (such as A. taxiformis, C. racemosa var. cylincomponent of the marine flora (Norton 1977; Critchley dracea and C. fragile subsp. fragile) is found in all four 1983). During the last 50 years, this species invaded the east basins of the Mediterranean (western, eastern, central, and Pacific coast of North America and Mexico, the Mediterranean also the Adriatic Sea) (Zenetos et al. 2010). This brown Sea (since 1980), the north Atlantic, and the North Sea as a algae was first discovered in 1986 (Boudouresque and consequence of the importation of cultivated Pacific oysters Verlaque 2010).

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10  Alien Benthic Algae and Seagrasses in the Mediterranean Sea and Their Connection to Global Warming

Fig. 10.4 (a, b and c) represent distribution in the eastern, western, and central Mediterranean, and (d) represents distribution in the Adriatic Sea (Modified from Zenetos et al. 2010 and Table 10.1)

Fig. 10.5  Distribution of alien algae by vectors of introduction to the Mediterranean. Blue represents shellfish transfer, green – shipping, red – Suez Canal, yellow – unknown vector, brown – Suez Canal and/or shipping, purple – shellfish transfer and/or shipping, pink – marine aquarium, and white – fishing bait

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 lien Seaweeds and Their Impact A in the Israeli Mediterranean Twenty-one alien-seaweed taxa from the Israeli Mediterranean have been identified so far (6) (Hoffman and

Dubinsky 2010, Hoffman et al. submitted; Table 10.1). Caulerpa mexicana (Fig. 10.6), Caulerpa racemosa var. lamourouxii, Caulerpa scalpelliformis (Fig. 10.7), Codium taylorii (Fig. 10.8), Boodleopsis sp., Ulva fasciata, Sarconema filiforme (Figs. 10.9 and 10.10), Asparagopsis taxiformis, Hypnea cornuta (Fig. 10.11), Hypnea spinella (Fig.  10.12), Acanthophora najadiformis (Fig. 10.13), Padina boergesenii (Fig. 10.14), Stypopodium schimperi (Fig.  10.15), and Ganonema farinosum (Fig. 10.16) were collected from the Israeli Mediterranean and stored at the national seaweed herbaria (Tel Aviv University and the Hebrew University of Jerusalem) in the twentieth century (Hoffman et al. submitted). During the first decade of the twenty-first century, seven new alien seaweeds (constituting 33 % of the total aliens found) were found along the Mediterranean shores of Israel. Seaweed surveys (Hoffman et al. submitted) took place during the new millennium and checklists of the found taxa were prepared and compared to the catalogs of the Israeli national seaweed herbaria of the Mediterranean. Literature reports of macroalgal surveys from the Israeli Mediterranean (Edelstein 1960, 1962, 1964; Lipkin and Safriel 1971; Lundberg 1981, 1986, 1991, 1995, 1996) were also checked.

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Fig. 10.6  Caulerpa Mexicana Fig. 10.9  Sarconema filiforme growing at the intertidal zone

Fig. 10.7  Caulerpa scalpelliformis

Fig. 10.10  Sarconema filiforme often used as fishing bait at the north Israeli shore

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Fig. 10.8  Codium taylorii

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The new aliens found were: Boodlea composita (two observations at the same location), Codium arabicum (Fig. 10.17), Codium parvulum (Fig. 10.18), Neomeris annulata, Hypnea spicifera, Galaxaura rugosa (Fig. 10.19), and Padina boryana (Hoffman et al. submitted). C. arabicum, C. parvulum, and G. rugosa were recorded at the northern Israeli Mediterranean shore, particularly near the marine port at Haifa Bay (Fig. 10.20). The reports of C. arabicum and C. parvulum from in the bay are the first records of these alien species in the Mediterranean (Hoffman et al. 2011).

10  Alien Benthic Algae and Seagrasses in the Mediterranean Sea and Their Connection to Global Warming

Fig. 10.11  Hypnea cornuta growing in an intertidal pool

Fig. 10.14  Padina boergesenii

Fig. 10.12  Hypnea spinella exposed during low tide

Fig. 10.15  Stypopodium schimperi

Fig. 10.13  Acanthophora najadiformis

Fig. 10.16  Ganonema farinosum

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Fig. 10.17  Codium arabicum specimen drifted to shore at Haifa Bay Fig. 10.20  Haifa Bay area (Insert map scale bars 100 km, main map scale bars 5 km)

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Fig. 10.18  Codium parvulum

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Fig. 10.19  Galaxaura rugosa

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There are some S. schimperi populations along the Israeli coast; however, a large population is concentrated in Haifa Bay and the surrounding area. This species, which is well known as being invasive in the eastern Mediterranean basin, especially along the Levantine shores (Verlaque and Boudouresque 1991) in Syria (Mayhoub and Billard 1991) and Lebanon (Bitar et al. 2000, 2003), also spread to Egypt, Libya, and Turkey (Bitar et al. 2000), and was even reported to be found in the Aegean Sea (Cocito et al. 2000). The appearance and concentration of S. schimperi, G. rugosa, C. parvulum, and C. arabicum in the Haifa Bay area indicated that the marine vegetation has changed since Edelstein described this site (Edelstein 1960, 1962, 1964) more than 50 years ago. The conspicuous phenomena that clearly indicate proliferation of these alien seaweeds are enormous winter and spring drift events that occurred each year at the bay. During the years 2004–2008, several major algal blooms cast ashore thousands of tons of algal biomass (Israel et al. 2010; Hoffman et al. 2011). These drifts, which mainly contained fragmented C. parvulum, G. rugosa, and S. schimperi (Fig. 10.21), filled the seawater and rotted along the bay’s beaches. Observation and later calculation of alien and local seaweed abundance in the bay drift indicated that winter drifts contained ~80 % alien seaweeds (Fig. 10.22a), while in the spring, their share decreased to ~50 % (Fig. 10.22b) of the total (Hoffman et al. 2011). It seems that most alien seaweed biomass that drifted to the Haifa Bay shores during winter and spring came from the infralittoral and sublittoral zones. However, C. parvulum, G. rugosa, S. schimperi, and C. arabicum (the latter was the main alien in the summer drifts) were also found growing in small quantities in

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potholes and pools located in the bay intertidal zone (Hoffman et al. 2011). The invasion and establishment of opportunistic alien seaweeds in Haifa Bay might be extremely harmful to the natural marine ecosystem for two reasons: (1) the replacement of local flora might lead to the extinction of some native seaweed species, e.g., the unexplained disappearance of Halimeda tuna (J. Ellis et Solander) J.V. Lamouroux (Hoffman et al. 2008b); this calcified green alga was very abundant in the Haifa Bay area over 50 years ago (Edelstein 1960, 1962; Edelstein and Komarovsky 1961); (2) alien Indo-Pacific seaweed proliferation might provide suitable settlement and establishment conditions for alien grazer species, which may displace native ones. In general, the invasion of alien species might cause the disruption of the local ecosystem structure and its energy and nutrient flows, resulting in its subsequent collapse (Hoffman et al. 2011). Since becoming invasive is the climax of the process that begins with establishment and local spread, followed by increase in abundance (Richardson et al. 2000; Kolar and

Fig. 10.21  The three invaders seaweeds found in the Haifa Bay winter and spring drifts. From right to left, Stypopodium schimpery, Galaxaura rugosa, and Codium parvulum

Lodge 2001), the aliens, S. schimperi, G. rugosa, C. parvulum, and C. arabicum, should be regarded and treated as invasive species in the Mediterranean, since they threaten the local marine flora, can reduce biodiversity, and have the potential for disrupting ecosystem function. Of these four species, G. rugosa and C. arabicum have the widest world dispersal among Indo-Pacific invaders, which may be indicative of their opportunistic capabilities and ecological flexibility. Therefore, it is quite possible that their dispersal might easily expand to other Mediterranean coastlines. On the basis of the observation that showed that these new four invader seaweed species were mainly found at Haifa Bay (Hoffman and Dubinsky 2010; Hoffman et al. 2011, submitted), where many cargo ships anchor, and taking into consideration the weather conditions in the eastern Mediterranean Sea, a new model (Fig. 10.23) that shows all of the factors likely to cause and facilitate Indo-Pacific seaweed invasions in the region, was established. As industrialization proceeds, the concomitant growth of marine trade increases the invasion and dispersal of alien organisms worldwide, and particularly in the eastern Mediterranean Basin (Rilov and Crooks 2009). The tendency of most of the four newly reported Indo-Pacific invader seaweeds to concentrate in the Haifa Bay area strongly points to cargo ships as the main transport vector. These ships carry seaweed attached to their hulls or as fragments in their ballast water, and spill them after loading containers at port. Alien seaweeds can survive microscopic stages in the ballast water tanks of cargo ships that arrive at Mediterranean ­harbors (Flagella et al. 2007). Seaweeds depend upon water-circulation patterns and waves to facilitate dispersal. As C. arabicum, C. parvulum, and G. rugosa were not found south of the Haifa Bay area, the flow through the Suez Canal probably had no effect on these invasions. However, their occurrence north of Haifa Bay indicates that the long-shore north-flowing currents may have had an effect on the northward spread following the first invasion (Hoffman et al. 2011).

Fig. 10.22  Distribution pool (%) of seaweeds in the Haifa Bay drifts during winter (a) and spring (b) of 2005–2009. Red sector represents G. rugosa, brown – S. schimperi, green – C. parvulum, and blue – native algal species

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R. Hoffman Fig. 10.23  Alien Indo-Pacific seaweed invasion model for Haifa Bay. Squares represent the conditions that cause invasions; circles represent the factors that facilitate settlement and establishment

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Former Indo-Pacific invaders previously reported from the Israeli Mediterranean, and which became very common, such as Acanthophora nayadiformis, Hypnea cornuta, Sarconema filiforme, and Codium taylori, were also commonly found on the southern shores of Israel. Hence, there is a possibility that some of these species might have arrived at the Israeli Mediterranean in a northward flow through the Suez Canal and through long-shore north-flowing currents (Hoffman et al. 2011). So far, there is no evidence that alien-seaweed species were accidentally released (as was the case of C. taxifolia in Monaco) or introduced to the Israeli Mediterranean coast through shellfish transfer since there are no oyster farms along these shores (Hoffman et al. 2011). Global warming has serious effects on marine ecosystems (Belkin 2009), and might play a large role in the invasion process (Mooney and Hobbs 2000). Mediterranean sea-surface temperatures have increased by 2–3 °C in the southern and eastern Mediterranean since the 1980s (EEA 2007). Comparison of annual mean seawater-surface temperatures between the Israeli Mediterranean and the tropical Israeli Red Sea shows that these temperatures are very similar (24 and 23.5 °C, respectively). However, the mean sea-­ surface temperature amplitude in the Israeli Mediterranean is greater than that of the Red Sea (Hoffman et al. 2011). Therefore, the main factors facilitating the invasion of alien

seaweed species of tropical origin into the Israeli Mediterranean shores might be the naturally high temperatures in the Levant Basin as well as the global-warming process. As sea-surface temperatures during winter rose, the conditions became ideal for the newly arriving tropical Indo-­Pacific seaweed species to settle, establish communities, and extend their dispersal. The mean sea-surface temperature in Haifa Bay during February is nearly 20 °C, which is similar to tropical Red Sea surface temperatures (~21 °C); therefore, tropical Indo-Pacific seaweed invaders that arrive at the eastern Mediterranean Sea (such as those arriving from the Red Sea) find favorable temperatures in the recipient Israeli-Mediterranean marine ecosystem. These high temperatures may initially facilitate survival and settlement and later facilitate reproduction and dispersal (Hoffman et al. 2011). Another important factor that makes the Haifa Bay shores a hotspot for alien seaweeds and facilitates their invasion is the low local macroalgal diversity. Although the Mediterranean Sea is considered rich in species considering its size (Rilov and Galil 2009), Israeli Levant macroalgal diversity is poor compared to that of other Mediterranean shores (on the basis of local published seaweed surveys and national herbaria). In addition, the Haifa Bay area is characterized by rich, diverse, and three-dimensional habitats present on the wide and long underwater reef.

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In general, seawater near marine ports is chemically p­ olluted (Ng and Song 2010), which sometimes makes environmental conditions less tolerable for some native species (Rilov and Crooks 2009). Therefore, seaweeds that grow near ports might be more tolerant than others to such pollution. Since Haifa Bay became highly polluted at the end of the twentieth century and at the beginning of the new millennium, some tolerant and opportunistic newcomer seaweeds might find this pollution to be a positive factor that gives them advantages over the less-tolerant local species, perhaps facilitating the success of invaders in the bay (Hoffman et al. 2011).

 alophila stipulacea – An Old-Timer Invasive H Alien Seagrass in the Mediterranean Nearly 60 seagrass species were reported found in marine ecosystems around the world. These are distributed in four families: Cymodoceaceae, Hydrocharitaceae, Posidoniaceae, and Zosteraceae [if we don’t include Potagmogetonacea, which provides eight more species not regarded as seagrasses because they do not occur in oceanic water with consistently high salinity (Den Hartog 1970)], and eleven genera; however, only four of these (Cymodocea nodosa, Posidonia oceanica (endemic), Zostera noltii, and Zostera marina) are regarded as native Mediterranean species (Phillips and Meñez 1988; Lipkin et al. 2003; Procaccini et al. 2003; Borum and Greve 2004). Halophila stipulacea (Forsskål) Ascherson (Hydrocharitaceae) (Fig. 10.24) is, so far, the only alien-seagrass species reported in the Mediterranean. This species,

Fig. 10.24  Halophila stipulacea growing in aquarium in Israel

which mainly grows on sandy and muddy substrates along the eastern coast of Africa, originally has Indian Ocean and Red Sea distribution. The first record of this invasive species from the Mediterranean was in June 1894 (nearly two and a half decades after the opening of the Suez Canal), from the island of Rhodes (Fritsch 1895; Por 1971; Lipkin 1975a). Since then, this species spread to many coasts along the eastern basin of the Mediterranean, where it was also reported to be found in the Egyptian Mediterranean (Täckholm et al. 1941; Aleem 1962), Cyprus (Lipkin 1975b), Lebanon (Lipkin 1975b) Turkey (Alpinar 1987; Taskin et al. 2008), Greece and its surrounding islands (Politis 1930; Tsirika and Haritonidis 2005; Guiry and Guiry 2011), Albania (Tan and Mullaj 2000; Kashta et al. 2011), Malta (Verlaque 1994), Libya, and some shores in eastern Tunisia (Sghaier et al. 2011). Although H. stipulacea was one of the first alien marine macrophytes reported in the Mediterranean since the opening of the Suez Canal, it did not spread fast and about 100 years after its first record from the eastern basin of the Mediterranean it was reported for the first time in the western Mediterranean (Procaccini et al. 2003), in the island of Sicily (Verlaque 1994; Procaccini et al. 1999; Di Martino et al. 2006). Later, it was also observed at the Tyrrhenian Sea in southwest Italy (Gambi et al. 2009). Lately, H. stipulacea has also been reported for the first time in the Caribbean Sea in the west tropical Atlantic shores (Ruiz and Ballantine 2004) where it was found growing off the shores of Granada, Dominica, and St. Lucia (all parts of the Lesser Antilles) (Willette and Ambrose 2009). On the island of Dominica, it was found growing at seven locations and it was observed that this invasive alien species became the third most common seagrass in the area (an overall of six indigenous species were reported in this island previously) (Steiner et al. 2010). H. stipulacea probably reached the Mediterranean through the Suez Canal; however, the fact that this species was mainly found in or near bays with ports, harbors, and marinas, such as the Port Said and Marsa Matrukh harbors in Egypt, Port of Sidon in Lebanon, Rhodes harbor, Cyprus harbors, Tobrouk Bay in Libya, the marina at Cap Monastir in Tunisia, Palinuro harbor in Italy, and several Caribbean bays, supports the assumption that the main transportation vector of this species is boats (Täckholm et al. 1941; Aleem 1962; Lipkin 1975a, b; Ruiz and Ballantine 2004; Gambi et al. 2009; Sghaier et al. 2011). According to Lipkin (personal communication), the main transportation vectors that spread H. stipulacea in the Mediterranean Sea are dredgers. These boats drag their nets in order to collect mollusks from the seabed. H. stipulacea shoots and other organisms are also caught in the nets and later released in the ports where the dredgers anchor. The fact that this seagrass was found all over the eastern basin of the Mediterranean except Israel supports this assumption. Owing to the political situation in

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R. Hoffman t2.1

Table 10.2  General features of Mediterranean seagrass meadows (Buia et al. 2000; Procaccini et al. 2003)

t2.2 t2.3 t2.4 t2.5 t2.6 t2.7

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Density (shoots/m2) Leaf area (m2/m2) Leaf biomass gdw/m2

Posidonia oceanica shallow 700 6.16–29 175–670

Posidonia oceanica deep 160 1.1–2.6 52–94

Cymodocea nodosa 925–1,925 0.2–3.5 17–159

the Middle East, dredgers from the Arabs countries that surround Israel are not allowed to approach the territorial Mediterranean seawater of Israel and, therefore, H. stipulacea did not reach the Israeli coast. Today, H. stipulacea is considered one of the 100 worst invasive species in the Mediterranean. Certain studies that compared the general features of Mediterranean seagrass-­ species meadows in Italy (Table 10.2) showed that H. stipulacea has extremely high shoot density (especially when its beds are located in shallow waters) compared to the other four species. The leaf area and biomass of this invasive species were also found to be high (Buia et al. 2000; Procaccini et al. 2003). Seagrass decline is a worldwide phenomenon and the global loss of seagrass from direct and indirect human impacts was estimated to be 33,000 km2, or 18 % of the documented seagrass area during 20 years of population monitoring (Duarte et al. 2004). The main reason for seagrass-bed decline is seawater pollution, which increases eutrophication that leads to reduction in water clarity. As seagrasses have relatively high light requirements, the decrease in light penetration of coastal waters reduces their photosynthesis efficiency and makes them vulnerable (Duarte et al. 2004; Bernard et al. 2007). Other reasons that contribute to seagrass decline include fishing, aquaculture, boating, anchoring, and coastal alteration. Introduced alien species also play an important role in seagrass decline, especially along the Mediterranean coasts. Two alien exotic and toxic green seaweed species, C. taxifolia and C. racemosa, were reported to be a major threat to seagrass beds of the Mediterranean since they grow rapidly and compete with seagrasses for the soft-bottom substratum, which is favored by seagrasses (de Ville`le and Verlaque 1995; Ceccherelli and Cinelli 1997; Ceccherelli et al. 2000; Duarte et al. 2004; Pergent et al. 2008). C. taxifolia grows rapidly, and largely appears to colonize areas devoid of seagrasses, but has also been reported to compete with P. oceanica off the shore of Monaco for space and resources, being able to damage its meadows (Duarte et al. 2004; Pergent et al. 2008). Moreover, this species drastically reduced biodiversity in seagrass beds (Streftaris and Zenetos 2006). The grape alga, C. racemosa var. cylindracea, easily invaded C. nodosa and Z. noltii beds and affected both soot and flower density of both seagrasses in their meadows (Ceccherelli and Campo 2002; Piazzi et al. 2005),

Halophila stipulacea shallow 19,728 5 157.8

Halophila stipulacea deep 13,000 5.9

Zostera noltii 269–1,246 0.2–0.4 13–79

Zostera marina 216–1,093 1.7–6.7 45–755

but when it comes to P. oceanica, the Grape Caulerpa prefers dominating on its dead mattes, and no colonization was observed in dense meadows (Streftaris and Zenetos 2006). No direct damage to the local seagrass meadows in the Mediterranean by H. stipulacea has been reported yet (Duarte et al. 2004); however, it seems that this invasive species prefers settling on dead mattes of endemic Mediterranean seagrass P. oceanica (Gambi et al. 2009), and therefore might prevent the future recovery of its mattes. H. stipulacea also plays an important role in the process and the success of other alien invasions, as was the case with the invasion of the seaweed C. pygmaea (Zenetos et al. 2011) or the anaspidean mollusk Syphonota geographica, which is dietary depends on this seagrass (Mollo et al. 2008). S. geographica example indicates that the initial invasion of an exotic pest such as H. stipulacea might have paved the way for the subsequent invasion of trophic specialists that take advantage of niche opportunities (Mollo et al. 2008) and some of these invaders might also have negative effects on local Mediterranean flora and fauna. Global climate changes might have a substantial long-­ term impact on seagrass ecosystems. The expected increase of surface-seawater temperatures in the Mediterranean may be a major threat to local seagrass populations, especially those living close to their low latitude border of distribution, such as Z. marina, C. nodosa, and in particular, the Mediterranean endemic seagrass P. oceanica (Duarte et al. 2004). Z. marina and P. oceanica have succeeded in colonizing cold temperate water; however, the rise of temperatures might push them to their distributional limits (Duarte et al. 2004), giving C. taxifolia, C. racemosa, and H. stipulacea advantages over the two indigenous seagrasses. Moreover, high water temperatures might increase the possibility of the invasion of other seagrasses from the Red Sea to the Mediterranean. Lipkin (1975c, 1977, 1979) reported seven species of seagrasses growing on the sandy or muddy bottom in the Gulf of Suez and Sinai Red Sea. Besides H. stipulacea, he also found Halodule uninervis (Forsskål) Ascherson, Cymodocea rotundata Ehrenberg and Hemprich ex Ascherson, Syringodium isoetifolium (Ascherson) Dandy, Thalassodendron ciliatum (Forsskål) den Hartog, Thalassia hemprichii (Ehrenberg) Ascherson, and Halophila ovalis (R. Brown) J.D. Hooker. These tropical species are possible invaders to the Mediterranean through the Suez Canal due to

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global warming and the rise of seawater temperatures. About 40 years ago, Lipkin (1972a, b, 1977) already found H. uninervis growing associated with H. stipulacea on sandy and muddy bottoms (2–3 m deep) in the Great Bitter Lake, which is at the middle of the Suez Canal and about 60 km from its estuary to the Mediterranean Sea at Port Said and therefore it is quite possible that this species already reached the Mediterranean Sea, waiting to be discovered somewhere.

 hellfish Transfer and Alien Seaweed S Invasion: A Study Case from the Gulf of Lion Several studies conducted in the middle of the twentieth century caused Elton to make the surprising statement: “The greatest agency of all that spreads marine organisms to new quarters of the world must be the business of oyster cultures” (Elton 1958). This statement was strongly supported by recent studies concerning alien-seaweed species and the vectors that transport them into the Mediterranean Sea. Today, shellfish transfer is regarded as the most important vector for seaweed introduction into that sea (Maggs and Stegenga 1999; Verlaque 2001; Boudouresque and Verlaque 2010). Shellfish transfer introduced 46 % of alien macrophytes, while shipping and the Suez Canal introduced 29 and 27 %, respectively. These results (the sum, including other vectors, is more than 100 %) also indicate that some alien macrophytes have been introduced several times by different vectors (Zenetos et al. 2010). The Gulf of Lion is an excellent example of the ­contribution of shellfish aquaculture (oysters, clams, and mussels) to seaweed invasion. The Thau Lagoon (located at the Sète area on the France Mediterranean coast in the middle of the Gulf of Lion), which is the leading site of shellfish aquaculture in the Mediterranean Sea, is now also regarded as the main hotspot for alien seaweeds in the Mediterranean, with 58 alien seaweed species reported so far. These alien seaweeds, which mostly originated from the North Pacific Ocean, contributed 64 % west-Mediterranean alien seaweeds, and nearly 50 % of the total alien macrophytes of the Mediterranean (Verlaque et al. 2007; Zenetos et al. 2010; Boudouresque et al. 2011). According to Boudouresque et al. (2011), introduced seaweeds represent 32 % of the species diversity and 48–99 % of the seaweed biomass estimated on hard ­substrates at the Thau Lagoon. The Thau Lagoon is not suitable for breeding the Japanese oyster Crassostrea gigas (Thunberg) (also called the Portuguese oyster), which is the main crop of the shellfish industry in the area and, therefore, the local C. gigas farms are completely dependent on importing new oysters and their spats from other locations. These farms have official permission to import spats and small C. gigas individuals produced

in the Atlantic alone since 1977; however, oyster farmers imported billions of small C. gigas oysters since the 1970s at least through the 1990s from British Columbia, Japan and Korea located in the North Pacific Ocean (Boudouresque et al. 2011). These evidences strongly point at C. gigas transfer as a primer vector of introduction, carrying alien seaweeds from the North Pacific Ocean as mature thalli or propagules attached to its shells or packing materials and also as a ­secondary dispersal of alien seaweeds in the temperate Gulf of Lion and other Mediterranean locations, such as Mar Piccolo and the Venice Lagoon in Italy.

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There is no doubt that the surface-water temperatures have increased rapidly in the Mediterranean Sea during recent decades, probably due to the global-warming process; however, its effects on invasion is still doubtable. Generally, studies from around the world have indicated that there is a big connection between global warming and the spread of alien exotic species from tropical origins. Some studies proved that invasive species from warm origins have a superior capacity to tolerate increased temperatures compared to native species (Stachowicz et al. 2002; Ward and Masters 2007; Sorte et al. 2010). Most of the alien species in the Mediterranean (especially in the eastern basin) are thermophiles. These species originate in warm water (Zenetos et al. 2010). However, several algologists and seaweed ecologists claim that it is too early to detect any quantitative or qualitative impacts of global warming on seaweed introduction; moreover, they showed that some alien seaweeds reported that were regarded as tropical actually originated in temperate seas (Boudouresque and Verlaque 2010). Although global warming itself does not increase the number of species introduced into the Mediterranean Sea, it facilitates the settlement and establishment of alien species from tropical origins to warmer recipient marine ecosystems and, later, also facilitates their dispersal to nearby warm locations. High average sea-surface water temperatures in the eastern basin of the Mediterranean, especially along the shores of Egypt, the Levant, Cyprus, and Turkey, welcome the tropical seaweeds and help them spread in the region. On the other hand, the western Mediterranean, which is still more temperate (colder than the eastern Mediterranean basin) is more welcoming to seaweeds coming from the colder seas of Japan, China, Korea, and even from the temperate shores of Australia (Boudouresque and Verlaque 2010).

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 ow Should We Deal with the Alien Invasion H in the Mediterranean Sea? The best way to compete with the invasive-species phenomenon is through prevention, early detection, and rapid response (Williams and Grosholz 2008). The natural migrations of alien species through the Suez Canal and the Straits of Gibraltar are fait accompli. Closing these sea crossings, stopping marine transportation, or even eliminating shellfish transfer to the Mediterranean in order to stop the invasion and introduction of alien marine creatures, are definitely not realistic and are out of the question. However, certain international actions should be taken in order to reduce or slow down the rate of introductions and invasions. The first action that should be taken has educational value and is very important: to increase public awareness of the negative impacts of alien invasions (including invasion in the Mediterranean Sea) (ICES 2005). The public has the right to know the effects of aliens on the environment and the direct and indirect consequences and risks of massive invasions on us. These consequences and the possible ways to control them should be seriously discussed at schools and universities all around the Mediterranean, and the effect of marine and terrestrial invasions should be a main subject and an integral part of biology curricula. The second action is to accept the recommendations proposed by marine scientists and act accordingly in order to reduce the invasion problem. It is shameful and very serious that Mediterranean countries that ratified international scientific conventions dealing with the solutions to this problem have not yet drafted any text of law to legally implement these conventions (Boudouresque and Verlaque 2005, 2010). Governments must adopt and implement conventions such as those published by the Food and Agriculture Organization of the United Nations (FAO 1996), the International Union for Conservation of Nature (IUCN 2002) the International Council for the Exploration of the Sea (ICES 2005), and the International Maritime Organization (IMO) (Tamelander et al. 2010), which recommended policies and actions that should take place in order to reduce marine-species introduction and their negative impacts. An excellent example of such a recommendation that should be implemented is the ones concerned with the reduction of alien invasion (especially alien seaweeds) due to mariculture and shellfish transfer. Verlaque et al. (2007) note a plan with seven comprehensive guidelines modified from the IUCN (Shine et al. 2000) and ICES (2005) guidelines in order to prevent future invasion by shellfish transfer. These guidelines are: (1) to increase the awareness of farmers concerning the risks associated with uncontrolled importation; (2) aquaculture should be based on native or local

stock whenever possible. Import and transfer of livestock should be kept to a minimum, and the animals should be thoroughly inspected and quarantined for an appropriate observation period; (3) special attention should be paid during aquaculture trials with new exotic species (even with livestock from hatcheries); (4) non-native livestock to be introduced should be produced in hatcheries; (5) live products destined for consumption, processing, aquaria, or ­display should not be placed into the natural environment; (6) in the case of livestock transfers (including interregional ones), decontamination processes and/or quarantine, as proposed by the ICES, should be followed; and (7) efficient treatments (e.g., hot seawater for sterilization of oysters from epiphytes growing on its shell) to avoid introduction or secondary dispersal of exotic or native species should be carried out prior to each transfer, i.e., after the period of reimmersion preceding the transfer, and should be repeated upon arrival. These seven guidelines should be adopted by all Mediterranean countries that have aquaculture based on imported marine organisms (especially shellfish). Shipping has universally been regarded as the single largest vector for the movement of aquatic alien species (Galil 2006b). A new convention formulated by the IMO focuses on ballast-water management strategies and recommends some new standards and procedures in order to prevent alien invasion via shipping, namely cargo ships. This convention had published recommendations designed to prevent the spread of alien species from ballast water origins (Tamelander et al. 2010). IMO Regulation D-2, which deals with ballast-water performance standards, recommends that “Ships conducting ballast water management shall discharge less than 10 viable organisms per cubic meter greater than or equal to 50  μm in minimum dimension and less than 10 viable organisms per milliliter less than 50 μm in minimum dimension and greater than or equal to 10 μm in minimum dimension; and discharge of the indicator microbes shall not exceed the specified concentrations” (Tamelander et al. 2010). In order to provide a new product to implement Regulation D-2, Siemens Water Technologies has developed and launched a new SiCURE™ Ballast Water Management System that provides a reliable, environmentally sound solution designed to protect against the proliferation of aquatic invasive species. This filter system is based on three pillars: (1) filters to remove or break larger organisms using a 40 μm weave wire screen; (2) hypochlorination (with NaOCl) using a concentric-tube electrode in order to oxidize and eliminate marine organisms that passed through the filters; and (3) proprietary control logic of the ballast water management system monitors the chlorine dose level necessary to provide the required efficacy (SiCURE™ 2012). Such a solution should be fixed by law all across the Mediterranean and every cargo

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ship that carries ballast water should be required to use an appropriate filtration system to minimize the spread of marine alien species in the Mediterranean Sea and the oceans. In several regions, hull fouling is the dominant species-­ introduction vector and it is estimated that biofouling is responsible for the introduction of over two thirds of all non-­ native algal species globally. In 2001, the IMO set up the International Convention on the Control of Harmful Anti-­ fouling Systems on Ships (Anti-Fouling Convention) (Tamelander et al. 2010). This convention and the ones by ICES that followed during 2006, recommended emerging hull-fouling regulations and treatment options (ICES 2006), including seven guidelines with a general objective to minimize the number of unintentional species introductions associated with hull fouling: (1) to encourage the necessary research, development, and sharing of an adequate knowledge base to address the problems of hull-fouling mediated introductions of alien species in the Mediterranean; (2) to increase awareness of hull fouling as a major introduction vector; (3) to technically assist and advise the Mediterranean coastal states, if requested, to ratify the IMO AFS Convention; (4) to encourage the development and implementation of control efforts, such as hull cleaning measures; (5) to encourage the development of a framework for national legislation and regional cooperation to regulate the introduction of hull-­ fouling mediated species introductions, their eradication, and control; (6) to design a lead agency that would have a central responsibility within the government for coordinating the national response to the above issues; (7) to form a national task force to develop and implement the proposed guidelines. This national task force can be cross-sectoral and multidisciplinary (ICES 2006). Other strategies on a national level published by the ICES were: (1) routine vessel monitoring to document the risk of species invasions in hull fouling; (2) identification of vessels that likely carry high-risk species in their hull fouling (risk assessment); (3) identification of ports that receive a large number of ‘critical’ vessels; (4) evaluation of hull treatment methods for ‘critical’ vessels; (5) make all dockyard and scrapyard operators aware that organisms removed from ship hulls should be collected and discharged safely on land; (6) strongly encourage marina operators to apply the proposed guidelines (ICES 2006). Meetings such as the ICES Working Group on Introduction and Transfers of Marine Organisms (WGITMO), taking place in March 2012 in Lisbon, accompanied by International Oceanographic Commission (IOC) and IMO, and dealing with the progress achieved using new technologies and treatments against the alien invasion from ballast water and other ship-vector origins, are very important and encouraging, and it is expected that new regulations on these subjects will be published soon (ICES 2012).

The third action is to start a new global Mediterranean monitoring program focussing on the Suez Canal and the Strait of Gibraltar, in order to detect the new aliens that arrive naturally, and also focusing on some hotspot areas such as some of the North African shores, the LevantineBasin coasts, harbors, and estuarine areas, which were not well studied so far. Monitoring the Suez Canal and its estuary near Port Said in order to detect and even prevent alien invasion to the Mediterranean is a very difficult and expensive mission that requires huge unending international efforts. A set of filters should be established through the canal in order to detect the new species that pass through it and reduce the infiltration of these alien species into the Mediterranean Sea.

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Acknowledgments  I would like to thank Sharon Victor from the Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, for editing this chapter.

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R. Hoffman 1183 1184 1185 1186 1187 1188 1189 1190 1191 1192 1193 1194 1195 1196 1197 1198 1199 1200 1201 1202 1203 1204 1205 1206 1207 1208 1209 1210 1211 1212 1213 1214 1215 1216 1217 1218 1219 1220 1221 1222 1223 1224 1225 1226 1227 1228 1229 1230 1231 1232 1233 1234 1235 1236 1237 1238 1239 1240 1241 1242 1243 1244 1245 1246 1247 1248

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Williamson M (1996) Biological invasions. Chapman and Hall, London Wynne MJ (2005) A check-list of benthic marine algae of the tropical and subtropical western Atlantic: second revision. Beihefte zur Nova Hedwigia 129:1–152 Zenetos A, Çinar ME, Pancucci-Papadopoulou MA, Harmelin JG, Furnari G, Andaloro F, Bellou N, Streftaris N, Zibrowius H (2005) Annotated list of marine alien species in the Mediterranean with records of the worst invasive species. Mediterr Mar Sci 6:63–118 Zenetos A, Meriç E, Verlaque M, Galli P, Boudouresque CF, Giangrande A, Çınar ME, Bilecenoglu M (2008) Additions to the annotated list of marine alien biota in the Mediterranean with special emphasis on Foraminifera and parasites. Mediterr Mar Sci 9:119–165 Zenetos A, Gofas S, Verlaque M, Cinar M, Garcia Raso J, Bianchi C, Morri C, Azzurro E, Bilecenoglu M, Froglia C, Siokou I, Violanti D, Sfriso A, San Martin G, Giangrande A, Katagan T, Ballesteros E, Ramos-Esplà A, Mastrototaro F, Ocana O, Zingone A, Gambi M, Streftaris N (2010) Alien species in the Mediterranean Sea. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution. Mediterr Mar Sci 11:381–493 Zenetos A, Katsanevakis S, Poursanidis D, Crocetta F, Damalas D, Apostolopoulos G, Gravili C, Vardala-Theodorou E, Malaquias M (2011) Marine alien species in Greek seas: additions and amendments by 2010. Mediterr Mar Sci 12:95–120

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Author Queries Chapter No.: 10

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AU1

Please check if the superscripted numbers in Table 10.1 should be reordered as they are not in the sequential order.

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AU3

Hoffman et al. (submitted), Verlaque (in press) are cited in text but not provided in the reference list. Please check.

AU4

Please provide citation for Verlaque (2011).

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