Introduced marine species of the North Sea coasts

(1)

HELGOL.~NDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters. 52, 219-234 {1999)

Introduced marine species of the North Sea coasts

K. R e i s e 1, S. G o l l a s c h 2 & W.J. W o l f f 3

i Alfred-Wegener-Institut f~r Polar- und Meeresforschung, Wattenmeerstation Sylt; D - 2 5 9 9 2 List, G e r m a n y

2 Institut f~ir M e e r e s k u n d e , D~Jsternbrooker W e g 20, D-24105 Kiel, G e r m a n y 9

~ Rijksuniversiteit Groningen, Mariene Biologie, Postbus 14, NL-9750 A A Haren, The Netherlands

ABSTRACT: About 80 non-indigenous species are a s s u m e d to have b e e n introduced into the North Sea by transoceanic shipping and aquaculture. The n u m b e r is certainly u n d e r e s t i m a t e d as most small organisms received insufficient attention at the species level. Also, the seafaring tradition of the North Sea countries is much longer than our biological surveys are. Most exotic invertebrates originate from the w e s t e r n Atlantic and were introduced by shipping, while most algae stem from the Pacific and c a m e with the introduced oysters. A peak of n e w c o m e r s was observed in the 1970s.

Most of the arrivals b e c a m e established in brackish environments, at harbor sites and in the vicinity of oyster farms, fouling on hard substrates or living as epibionts. A few live in sediments, are holoplanktonic or are parasites. At the open coast, approximately 6% of the macrobenthic species are exotics, while in estuaries their share is up to 20%. Most exotics have b e e n e n c o u n t e r e d in the southern North Sea first, and many did not s p r e a d further north. About 25% of the established non-natives are w i d e s p r e a d and attain locally high a b u n d a n c e s . As a consequence, some inshore habitats are entirely dominated by exotics. The overall effect on the ecosystem s e e m s to be more additive than one of displacement. This s u g g e s t s that the coastal biota of the North Sea are quite capable of a c c o m m o d a t i n g newcomers. However, this is no g u a r a n t e e that the next introduced species may not cause severe ecological c h a n g e or economic harm. There is a n e e d to minimize the risk of unintentional introductions by ballast water treatment and by adhering to quarantine pro- c e d u r e s in aquaculture. Current research on exotics in the North Sea is regarded as i n a d e q u a t e for proper evaluation and m a n a g e m e n t requirements.

I N T R O D U C T I O N

M a r i t i m e traffic a c r o s s t h e o c e a n s a n d c u l t u r i n g of n o n m a t i v e o r g a n i s m s at t h e e d g e of t h e s e a c o n t r i b u t e d to t h e s p r e a d a n d e s t a b l i s h m e n t of a n e v e r i n c r e a s i n g n u m b e r of e x o t i c s p e c i e s in c o a s t a l a n d b r a c k i s h w a t e r e n v i r o n m e n t s . E x o t i c s p e c i e s of t h e N o r t h S e a a r e h e r e o p e r a t i o n a l l y d e f i n e d a s s p e c i e s o c c u r r i n g o n l y o u t s i d e t h e r e g i o n of t h e A t l a n - tic c o a s t of E u r o p e ( G i b r a l t a r to N o r t h C a p e ) ; h e n c e M e d i t e r r a n e a n a n d P o n t o - C a s p i a n s p e c i e s a r e c o n s i d e r e d as e x o t i c s . W e f u r t h e r r e s t r i c t t h i s o v e r v i e w to s p e c i e s w h i c h h a v e p r e s u m a b l y a r r i v e d b y m e a n s of h u m a n t r a n s p o r t , b o t h i n t e n t i o n a l as w e l l a s u n i n t e n - t i o n a l i n t r o d u c t i o n s . B o u n d a r i e s of t h e N o r t h S e a a r e d e f i n e d a c c o r d i n g to t h e N o r t h S e a T a s k F o r c e (1993), w h i c h i n c l u d e s t h e C h a n n e l r e g i o n i n t h e s o u t h , t h e S k a g e r r a k a n d K a t t e g a t in t h e e a s t , a n d t h e S h e t l a n d I s l a n d s i n t h e n o r t h . S p e c i e s of b r a c k i s h h a b i t a t s h a v e b e e n i n c l u d e d w h e n a s a l i n i t y of > 5 p s u is r e g u l a r l y e n c o u n t e r e d a t t h e s i t e s . 9 Biologische Anstalt Helgoland, H a m b u r g

(2)

220 K. Reise, S. Gollasch & W. J. Wolff

To r e g a r d a n exotic species as b e i n g e s t a b l i s h e d in the North Sea, there m u s t be ev- i d e n c e of c o n t i n u e d p r o p a g a t i o n by more t h a n one g e n e r a t i o n . In practice, w h e n de- v e l o p i n g offspring have b e e n o b s e r v e d in more t h a n o n e s e a s o n or w h e n t h e p r e s e n c e of a species clearly exceeds the e x p e c t e d lifetime of a n individual, we h a v e c o n s i d e r e d this as sufficient e v i d e n c e of successful e s t a b l i s h m e n t .

M a n y of those coastal species which the coastal North Sea has in c o m m o n with the M e d i t e r r a n e a n Sea, the w e s t e r n Atlantic, the n o r t h e r n Pacific or e v e n t h e s o u t h e r n h e m i s p h e r e m a y h a v e crossed the n a t u r a l barriers of dispersal with the aid of o c e a n - g o - ing vessels or with transports of c o m m e r c i a l fishery products. This p r o b a b l y com- m e n c e d early on with the M e d i t e r r a n e a n region. T h e first e x p e d i t i o n s of t h e Vikings a n d the Basques to North A m e r i c a n shores date b a c k to a b o u t A. D. 1000, a n d for four c e n t u r i e s the North Sea has b e e n c o n n e c t e d with almost all coasts of the g l o b e by ex- t e n s i v e seafaring. Thus, there is a rich s u p p l y of exotic species.

Ships r e p r e s e n t floating biological islands, g i v i n g rise to a spring tide of p o t e n t i a l i n v a d e r s at the coast w h e r e they arrive (Carlton, 1985, 1989; Carlton & Geller, 1993).

W o o d e n ships h a v e invited boring o r g a n i s m s such as the shipworm Teredo navalis a n d the g r i b b l e Limnoria spp., foulers a t t a c h e d to the ships' hull, a n d ballast s a n d or rock were often carried from coast to coast, a n d a d h e r i n g o r g a n i s m s had a fair c h a n c e to get abroad. Since the i n t r o d u c t i o n of s t e e l - h u l l e d vessels in the 1870s, ballast w a t e r dis- c h a r g e s h a v e i n c r e a s e d considerably. T h e probability of e s t a b l i s h i n g s e l f - s u s t a i n i n g p o p u l a t i o n s of n o n - i n d i g e n o u s species i n c r e a s e d with g r e a t e r v o l u m e s of b a l l a s t water in larger a n d faster vessels. A recent s t u d y of North Sea a n d Baltic ports on ships as in- t r o d u c i n g vectors of exotic species r e v e a l e d 404 species in samples from ballast water, s e d i m e n t in the tanks a n d ship hulls, r a n g i n g from u n i c e l l u l a r algae to 15-cm-long fishes. A b o u t 60% of these species are n o n - i n d i g e n o u s to the North Sea a n d the Baltic (Gollasch, 1996; Lenz et al., in preperation).

Large-scale transfers of oysters b e t w e e n distant coasts c o m m e n c e d as e a r l y as the m i d d l e of the n i n e t e e n t h c e n t u r y (Mbbius, 1877; Korringa, 1976 a, b). T h e s e s h i p m e n t s often comprised entire oyster b e d c o m m u n i t i e s . Since the 1970s, more a n d m o r e oyster t r a n s p l a n t s originate from e n c l o s e d hatcheries (Chew, 1990), a n d this m i g h t e v e n t u a l l y close this major g a t e w a y of m a r i n e introductions. I n t e r n a t i o n a l trade i n seafood still forms a risk, however.

Introductions of exotic species have occasionally resulted in striking c h a n g e s , e.g. the West-Atlantic c t e n o p h o r e M n e m i o p s i s leidyi into the Black Sea w h e r e it tilted the re- gional a n c h o v y fishery (Travis, 1993); the tropical g r e e n algae Caulerpa taxifolia into the M e d i t e r r a n e a n w h e r e it is rapidly o v e r g r o w i n g seagrass beds (de Vill~le & Verlaque, 1995; Ceccherelli & Cinelli, 1997); the A s i a n b i v a l v e Potamocorbula a m u r e n s i s into S a n Francisco Bay w h e r e it c h a n g e d the e n t i r e food w e b structure (Carlton et al., 1990;

Nichols et al., 1990; Kimmerer et al., 1994); the North Sea crab Carcinus m a e n a s s h o w i n g g i g a n t i s m a n d strong p r e d a t o r y effects at the coast of California a n d T a s m a n i a (Gros- holz & Ruiz, 1995; Hewitt, p e r s o n a l c o m m u n i c a t i o n ) ; the East-Atlantic p e r i w i n k l e Litto- rina littorea c a u s i n g cascades of ecological c h a n g e s in the recipient West-Atlantic coastal biota (Brenchley & Carlton, 1983; Bertness, 1984), a n d finally various i n t r o d u c e d diseases of oysters a n d fish (Lauckner, 1983; K i n n e , 1984) as well as toxic a l g a e in the p l a n k t o n (Anderson, 1994) have c a u s e d trouble a n d c o n c e r n in different places a r o u n d the world.

(3)

I n t r o d u c e d m a r i n e species of the North Sea coasts 221

T h e various coasts differ in the n u m b e r of exotics they have received, in the n u m - b e r of exotics which h a v e b e c o m e established, a n d in the effects of the exotics on the n a t i v e biota (Ruiz et al., 1997). We here a t t e m p t a brief overview of i n t r o d u c e d species into the North Sea. More e x t e n s i v e reviews c o v e r i n g in part the North Sea r e g i o n are g i v e n by Eno et aL (1997), J a n s s o n (1994) a n d N e h r i n g & Leuchs (1999). We here particularly ask the questions: How m a n y b e c a m e established, w h e r e did they come from a n d at what time were they discovered, b y w h a t m e a n s did they arrive, a n d w h e r e a n d how did they fit into the habitats of the n a t i v e biota? Finally, what is the overall effect a n d what should be d o n e a b o u t it?

H O W MANY EXOTICS IN THE NORTH SEA?

T h e n u m b e r of n o n - i n d i g e n o u s taxa a s s u m e d to h a v e b e e n e s t a b l i s h e d in the North Sea a m o u n t s to a b o u t 80 species (Table 1). This total n u m b e r is lower t h a n w h a t has b e e n recorded from some e s t u a r i n e r e g i o n s in North America, i.e., 116 in C h e s a p e a k e Bay, 137 in the Great Lakes a n d 212 in S a n Francisco Bay (reviewed in Ruiz et al., 1997), but these s t u d i e s i n c l u d e d o r g a n i s m s from f r e s h w a t e r as well as terrestrial shores a n d w e t l a n d s to a variable extent, while ours is c o n f i n e d to m a r i n e a n d brackish w a t e r organisms. T h e majority of exotics in the North Sea are i n v e r t e b r a t e s (47), primarily crus- taceans, molluscs, p o l y c h a e t e s a n d hydroids (Table 2). I n t r o d u c e d m a c r o a l g a e comprise 20 taxa, mostly red a n d b r o w n ones. O n l y 12 species of protists are a m o n g the a s s u m e d exotics of the North Sea.

Of the 80 species listed in Table 1, 22 occur p r e f e r e n t i a l l y in brackish e n v i r o n m e n t s . 'Hotspots' of i n t r o d u c e d species are h a r b o r sites a n d in the vicinity of oyster farms, w h e r e they grow or climb on the artificially p r o v i d e d hard substrates. At least 26 species b e l o n g to this category. Only a b o u t t e n of these have diffused onto the rocky shores of the o p e n coast. A f r e q u e n t m o d e of life is as epibionts, mostly on molluscs a n d a l g a e (27 species). Six i n t r o d u c e d species are parasites. Of the exotic species s e v e n t e e n dwell in or on coastal m u d a n d sand. O n l y t e n h o l o p l a n k t o n i c species have b e e n recognized as exotics. However, in this group a distinction b e t w e e n introduction a n d n a t u r a l drift by o c e a n i c currents is often impossible.

T h e snail Corambe (obscura) batava, o n c e locally established, has g o n e a g a i n be- cause the h a b i t a t has b e e n altered by coastal e n g i n e e r i n g . Almost all i n t r o d u c t i o n s occurred accidentally. Also, the marsh grass Spartina anglica a n d the a m p h i p o d Gam- marus tigrinus originate from a c c i d e n t a l i n t r o d u c t i o n s b u t were further d i s t r i b u t e d de- liberately in the North Sea region. T h e bivalves Mercenaria mercenaria, races of Ostrea edufis, Crassostrea gigas, C. angulata a n d C. virginica w e r e d e l i b e r a t e l y i n t r o d u c e d , b u t the latter two did not establish r e p r o d u c i n g p o p u l a t i o n s (Hedgpeth, 1980; Eno et al., 1997). This is different to the situation in the a d j a c e n t freshwater habitats of central a n d w e s t e r n Europe. Similar to the North Sea, a b o u t 80 species have b e e n i n t r o d u c e d a n d b e c a m e established, but n e a r l y half of t h e s e w e r e i n t e n d e d introductions, particularly fish (Kinzelbach, 1995).

T h e s h a r e of exotics in the North Sea biota i n c r e a s e s from the offshore part towards the coast, a n d there it increases further from the o p e n coast towards the estuaries. In the latter, the p e r c e n t a g e of exotic species is a b o u t 20 (Wolff, 1999). In the waters a r o u n d

(4)

2 2 2 K. R e i s e , S. G o l l a s c h & W. J. W o l f f

T a b l e 1. N o n - n a t i v e s p e c i e s e s t a b l i s h e d in t h e N o r t h S e a i n c l u d i n g t h e C h a n n e l a n d K a t t e g a t re- g i o n s . O r i g i n : e a s t e r n A t l a n t i c o u t s i d e N o r t h S e a (EA), w e s t e r n A t l a n t i c (WA), s o u t h e r n A t l a n t i c (SA), n o r t h e r n Pacific (NP), s o u t h e r n Pacific (SP), I n d o - P a c i f i c (IP); + no l o n g e r p r e s e n t b e c a u s e h a b i t a t h a s c h a n g e d ; t r a n s p o r t k n o w n or a s s u m e d to h a v e o c c u r r e d with a q u a c u l t u r e (A) or s h i p s (S); s t a t u s : o c c u r r i n g a l o n g m o s t of t h e c o a s t s (+++), in part of t h e a r e a (++), at o n e or a f e w locali- ties (+), p r i m a r i l y in f r e s h w a t e r b u t e x t e n d i n g into b r a c k i s h e s t u a r i e s a n d l a g o o n s (b); ? s p e c i e s of u n c e r t a i n t a x o n o m i c s t a t u s or w h i c h m a y h a v e a r r i v e d also b y n a t u r a l m e a n s . R e f e r e n c e s a r e lim- i t e d to o n e or two s o u r c e s w h e r e f u r t h e r i n f o r m a t i o n m a y b e o b t a i n e d : 1 C h a p m a n , 1999; 2 El- brfichter, 1999; 3 E n o et al., 1997; 4 E s s i n k , 1999; 5 F l e t c h e r & Farrell, 1999; 6 H a y w a r d & R y l a n d , 1990; 7 L a u c k n e r , 1983; 8 M a g g s & S t e g e n g a , 1999; 9 N e h r i n g , 1998; 10 Stock, t 9 9 3 ; 1I Thiel,

1968; 12 Wolff, 1999; 13 Z i b r o w i u s & T h o r p , 1989; 14 G o l l a s c h & R i e m a n n - Z f i r n e c k , 1996

T a x o n O r i g i n First T r a n s - S t a t u s Ref.

r e c o r d port D i n o p h y c e a e ( d i n o f l a g e l l a t e s )

? G y m n o d i n i u m mikimotoi N P M i y a k e & K o m i n a m i (syn. G. aureolum, G. nagasakiensis)

A l e x a n d r i u m leeii B a l e c h NP

Raphidophyceae

Fibrocapsa japonica T o r i u m i & T a k a n o NP

Chattonella sp. N P

B a c i l l a r i o p h y c e a e (diatoms)

Odontella (Biddulphia) sinensis (Greville) NP Thulussiosira punctigera Castr. N P Thalassiosira tealata T a k a n o N P

? Thalassiosira h e n d e y i H a s l e & Fryxelt SA Coscinodiscus wailesii G r a n & A n g s t NP

Phaeophyceae ( b r o w n a l g a e )

Sargassum m u t i c u m F e n s h o l t N P Undaria pinnatifida S u r i n g e r N P

? Fucus e v a n e s c e n s C . A g . N P Colpomenia peregrina H a m e l IP Corynophlaea umbellata Ktitzing N P

Rhodophyceae (red a l g a e )

Bonnernaisonia hamifera Harlot NP Asparagopsis armata H a r v e y SP Grateloupia doryphora H o w e N P Grateloupia luxurians G e p p IP

? Agardiella subulata Kraft & W y n n e ? A n t i t h a m n i o n e l l a ternifolia Lyle SP A n t i t h a m n i o n e l l a spirographidis S c h i f f n e r N P Dasya baillouviana M o n t a g n e W A ?

? Dasysiphonia sp. NP

A n o t r i c h i u m furcellaturn B a l d o c k N P Polysiphonia senticulosa H a r v e y N P

Polysiphonia harveyi Bailey NP

Chlorophyceae ( g r e e n a l g a e )

Codium fragile ssp. atlanticum Silva N P Codium fragile ssp. tomentosoides Silva N P Codium fragile ssp. scandinavicum Silva N P

1966 +++ 2,9

1995 + 2

1991 ++ 2,9

1903 S +++ 3,9

1978 A/S +++ 3,9

1950 A/S ++ 3,9

1978 S ++ 3,9

1977 A/S +++ 3,9

1960s A +++ 3,5

1986 A/S ++ 3,5

1902 + 5

1905 A § 3,5

1990 A + 5

1890 A +++ 3,8

1950 A + 3,8

1969 A + 3,8

1947 A ++ 3,8

1973 A + 3,8

1926 S ++ 3,8

1906 S ++ 3,8

1950 A +++ 8

1994 A + 8

1976 + 8

1993 A + 8

1908 A ++§ 3,8

1839 A ++ 1,3

1900 A / S +++ 1,3

1919 A/S ++ 1

(5)

I n t r o d u c e d m a r i n e s p e c i e s of t h e N o r t h S e a c o a s t s 223 Table 1 (continued)

T a x o n Origin First Trans- S t a t u s Ref.

record port

Poaceae ( g r a s s e s )

Spartina anglica H u b b a r d 1890s S +++ 3

Ascetospora (parasitic p r o t o z o a n s )

Bonamia ostreae Pichot et al. WA 1982 A + 7

Marteilia refringens Grizet et al. EA 1970s A + 7

Haplosporidium armoricanum EA 1970s A + 7

(van B a n n i n g ) Hydrozoa (hydroids)

Cordylaphora caspia (Pallas) P o n t o - C a s p . 1884 S b 12

G o n i o n e m u s vertens Agassiz NP 1913 A/S + 3

(syn. murbachi Mayer)

Garveia (Bimeria) franciscana Torrey ? 1920 S + 12

Clavopsella navis (Millard) ? 1973 S + 3

N e m o p s i s bachei A g a s s i z WA 1905 S + 11

Anthozoa (sea a n e m o n e s )

Nematostella vectensis S t e p h e n s o n WA 1935 + 6

Haliplanella lineata (Verrill) NP 1896 S ++ 3,12

(incl. H. luciae Verrill)

Diadumene cincta ( S t e p h e n s o n ) ?NP 1925 A/S ++ 9,14 Bivalvia ( l a m e l l i b r a n c h s )

Crassostrea gigas ( T h u n b e r g ) NP 1964 A ++ 3

(incl. C. angulata)

Ensis americanus (Binney) WA 1978 S +++ 3

(syn. directus C o n r a d )

Mytilopsis (Congeria) leucophaeta (Conrad) EA 1835 S b 12

M y a arenaria (L.) WA 1250? +++ 3

Mercenaria mercenaria (L.) WA 1864 A + 3,12

Petricola pholadiformis L a m a r c k WA 1890 A +++ 3

Teredo navalis L. IP < 1800 S +++ 12

Gastropoda (snails)

Corambe (obscura) batava K e r b e n t WA 1886 § + 12

Crepidula [ornicata (L.) WA 1887 A +++ 3

Urosalpinx cinerea (Say) WA 1900 A + 3

Potamopyrgus antipodarum (Gray) SP 1883 S b 3,12

(syn. ]enkinsi) Polychaeta

Clymenella torquata (Leidy) WA 1936 A + 3

Marenzelleria cf. viridis (Verrill) WA 1996 S + 4

Marenzelleria cf. wireni A u g e n e r WA 1982 S ++ 4

Janua brasiliensis (Grube) WA 1974 S + 3,13

Pileolaria b e r k e l e y a n a (Rioja) NP 1974 S ++ 3,13 (syn. rosepigmentata)

Ficopomatus (Mercierella) enigmaticus SP 1921 S ++ 12,13

(Fauvel)

Hydroides dianthus (Verrill) WA 1970 A/S + 3,13

Hydroides ezoensis O k u d a NP 1976 A/S + 3,13

Hydroides e l e g a n s (Haswell) ? 1937 S + 12,13

h y b r i d : W A / E A

(6)

224 K. R e i s e , S. G o l l a s c h & W. J. W o l f f

Table 1 (continued)

Taxon Origin First Trans- S t a t u s Ref.

record port

C r u s t a c e a

Balanus amphitrite D a r w i n IP Balanus improvisus D a r w i n WA Balanus e b u r n e u s Gould WA Elminius m o d e s t u s D a r w i n SP

Eriocheir sinensis Milne-Edw. NP

Brachynotus s e x d e n t a t u s (Risso) EA Rhithropanopeus harrisii IGould) WA Callinectes sapidus R a t h b u n WA Caprella m a c h o Platvoet et al. ? Corophium sextonae C r a w f o r d SP Eusarsiella (Sarsiella) zostericola ( C u s h m a n ) WA

Acartia tonsa D a n a WA,IP

Mytilicola orientalis Mori NP

Mytilicola ostreae H o s h i n a & S u g m r a NP P y c n o g o n i d a (sea spiders)

A m m o t h e a hilgendorfi (B6hm) NP B r y o z o a

Bugula neritina (L.) WA

? Victoriellu puvidu Saville Kent ? N e m a t o d a (here: s w i m - b l a d d e r n e m a t o d e ) Anguillicola crassus K u w a h a r a et al. NP A s c i d i a c e a (sea squirts)

Styela clara H e r d m a n NP

1937 S + 3,12

1850 S ++ 12

1900 S + 12

1943 S +++ 3,12

1912 S +§ 3,12

? S + 6

1870s S b 3,12

1932 S + 12

1995 + 12

1930s +++ 3

1940 A + 3

1916 S +++ 3

1992 A + 10

1978 S + 3

1973 S + 6

1870 S b 6

1982 A +++ 3

1952 S +++ 3

Table 2. N u m b e r of i n t r o d u c e d s p e c i e s w h i c h b e c a m e e s t a b l i s h e d in the North Sea, a n d their as- s u m e d origin a n d m o d e of t r a n s p o r t . W h e r e t w o a l t e r n a t i v e s are a s s u m e d to be e q u a l l y alike, a

s p e c i e s is c o u n t e d twice; if u n k n o w n no e n t r y is m a d e

Major N u m b e r Origin I m p o r t e d by

g r o u p of s p e c i e s Atlantic Pacific s h i p a q u a c u l t u r e

P h y t o p l a n k t o n 9 1 8 5 3

M a c r o a l g a e 20 1 18 5 16

P o a c e a e 1 1 - I -

Protozoa 3 3 - - 3

C n i d a r i a 8 2 3 7 2

Mollusca 11 8 3 4 5

A n n e l i d a 9 5 3 8 3

C r u s t a c e a 14 7 7 9 3

O t h e r i n v e r t e b r a t e s 5 1 3 4 1

(7)

the i s l a n d of Sylt, which are not e s t u a r i n e , the m a c r o b e n t h o s of a p p r o x i m a t e l y 300 species i n c l u d e s 20 exotics (Reise & Lackschewitz, 1998, u n p u b l i s h e d data). A share of r o u g h l y 6% is also e s t i m a t e d for the D u t c h coast (Wolff, 1999). [n offshore areas, only a few exotic species occur in the p l a n k t o n . A n e x p l a n a t i o n for this p a t t e r n is to b e f o u n d in the availability of vectors. M a r i c u l t u r e a n d ships transport m a i n l y o r g a n i s m s from coast to coast.

A l t h o u g h we were rather restrictive, the list of e s t a b l i s h e d exotics in Table 1 m a y e r r o n e o u s l y i n c l u d e some n a t i v e species, w h i c h were discovered late b u t m a y have b e e n a r o u n d l o n g before without b e i n g noticed. As a n example, Z i b r o w i u s & Thorp (1989) m e n t i o n three species of serpulids recorded from some harbors i n s o u t h e r n 5 n g - l a n d not before the 1980s, in spite of a n e s t a b l i s h e d tradition of s t u d y i n g t u b e w o r m s in this region. Initially there was some s u s p i c i o n that these m a y b e exotics: however, their wide b u t cryptic occurrence e l s e w h e r e i n the e a s t e r n Atlantic s u g g e s t s that these n a t i v e s were previously overlooked. Nevertheless, the n u m b e r of u n r e c o g n i z e d exotics in the North Sea is likely to e x c e e d by far the m i s t a k e n natives, a n d this is for several reasons:

1. Small o r g a n i s m s h a v e b e e n poorly studied. Approximately 80% of i n d i g e n o u s species in the North Sea is of microscopic size (2 mm), while only 20% of the listed exotics b e l o n g s to this category. This d i s c r e p a n c y m a y in part be e x p l a i n e d by a h i g h e r share of cosmopolitans a m o n g small o r g a n i s m s (Fenchel, 1993). O n the other hand, the c h a n c e of passive t r a n s p o r t with ships or oyster cultures is certainly in- creased with a d e c r e a s i n g i n d i v i d u a l size. Furthermore, as our a t t e n t i o n a n d taxo- n o m i c expertise g e n e r a l l y d e c r e a s e with the s m a l l n e s s of the organisms, we b e l i e v e the u n d e r r e p r e s e n t a t i o n of u n i c e l l u l a r algae, protozoans a n d small m e t a z o a n s a m o n g the exotics to be m a i n l y a n artifact.

2. M a n y introductions of exotic species certainly occurred long before they w e r e taxo- n o m i c a l l y recognized. Our list of exotics comprises only two species Ithe bivalves NIya arenaria a n d Teredo navalis) for w h i c h the date of introduction is a s s u m e d to b e before 1800. Also, in some other species, the first introduction was p r o b a b l y before 1800. For example, the n u d i b r a n c h Corarnbe (obscura) batava a n d the crab Rhithropanopeus harrisii were d e s c r i b e d as n e w species from the former Z u i d e r z e e a r o u n d 1880, i.e., d u r i n g the p e r i o d w h e n Dutch biologists first t u r n e d their a t t e n t i o n to the coastal f a u n a of the Z u i d e r z e e . However, at that time Dutch vessels h a d b e e n sailing b e t w e e n A m s t e r d a m (which u s e d to be a Zuiderzee port) a n d N i e u w Ams- t e r d a m (= N e w York n o w a d a y s ) a n d other A m e r i c a n ports for n e a r l y three centuries.

Thus, the actual dates of i n t r o d u c t i o n m a y well b e long before the 1880s w h e n these two i n c o n s p i c u o u s species w e r e first discovered. T h e long d u r a t i o n of former voy- ages across the sea m a y h a v e c o n t r i b u t e d to low survival rates of t r a n s p o r t e d o r g a n - isms. However, in times of w o o d e n s a i l i n g vessels, ships had less effective antifoul- i n g strategies, a n d their ballast often i n c l u d e d e s t u a r i n e a n d m a r i n e s e d i m e n t s , a n ideal m e d i u m for b e n t h o s to travel across the o c e a n (Gerlach, 1977).

3. Taxa that c a n n o t reliably b e a s s i g n e d to n o n - n a t i v e introductions h a v e b e e n t e r m e d ' c r y p t o g e n i c species' by C a r l t o n (1996), a n d only some are i n c l u d e d in Table 1 ( m a r k e d with a q u e s t i o n m a r k ) . A n e x a m p l e m a y illustrate such a case. T h e l a r g e

(8)

226 K. Reise, S. G o l l a s c h & W. J. Wolff

s a n d w o r m or k i n g r a g N e r e i s virens was first d e s c r i b e d by Sars in 1835 from B e r g e n in Norway. N o w a d a y s this is a v e r y c o n s p i c u o u s a n d c o m m o n p o l y c h a e t e in the North Sea. If its distribution a n d a b u n d a n c e h a d b e e n the s a m e in the e i g h t e e n t h c e n t u r y at the t i m e of Carl Linne, almost c e r t a i n l y he w o u l d not h a v e m i s s e d n a m i n g this obvious w o r m . Instead, it was not r e c o r d e d from the North S e a p r o p e r prior to 1900. H a g m e i e r (1925) m e n t i o n e d an i n c r e a s i n g a b u n d a n c e in the last d e c a d e s of his time, a n d R a s m u s s e n (1973) n o t e d an i n v a s i o n in a Danish fjord in the 1940s. As N.

virens s e e m s to be an e v e n m o r e p r o m i n e n t c o m p o n e n t of the coastal f a u n a on the o t h e r side of the Atlantic, it m a y h a v e b e e n i n t r o d u c e d from t h e r e to n o r t h e r n Eu- rope. N e v e r t h e l e s s , w e still c o n s i d e r the e v i d e n c e too w e a k to i n c l u d e N. v i r e n s in Table 1, b e c a u s e t h e r e m a y h a v e b e e n a natural s p r e a d s o u t h w a r d from arctic w a - ters. A g e n e t i c analysis of s p e c i e s with a m p h i - A t l a n t i c distribution m a y p e r h a p s cast s o m e light on s u c h c r y p t o g e n i c s .

In conclusion, the n u m b e r of a b o u t 80 exotic s p e c i e s e s t a b l i s h e d in the North Sea is certainly an u n d e r e s t i m a t e , and a n y ratio of exotic v e r s u s n a t i v e species n u m b e r s m u s t be restricted to m a c r o o r g a n i s m s only. In c o m p a r i s o n to shores of o t h e r continents, it should b e c o n s i d e r e d that the North S e a countries had a s e a f a r i n g tradition long b e f o r e natu- ralists b e g a n to t a k e their records.

O R I G I N S A N D ARRIVAL OF E X O T I C S

In terms of h o m o c l i m a t i c conditions, d i s t a n c e a n d f r e q u e n c y of s e a f a r i n g , o n e w o u l d e x p e c t a c l e a r d o m i n a n c e of exotics e m a n a t i n g from the other side of the At- lantic. Indeed, in the i n v e r t e b r a t e s m o r e exotics o r i g i n a t e from the other s i d e of the At- lantic than from Pacific regions, particularly in molluscs a n d p o l y c h a e t e s (Table 2).

H o w e v e r , p h y t o p l a n k t o n i c a n d m a c r o a l g a l exotics are almost all of Pacific origin. Be- sides the possibility that all p o t e n t i a l s p e c i e s had b e e n i n t r o d u c e d long b e f o r e our biological studies c o m m e n c e d , this d i f f e r e n c e b e t w e e n plants and animals m a y h a v e two causes. T h e m a c r o a l g a e of the cold a n d w a r m t e m p e r a t e coasts are m u c h p o o r e r in en- d e m i c s in the w e s t e r n than the e a s t e r n Atlantic (L~ining, 1990). Thus, t h e r e a r e not m a n y n e w s p e c i e s to b e r e c e i v e d from A m e r i c a . T h e North Pacific region, on the o t h e r h a n d , is very rich in e n d e m i c a l g a l species, a n d the s u b s t a n t i a l imports of Pacific oysters (Chew, 1990) p r o v i d e d a suitable v e c t o r for a t t a c h e d a l g a e a n d their spores, a n d occasionally a l g a e are u s e d as p a c k i n g m a t e r i a l for live oyster shipping. Transports c a m e ei- t h e r directly from the w e s t e r n Pacific or from cultures in the e a s t e r n Pacific. T h e a l g a e usually a p p e a r e d first a r o u n d F r e n c h oyster farms, a n d from t h e r e most s p r e a d by their o w n m e a n s into t h e N o r t h Sea ( M a g g s & S t e g e n g a , 1999).

A l t h o u g h s o m e i n v e r t e b r a t e s c a m e by the s a m e route, most t r a v e l l e d by ship (Table 2), e i t h e r as l a r v a e in ballast tanks or as adults a t t a c h e d to hulls. In t h e s e cases, the s h o r t e r d i s t a n c e a n d h i g h e r f r e q u e n c y of s h i p p i n g across the Atlantic to t h e N o r t h Sea c o m p a r e d to t h e l o n g v o y a g e s from the Pacific m a y b e decisive. F u r t h e r m o r e , v o y a g e s from the Pacific r e g i o n to E u r o p e n e e d to pass t h r o u g h tropical areas, w h i c h m a y affect t h e survival rates of s p e c i e s a d a p t e d to c o l d - t e m p e r a t e r e g i o n s such as n o r t h e r n J a p a n . In addition, s e v e r a l i n v e r t e b r a t e s w e r e i n t r o d u c e d with A m e r i c a n oysters (Crassostrea virginica) to the British Isles a n d the North S e a ( H e d g p e t h , 1980; Eno et al., 1997). In

(9)

contrast to m a c r o a l g a e , the m a c r o b e n t h i c f a u n a a l o n g the North A m e r i c a n Atlantic shores does not s e e m to be less diverse t h a n its c o u n t e r p a r t on the E u r o p e a n Atlantic shore (Briggs, 1974).

T a k i n g all n o n - n a t i v e s together (Table 1), up to 32 species are a s s u m e d to b e intro- d u c e d with A m e r i c a n a n d Pacific oysters. Almost all others were p r o b a b l y u n i n t e n t i o n - ally i n t r o d u c e d by shipping. About 20 species h a v e also i n v a d e d other coasts outside the E u r o p e a n Atlantic, a n d thus s e e m to h a v e a n intrinsic aptitude to b e c o m i n g intro- d u c e d a n d t h e n established. T h e s e species are t r a m p i n g from harbor to h a r b o r a n d es- t u a r y to e s t u a r y by ship or have followed the w o r l d w i d e trade with Pacific oysters (Cras- sostrea gigas).

Within the North Sea, by far the majority of i n t r o d u c e d exotics first b e c a m e established in the south a n d a b o u t half of t h e m h a v e not yet b e e n e n c o u n t e r e d in the north.

This a s y m m e t r y m a y be c a u s e d by three p h e n o m e n a : (1) n e a r l y all the i m p o r t a n t ports of the North Sea are in the s o u t h e r n half: Le Havre, S o u t h a m p t o n , London, Antwerp, Rotterdam, A m s t e r d a m , B r e m e n a n d H a m b u r g ; (2) species associated with i n t r o d u c e d oysters t e n d to originate from regions with h i g h e r t e m p e r a t u r e s than from the n o r t h e r n North Sea, a n d most of these i n t r o d u c t i o n s occurred t h r o u g h the g a t e w a y of the F r e n c h a n d s o u t h e r n British coasts (Korringa, 1976a,b; Chew, 1990); (3) the c o l d - t e m p e r a t e flora a n d f a u n a in the e a s t e r n a n d w e s t e r n provinces of the n o r t h e r n Atlantic have m a n y species in common, while the w a r m - t e m p e r a t e biota have no close relationship b e t w e e n the opposite coasts b e c a u s e both h a v e b e e n geographically isolated so m u c h l o n g e r t h a n the biota further north (Briggs, 1974; Watling, 1979; Lfining, 1990). Thus, there is a c o n s i d e r a b l y larger species pool in the w a r m - t e m p e r a t e r e g i o n from which r e c o g n i z a b l e introductions m a y be d r a w n . C o n s e q u e n t l y , u n d e r climatic w a r m i n g the i m p o r t a n c e of exotics in the entire North Sea could increase.

Based on s h i p p i n g intensity, with v o l u m e s of ballast water i n c r e a s i n g a n d p a s s a g e times d e c r e a s i n g , the rate of introductions is e x p e c t e d to increase t h r o u g h o u t the t w e n -

Fig. 1. Timeline of recorded North Sea introductions (n = 79} sorted by assumed mode of transport

(10)

tieth century. This is exemplified by the S a n Francisco Bay a n d the Great Lakes (Mills et al., 1994; C o h e n & Carlton, 1996). T h e a c t u a l time course of first records from intro- d u c e d species in the North Sea does not refute this t r e n d b u t is less r e g u l a r (Fi 9, 1).

T h e r e is a p e a k in the 1970s, which m a y partly be e x p l a i n e d by imports of Crassostrea gigas a n d its associated organisms. T h e s e imports occurred to France, Britain a n d T h e N e t h e r l a n d s in the 1960s to 1970s (Korringa, 1976b). Also, the c o m p o n e n t s of ship an- tifouling p a i n t s w e r e c h a n g e d in the 1970s. T h e n e w hull coating which c o n t a i n e s tri- b u t y l - t i n n (TBT) might be more effective c o m p a r e d to previously used c o m p o u n d s . This m a y have p r e v e n t e d a further i n c r e a s e in the rate of introductions since the 1970s (Minchin & S h e e h a n , 1995). No difference in the time course of i n t r o d u c t i o n s b e t w e e n algae a n d i n v e r t e b r a t e s is a p p a r e n t .

THE NET E F F E C T OF EXOTICS

D u r i n g the last glaciation approx. 18 000 years ago, surface water t e m p e r a t u r e s in the residual North Sea w e r e a b o u t 10 ~ lower t h a n today (Mclntyre et al., 1976). Con- c o m i t a n t with this drop in t e m p e r a t u r e , the sea level fell by at least 110 m, t u r n i n g most of the North Sea into arctic dry land. Thus, the coastal North Sea was a hostile e n v i r o n - m e n t for m a r i n e o r g a n i s m s at that time. Recolonization from refuges m a y still not be complete, a n d the North Sea m a y well be below its p o t e n t i a l c o n t i n g e n t of species within the North Atlantic. C o m p a r e d to the n o r t h e r n Pacific with its rich coastal flora a n d fauna, the entire n o r t h e r n Atlantic is poor in species. Transarctic i n t e r c h a n g e s dur- ing i n t e r g l a c i a l periods w e r e highly a s y m m e t r i c with almost all i m m i g r a t i o n s directed from the Pacific to the Atlantic region r a t h e r t h a n the reverse (Vermeij, 1991). Thus, its ecological history m a y predispose the North Sea as a recipient area for exotic introductions from outside the Atlantic region.

What is the overall effect of the i n t r o d u c e d exotics on the North Sea biota? Up to now, there is no e v i d e n c e that exotics h a v e d r i v e n n a t i v e s to extinction. Thus, the species n u m b e r in the North Sea w o u l d h a v e b e e n i n c r e a s e d , if there w e r e no extinctions c a u s e d by other m e a n s , i.e., fishing, h u n t i n g , h a b i t a t alterations or toxic substances. Locally, the n u m e r i c a l n e t b a l a n c e m a y come close to zero (i.e., Reise, 1982), b u t the type of o r g a n i s m s is not c o n g r u e n t . As has b e e n r e v i e w e d e l s e w h e r e (Williamson, 1996), not all but most of the successful i n v a d e r s are generalists. Those t a k e n u p by ships should be c o m m o n a n d a b u n d a n t at h a r b o r sites. Accordingly, they are often e s t u a r i n e a n d well a d a p t e d to h u m a n - m o d i f i e d e n v i r o n m e n t s . To survive a long v o y a g e , high physiological tolerance is n e e d e d , at least for some s t a g e of the life cycle. To establish a p e r s i s t e n t a n d e x p a n d i n g p o p u l a t i o n with a small n u m b e r of arrivals requires high f e c u n d i t y a n d good m e a n s of dispersal. Exotics i m p o r t e d with mar- icultures do not n e e d to h a v e such properties. However, as q u a r a n t i n e p r o c e d u r e s are b e c o m i n g a n obligatory practice in a q u a c u l t u r e , a c c i d e n t a l introductions w i t h this vector will p r e s u m a b l y be limited to o r g a n i s m s with microscopic spores, r e s t i n g s t a g e s or to e n d o p a r a s i t e s . Species which v a n i s h e d from the North Sea coast, on the other h a n d , are to be f o u n d more a m o n g slow-growing, l a t e - m a t u r i n g , l a r g e - s i z e d species with limited offspring, w h e n fishing or h u n t i n g was the p r i m a r y threat, a n d with n a r r o w h a b i t a t re- q u i r e m e n t s w h e n h a b i t a t loss was the p r i m a r y cause.

(11)

T h e m a i n effect of species i n t r o d u c t i o n s into the North Sea s e e m s to b e a species a d d i t i o n r a t h e r t h a n a n e x c h a n g e . Some local d i s p l a c e m e n t s have occurred, however. A cIear e x a m p l e is the m a r s h g r a s s Spartina anglica, e s t a b l i s h i n g m o n o s t a n d s w h e r e other saltmarsh v e g e t a t i o n or seagrass h a d b e e n before, a n d which greatly modifies the h a b i - tat ( M e e s e n b u r g , 1975; Gray et al., 1991): In the Dutch Delta region S. anglica e v e n dis- p l a c e d the former s t a n d s of S. maritima (almost) completely. In E n g l a n d , however, S. an- glica a n d S. rnaritima rarely co-occurred, a n d the latter is a s s u m e d to h a v e d e c l i n e d since the 1930s b e c a u s e of l a n d r e c l a m a t i o n , coastal erosion a n d d i s p l a c e m e n t by Hal- i m i o n e portulacoides (Gray et al., 1991). Spartina maritima m a y itself b e a n early intro- d u c t i o n to E u r o p e from Africa (Chevalier, 1923). It h y b r i d i z e d with the North A m e r i c a n S. alterniflora a r o u n d 1870 n e a r S o u t h a m p t o n , w h e r e the latter was first recorded in 1816. From the sterile hybrid S. x townsendii, the n e w fertile species S. anglica origi- n a t e d by c h r o m o s o m e d o u b l i n g . This is at p r e s e n t a w i d e s p r e a d species in the North Sea region, b u t r e m n a n t p o p u l a t i o n s of S. maritirna, S. alterniflora a n d S. x townsendii still exist.

N e a r the island of Sylt in the e a s t e r n North Sea, the i n t r o d u c e d razor clam Ensis a m e r i c a n u s first occurred in 1979. In a s a n d y s e d i m e n t close to the s p r i n g low tide line, m a c r o f a u n a l biomass c o m p r i s e d 118 g dry organic w e i g h t m -2 in M a r c h 1993 (see Ar- m o n i e s & Reise, 1998). Of this biomass, 66% was c o n t r i b u t e d by the razor clam a n d a n - other 3 0 % b y the r a g w o r m N e r e i s virens, s u s p e c t e d to b e a n i n t r o d u c e d species as well (see above). T h e site was formerly o c c u p i e d by a d e n s e eelgrass m e a d o w which completely fell victim to a n i n v a s i v e d i s e a s e c a u s e d by the protist Labyrinthula zosterae in the 1930s (Wohlenberg, 19357 d e n Hartog, 1987). This ' w a s t i n g disease' r a p i d l y s p r e a d on both sides of the Atlantic at that time, a n d m a y be s u s p e c t e d to b e a h u m a n - a i d e d i n v a s i o n too. At the site n e a r Sylt, the eelgrass n e v e r came back. T h e former b e n t h i c f a u n a was c o m p o s e d m a i n l y of Lanice conchilega, P s a m m e c h i n u s miliaris a n d Littorina littorea a n d its zoomass was p r o b a b l y not m u c h h i g h e r t h a n the 28 g m -2 of a n a d j a c e n t l u g w o r m flat in March 1993 (Reise, u n p u b l i s h e d data). This local e x a m p l e m a y illustrate the p e r v a s i v e n e s s of i n t r o d u c t i o n s on coastal North Sea biota, a n d t h e history d e p e n - d e n c e of p r e s e n t - d a y a s s e m b l a g e s .

A b o u t 20 species of those listed in Table 1 are today w i d e s p r e a d i n the North Sea a n d are at least locally a b u n d a n t . Except for some parasites a n d t h e s h i p w o r m Teredo navalis, e c o n o m i c implications of the k n o w n i n t r o d u c t i o n s into the North Sea are low u p to now. Early in the e i g h t e e n t h c e n t u r y the w o o d - b o r i n g T. navalis c a u s e d a revolution i n Dutch coastal defence. Before its s u p p o s e d introduction, seawalls w e r e reinforced with w o o d e n posts, while since t h e n stones a n d other m e a n s h a d to b e used. C o n t e m - porary p e o p l e c o n s i d e r e d the ' p a a l w o r m ' a p l a g u e sent by God; in c o n s e q u e n c e , prayers w e r e said in the churches. Terodo navalis c o n t i n u e s to cause t r o u b l e i n w o o d e n structures built into the sea u n t i l today.

WHAT IS T O BE DONE ABOUT EXOTICS IN THE SEA?

N o n e of the exotics that h a v e i n v a d e d the North Sea c a n be r e m o v e d . As every introduction has the p o t e n t i a l of u n w a n t e d a n d u n c o n t r o l l a b l e c o n s e q u e n c e s , only pre- v e n t i v e m e a s u r e s m a y be effective. O n c e a n e w c o m e r has arrived, it has to b e accepted,

(12)

a n d its spread c a n only be o b s e r v e d with curiosity or scientific interest to l e a r n from its interactions with habitats, native c o m m u n i t i e s as well as other exotics. T h e s e mostly in- a d v e r t e n t introductions have irreversibly modified the North Sea ecosystem. This is a c u m u l a t i v e process m u c h faster t h a n a n y n a t u r a l c h a n g e could ever accomplish, a n d enforces a progressive d e t h r o n e m e n t of the n a t i v e o r g a n i s m s from the c e n t e r of their a c c u s t o m e d ecological c o m m u n i t i e s . Q u a l i t a t i v e l y a n d m a y b e also quantitatively, the c o m b i n e d effect of i n t r o d u c e d n e o p h y t e s a n d n e o z o a n s exceeds the more often consid- ered e n v i r o n m e n t a l effects of e u t r o p h i c a t i o n a n d toxic substances, a n d m a y rival those of the fishery in the North Sea a n d of h a b i t a t loss along its coastline.

In view of the fact that in the North Sea exotic species have b e e n primarily addi- tions rather t h a n the cause of d i s p l a c e m e n t s or e v e n extinctions, problems with the exotics m a y reside less in ecology a n d more in e c o n o m y or h u m a n health. As i n t r o d u c t i o n s e l s e w h e r e have shown, there is a l w a y s a n e l e m e n t of risk w h e n n e w species arrive.

T h e y m a y prey on commercially v a l u a b l e species or cause diseases in species consid- ered also to be otherwise important, i n c l u d i n g h u m a n s themselves. T h e y m a y drill holes t h r o u g h dikes a n d w o o d e n docks or infest other sensitive structures. To m i n i m i z e these risks, existing q u a r a n t i n i n g protocols for m a r i c u l t u r a l organisms should be strictly ad- h e r e d to. Being a w a r e of the p r o b l e m of u n - i n t e n t i o n a l l y i n t r o d u c e d n o n - t a r g e t species for a q u a c u l t u r e , the ICES Working G r o u p on Introductions a n d Transfers on M a r i n e Or- g a n i s m s d e v e l o p e d a 'Code of Practice' listing p r e d o m i n a n t l y q u a r a n t i n e p r o c e d u r e s prior to a n d after the import of a target species. Problems are m a i n l y with g a p s in the a d h e r e n c e to these procedures, a n d more a w a r e n e s s , t r a i n i n g a n d control is n e e d e d .

C o n c e r n i n g u n i n t e n t i o n a l l y i n t r o d u c e d species by ballast water of o c e a n - g o i n g ships, the I n t e r n a t i o n a l Maritime O r g a n i z a t i o n {IMO) d e v e l o p e d g u i d e l i n e s to m i n i m i z e the transport of species in ballast water. T h e s e are m a i n l y b a s e d on the a v o i d a n c e of ballast water u p t a k e in shallow areas, in areas with k n o w n disease o u t b r e a k s or phyto- p l a n k t o n blooms, a n d on attempts to r e d u c e the a m o u n t of ballast w a t e r to be dis- charged. Additionally, a complete m i d - o c e a n e x c h a n g e of the ballast w a t e r on b o a r d is r e c o m m e n d e d , a s s u m i n g that m i d - o c e a n species are u n l i k e l y to survive in coastal w a - ters a n d vice versa. O t h e r possible ballast w a t e r t r e a t m e n t s are filtering a n d h e a t i n g . Some countries (e.g. Australia, Brazil, C a n a d a , Chile, Israel, N e w Z e a l a n d a n d the USA) require ballast water e x c h a n g e or t r e a t m e n t prior to the release in their coastal waters. T h e North Sea countries should follow the ICES Code of Practice a n d enforce the ballast w a t e r r e g u l a t i o n s a n d d e v e l o p m e n t s by the IMO as legally b i n d i n g provi- sions. Ballast w a t e r m a n a g e m e n t also n e e d s to be t a k e n into a c c o u n t in the c o n s t r u c t i o n a n d d e s i g n of n e w vessels.

M u c h r e m a i n s u n k n o w n in terms of the p a t t e r n s a n d processes of i n v a s i o n s . T h e g e n e r a l d e c l i n e in the n u m b e r of t a x o n o m i c experts is a major i m p e d i m e n t in the i d e n - tification of exotics, in m o n i t o r i n g their i n v a s i o n s a n d r e c o g n i z i n g their effects. T h e r e - fore large gaps r e m a i n in the k n o w l e d g e n e e d e d to establish effective m a n a g e m e n t plans. E x a m p l e s of research n e e d s are:

1. F u r t h e r studies on the ecology of i n t r o d u c e d species: only a few of the i n t r o d u c e d n o n - i n d i g e n o u s species h a v e b e e n the s u b j e c t of q u a n t i t a t i v e a n d e x p e r i m e n t a l studies. Particularly, their c o m b i n e d i m p a c t on n a t i v e ecosystems c a n n o t be esti-

(13)

I n t r o d u c e d m a r i n e s p e c i e s of t h e N o r t h S e a coasts 231

m a t e d at p r e s e n t . E c o n o m i c i m p a c t s of (e.g.) w o o d b o r e r s ( s h i p w o r m s a n d isopods) a n d of f o u l i n g o r g a n i s m s (on v e s s e l s a n d s u b m e r g e d i n s t a l l a t i o n s ) a r e w i d e l y u n - k n o w n a n d r e m a i n l a r g e l y u n d o c u m e n t e d a n d e n t i r e l y u n q u a n t i f i e d .

2. G e n e t i c s t u d i e s of i n v a d e r s : t h e a p p l i c a t i o n of m o l e c u l a r g e n e t i c s h a s a l r e a d y re- v e a l e d t h e c r y p t i c p r e s e n c e of p r e v i o u s l y u n r e c o g n i z e d i n v a d e r s in t h e S a n F r a n - cisco Bay a r e a . S t u d i e s o n t h e p o l y c h a e t e M a r e n z e l l e r i a r e v e a l e d t h a t in fact t w o s p e c i e s , M. cf. v i r i d i s a n d M. cf. w i r e n i , d i d i n v a d e , t h e f o r m e r p r e d o m i n a n t l y t h e Baltic S e a a n d t h e l a t t e r t h e N o r t h S e a (Essink & Schbttler, 1997; E s s i n k , 1999). T h e o b j e c t i v e to e v a l u a t e ' h o t s p o t a r e a s of o r i g i n ' of f u r t h e r s p e c i e s i n t r o d u c t i o n s m a y b e d e t e r m i n e d m o r e p r e c i s e l y b y g e n e t i c a l c o m p a r i s o n b e t w e e n i n t r o d u c e d s p e c i e s a n d t h e i r n a t i v e d i s t r i b u t i o n a r e a . A l s o t h e o c c u r r e n c e of s e c o n d a r y i n t r o d u c t i o n s c a n b e p r o v e n in this way.

3. Risk a s s e s s m e n t : as e v e r y s i n g l e v e s s e l h a s t h e p o t e n t i a l to i n t r o d u c e s p e c i e s , it s e e m s to b e less i m p o r t a n t to e s t i m a t e t h e total a m o u n t of b a l l a s t w a t e r d i s c h a r g e s t h a n to k n o w all p o t e n t i a l s o u r c e a r e a s of b a l l a s t w a t e r a c c o r d i n g to t h e s h i p p i n g r o u t e s out- s i d e t h e N o r t h Sea. A q u a n t i t a t i v e risk a s s e s s m e n t c a n b e c a r r i e d o u t for s h i p s w h e n sites of b a l l a s t i n g a n d d e b a l l a s t i n g a r e k n o w n a n d o p t i o n s for b a l l a s t w a t e r t r e a t - m e n t h a v e to b e d e c i d e d on ( H a y e s , 1998), a n d for ports w h e r e t h e e x a c t p r o f i l e s of b a l l a s t w a t e r s o u r c e s a r e k n o w n . Similarly, c o s t / b e n e f i t a n a l y s i s for p l a n n e d intro- d u c t i o n s in a q u a c u l t u r e s h o u l d b e o b l i g a t o r y . M a n y a s p e c t s of i n v a s i o n s will r e m a i n n e a r l y u n p r e d i c t a b l e as no a n s w e r s c a n b e g i v e n to t h e c r u c i a l q u e s t i o n s : W h i c h s p e c i e s will i n v a d e , w h e n a n d w h e r e will it i n v a d e a n d w h a t will b e t h e i m p a c t of this n e w s p e c i e s ? W e k n o w t h a t h a b i t a t s at p a r t i c u l a r risk a r e e s t u a r i e s w i t h i n t e r - n a t i o n a l ports, w a t e r w a y s a n d s h i p p i n g r o u t e s as w e l l as a q u a c u l t u r e sites. T h e y r e p r e s e n t h i g h risk a r e a s for f u r t h e r i n t r o d u c t i o n s , a n d s h o u l d b e m o n i t o r e d a c c o r d - ingly.

It is false to s a y t h a t e v e r y s p e c i e s t h a t c o u l d h a v e b e e n i n t r o d u c e d w o u l d b e in t h e N o r t h S e a by now. T h e t i m e c o u r s e of i n t r o d u c t i o n s d o e s n o t s u g g e s t a s a t u r a t i o n l e v e l (Fig. 1). T h e c h a n c e of a s p e c i e s b e c o m i n g i n t r o d u c e d , e s t a b l i s h e d a n d t h e n b e c o m i n g a s e r i o u s p r o b l e m for t h e e n v i r o n m e n t or e c o n o m y at t h e r e c i p i e n t c o a s t is small. H o w - ever, o n e s i n g l e i n t r o d u c e d s p e c i e s m a y b e a b l e to c a u s e s e v e r e e c o l o g i c a l c h a n g e a n d e c o n o m i c d a m a g e , a n d this m i g h t b e t h e n e x t s p e c i e s a b o u t to a r r i v e .

A c k n o w l e d g e m e n t s . We wish to thank the participants of the workshop on Exotic Invaders of the North Sea Shore, held on Sylt in February 1998, for contributing facts and ideas incorporated in this review. This is Alfred Wegener Institute Publication No. 1553.

L I T E R A T U R E C I T E D Anderson, D. M., 1994. Red tides. - Sci. Am., August, 52-58.

Armonies, W. & Reise, K., 1998. On the population development of the introduced razor clam En- sis a m e r i c a n u s near the island of Sylt (North Sea). - Helgol/inder Meeresunters. 52.

Bertness, M. D., 1984. Habitat and community modification by an introduced herbivorous snail. - Ecology 65,370-381.

Brenchley, G. A. & Carlton, J. T., 1983. Competitive displacement of native mud snails by introduced periwinkles in the N e w England intertidal zone. - Biol. Bull. 165, 543-558.

Briggs, J. C., 1974. Marine zoogeography. - McGraw-Hill, New York, 475 pp.

(14)

2 3 2 K. R e i s e , S. G o l l a s c h & W. J. W o l f f

C a r l t o n , J. T., 1985. T r a n s o c e a n i c a n d i n t e r o c e a n i c d i s p e r s a l of c o a s t a l m a r i n e o r g a n i s m s : t h e biol- o g y of b a l l a s t w a t e r . - O c e a n o g r . Mar. Biol. A n n u . Rev. 23, 3 1 3 - 3 7 1 .

C a r l t o n , J. T., 1989. M a n ' s role in c h a n g i n g t h e f a c e of t h e o c e a n : biological i n v a s i o n s a n d impli- c a t i o n s for c o n s e r v a t i o n of n e a r - s h o r e e n v i r o n m e n t s . - C o n s e r v . Biol. 3, 2 6 5 - 2 7 3 .

C a r l t o n , J. T., 1996. Biological i n v a s i o n s a n d c r y p t o g e n i c s p e c i e s . - E c o l o g y 77, 1 6 5 3 - 1 6 5 5 . C a r l t o n , J. T. & Geller, J. B., 1993. E c o l o g i c a l roulette: t h e g l o b a l t r a n s p o r t of n o n i n d i g e n o u s m a -

rine o r g a n i s m s . - S c i e n c e 26I, 7 8 - 8 2 .

C a r l t o n , J. T., T h o m p s o n , J. K., S c h e m e l , L. E. & Nichols, F. H., 1990. R e m a r k a b l e i n v a s i o n of S a n F r a n c i s c o Bay (California, USA) by t h e A s i a n c l a m Potamocorbula amurensis. I. I n t r o d u c t i o n a n d d i s p e r s a l . - Mar. Ecol. Prog. Ser. 66, 81-94.

C e c c h e r e l l i , G. & Cinelli, F., 1997. S h o r t - t e r m effects of n u t r i e n t a d d i t i o n a n d i n t e r a c t i o n s b e t w e e n t h e s e a g r a s s C y m o d o c e a nodosa a n d t h e i n t r o d u c e d g r e e n a l g a Caulerpa taxifolia in a M e d i t e r - r a n e a n bay. - J. Exp. Mar. Biol. Ecol. 217, 165-177.

C h a p m a n , A. S., 1999. F r o m i n t r o d u c e d s p e c i e s to i n v a d e r : w h a t d e t e r m i n e s v a r i a t i o n in t h e s u c - c e s s of Codium fragile ssp. t o m e n t o s o i d e s ( C h l o r o p h y t a ) in t h e N o r t h A t l a n t i c O c e a n . - H e l g o - l ~ n d e r M e e r e s u n t e r s . 52.

C h e v a l i e r , A., 1923. N o t e s u r les Spartina d e la flore f r a n q a i s e . - Bull. Soc, Bot. Fr. 70, 5 4 - 6 3 . C h e w , K. K., 1990. G l o b a l b i v a l v e s h e l l f i s h i n t r o d u c t i o n s . - World A q u a c u l t u r e 21, 9 - 2 4 .

C o h e n , A. N. & C a r l t o n , J. T., 1996. N o n i n d i g e n o u s s p e c i e s in a U n i t e d S t a t e s e s t u a r y : a c a s e history of t h e e c o l o g i c a l a n d e c o n o m i c effects of b i o l o g i c a l i n v a s i o n s in t h e S a n F r a n c i s c o a n d Delta r e g i o n . - Report to t h e US Fish & Wildlife Service, 246 pp. (+ a p p e n d i c e s ) .

d e Vill61e, X. & V e r l a q u e , M., 1995. C h a n g e s a n d d e g r a d a t i o n in a Posidonia oceanica b e d i n v a d e d by t h e i n t r o d u c e d tropical a l g a Caulerpa taxifolia in t h e n o r t h w e s t e r n M e d i t e r r a n e a n . - Bot.

Mar. 38, 7 9 - 8 7 .

Elbr~ichter, M., 1999. Exotic f l a g e l l a t e s of c o a s t a l N o r t h S e a w a t e r s . - Helgol~inder M e e r e s u n t e r s . 52.

Eno, N. C., Clark, R. A. & S a n d e r s o n , W. G., 1997. N o n - n a t i v e m a r i n e s p e c i e s in British w a t e r s : a r e v i e w a n d directory. J o i n t N a t u r e C o n s e r v a t i o n C o m m i t t e e , P e t e r b o r o u g h , 152 pp.

E s s i n k , K., 1999. D i s p e r s a l a n d d e v e l o p m e n t of Marenzelleria s p p . ( P o l y c h a e t a , S p i o n i d a e ) p o p u - l a t i o n s in N W E u r o p e a n d T h e N e t h e r l a n d s . - H e l g o K i n d e r M e e r e s u n t e r s . 52

Essink, K. & Sch6ttler, U. (eds), 1997. Studies on M a r e n z e l l e r i a spp. (Polychaeta: Spionidae). - Aquat. Ecol. 31, 117-258.

F e n c h e l , T., 1993. T h e r e a r e m o r e s m a l l t h a n l a r g e s p e c i e s ? - O i k o s 68, 3 7 5 - 3 7 8 .

Fletcher, R. L. & Farrell, P., 1999. I n t r o d u c e d b r o w n a l g a e in t h e N o r t h East A t l a n t i c , w i t h p a r t i c u - lar r e s p e c t to Undaria pinnatifida ( H a r v e y ) S u r i n g a r . - H e l g o l ~ n d e r M e e r e s u n t e r s . 52.

Gerlach, S. A., 1977. M e a n s of m e i o f a u n a dispersal. - Mikrofauna M e e r e s b o d e n 61, 89-103.

G o l l a s c h , S., 1996. U n t e r s u c h u n g e n d e s A r t e i n t r a g e s d u r c h d e n i n t e r n a t i o n a l e n S c h i f f s v e r k e h r u n - ter b e s o n d e r e r B e r f i c k s i c h t i g u n g n i c h t h e i m i s c h e r A r t e n . - V e r l a g Dr. Kovac, H a m b u r g , 210 pp.

G o l l a s c h , S. & R i e m a n n - Z i i r n e c k , K., 1996. T r a n s o c e a n i c d i s p e r s a l of b e n t h i c m a c r o f a u n a : Huli- planella luciae (VerrilI, 1898) ( A n t h o z o a , Actiniaria) f o u n d on a s h i p ' s hull in a s h i p y a r d d o c k in H a m b u r g H a r b o u r , G e r m a n y . - H e l g o l ~ n d e r M e e r e s u n t e r s . 50, 2 5 3 - 2 5 8 .

Gray, A. J. D., M a r s h a l l , D. F. & R a y b o u l d , A. F., 1991. A c e n t u r y of e v o l u t i o n in Spartina anglica.

- Adv. Ecol. Res. 2 I, 1-62.

G r o s h o l z , E. D. & Ruiz, G. M., 1995. S p r e a d a n d p o t e n t i a l i m p a c t of t h e r e c e n t l y i n t r o d u c e d Euro- p e a n g r e e n crab, Carcinus maenas, in c e n t r a l California. - Mar. Biol. 122, 2 3 9 - 2 4 7 .

H a g m e i e r , A., 1925. Vorl~iufiger B e r i c h t iiber d i e v o r b e r e i t e n d e n U n t e r s u c h u n g e n d e r B o d e n f a u n a d e r D e u t s c h e n B u c h t m i t d e m P e t e r s e n - B o d e n g r e i f e r . - Ber. D t s c h . Wiss. K o m m . M e e r e s f o r s c h . , N e u e F o l g e 1 , 2 4 7 - 2 7 2 .

H a r t o g , C. d e n , 1987. " W a s t i n g d i s e a s e " a n d o t h e r d y n a m i c p h e n o m e n a in Zostera b e d s . - A q u a t . Bot. 27, 3 - 1 4 .

H a y e s , K. R., 1998. E c o l o g i c a l risk a s s e s s m e n t for b a l l a s t w a t e r i n t r o d u c t i o n s : a s u g g e s t e d a p - p r o a c h . - ICES J. Mar. Sci. 55, 2 0 1 - 2 1 2 .

H a y w a r d , P. J. & R y l a n d , J. S., 1990. T h e m a r i n e f a u n a of t h e British Isles a n d N W - E u r o p e . C l a r e n - d o n Press, Oxford, 996 pp.

(15)

I n t r o d u c e d m a r i n e s p e c i e s of t h e N o r t h S e a c o a s t s 2 3 3 H e d g p e t h , J.W., 1980. T h e p r o b l e m of i n t r o d u c e d s p e c i e s in m a n a g e m e n t a n d m i t i g a t i o n . - H e l g o -

l~inder M e e r e s u n t e r s . 33, 6 6 2 - 6 7 3 .

J a n s s o n , K., 1994. A l i e n s p e c i e s in t h e m a r i n e e n v i r o n m e n t : i n t r o d u c t i o n s to t h e Baltic S e a a n d t h e S w e d i s h W e s t C o a s t . - S w e d i s h E n v i r o n m e n t a l P r o t e c t i o n A g e n c y , Solna, S w e d e n , 68 p p . K i m m e r e r , W. J., G a r t s i d e , E. & Orsi, J. J., 1994. P r e d a t i o n by a n i n t r o d u c e d c l a m as t h e likely

c a u s e of s u b s t a n t i a l d e c l i n e s in z o o p l a n k t o n of S a n F r a n c i s c o Bay. - Mar. Ecol. Prog. Ser. 113, 81-93.

K i n n e , O., 1984. D i s e a s e s of m a r i n e a n i m a l s , vol. IV, Part 1. Biologische A n s t a l t H e l g o l a n d , H a m ~ b u r g , 541 pp.

K i n z e l b a c h , R., 1995. N e o z o a n s in E u r o p e a n w a t e r s - e x e m p l i f y i n g t h e w o r l d w i d e p r o c e s s of i n v a - s i o n a n d s p e c i e s m i x i n g . - E x p e r i e n t i a 5I, 5 2 6 - 5 3 8 .

K o r r i n g a , P., 1976 a. F a r m i n g t h e flat o y s t e r s of t h e g e n u s Ostrea. - Elsevier, A m s t e r d a m , 238 pp.

K o r r i n g a , P., 1976 b. F a r m i n g t h e C u p p e d o y s t e r s of t h e g e n u s Crassostrea. - Elsevier, A m s t e r d a m , 224 pp.

L a u c k n e r , G., 1983. D i s e a s e s of m a r i n e M o l I u s c a : Bivalvia. In: D i s e a s e s of m a r i n e a n i m a l s , vol. II.

Ed. b y O. K i n n e . B i o l o g i s c h e A n s t a l t H e l g o l a n d , H a m b u r g , 477-961.

Ltining, K., 1990. S e a w e e d s , t h e i r e n v i r o n m e n t , b i o g e o g r a p h y , a n d e c o p h y s i o l o g y . - Wiley, N e w York, 527 pp.

M a g g s , C. A. & S t e g e n g a , H., 1999. R e d a l g a l e x o t i c s o n N o r t h S e a coasts. - H e l g o l ~ i n d e r M e e r e - s u n t e r s . 52

M c l n t y r e , C. D. et al. ( C L I M A P project m e m b e r s ) , 1976. The surface of the ice-age earth. - Science 191, 1131-1137.

M e e s e n b u r g , H., 1975. S p a r t i n a s k o l o n i s a t i o n l a n g s H o Bugt. - Geogr. Tidskr. 71, 37-45.

Mills, E. L., L e a c h , J. H., C a r l t o n , J. T. & Secor, C. L., 1994. Exotic s p e c i e s a n d t h e i n t e g r i t y of t h e G r e a t L a k e s . - B i o S c i e n c e 44, 6 6 6 - 6 7 6 .

M i n c h i n , D. & S h e e h a n , J., 1995. T h e s i g n i f i c a n c e of b a l l a s t w a t e r in t h e i n t r o d u c t i o n of e x o t i c m a - rine o r g a n i s m s to C o r k H a r b o u r , Ireland. - ICES A n n u a l S c i e n c e C o n f e r e n c e , A a l b o r g , D e n - m a r k , S e s s i o n O:1, 15 pp.

M 6 b i u s , K., 1877. Die A u s t e r u n d die A u s t e r n w i r t h s c h a f t . W i e g a n d t , H e m p e l & Parey, Berlin, 126 pp.

N e h r i n 9, S., 1998. N o n - i n d i g e n i o u s p h y t o p t a n k t o n s p e c i e s in t h e N o r t h Sea: s u p p o s e d r e g i o n of origin a n d p o s s i b l e t r a n s p o r t vector. - A r c h . Fish. Mar. Res. 46, 181-194.

N e h r i n g , S. & L e u c h s , H., 1999. N e o z o a ( M a k r o z o o b e n t h o s } a n d e r d e u t s c h e n N o r d s e e k f i s t e : e i n e 0 b e r s i c h t . - B u n d e s a n s t a l t ffir G e w ~ s s e r k u n d e , K o b l e n z , Bericht BfG-1200, 131 pp.

Nichols, F. H., T h o m p s o n , J. K. & S c h e m e l , L. E., 1990. R e m a r k a b l e i n v a s i o n of S a n F r a n c i s c o B a y (California, USA) by t h e A s i a n c l a m Potarnocorbula amurensis. [I. D i s p l a c e m e n t of a f o r m e r c o m m u n i t y . - Mar. Ecol. Prog. Set. 66, 9 5 - 1 0 1 .

N o r t h S e a T a s k Force, 1993. N o r t h S e a Q u a l i t y S t a t u s Report 1993. Oslo a n d Paris C o m m i s s i o n s , L o n d o n . O l s e n & O l s e n , F r e d e n s b o r g , D e n m a r k , 132 + vi pp.

R a s m u s s e n , E., 1973. S y s t e m a t i c s a n d e c o l o g y of t h e Isefjord m a r i n e f a u n a ( D e n m a r k ) . - O p h e l i a 11, 1-495.

Reise, K., 1982. L o n g - t e r m c h a n g e s in t h e m a c r o b e n t h i c i n v e r t e b r a t e f a u n a of t h e W a d d e n Sea: a r e p o l y c h a e t e s a b o u t to t a k e over? - N e t h . J. S e a Res. 16, 29-36.

Reise, K. & L a c k s c h e w i t z , D., 1998. B e n t h o s d e s W a t t e n m e e r e s z w i s c h e n Sylt u n d R e m o . In:

C ) k o s y s t e m W a t t e n m e e r , A u s t a u s c h - , T r a n s p o r t - u n d S t o f f u m w a n d l u n g s p r o z e s s e . Ed. b y C.

G~itje & K. Reise. S p r i n g e r , Berlin H e i d e l b e r g N e w York, 55-64.

Ruiz, G. M., C a r l t o n , J. T., G r o s h o l z , E. D. & H i n e s , A. H., 1997. G l o b a l i n v a s i o n s of m a r i n e a n d e s - t u a r i n e h a b i t a t s b y n o n - i n d i g e n o u s s p e c i e s : m e c h a n i s m s , e x t e n t , a n d c o n s e q u e n c e s . - A m . Zool. 37, 6 2 1 - 6 3 2 .

Stock, J.H., 1993. C o p e p o d a ( C r u s t a c e a ) a s s o c i a t e d w i t h c o m m e r c i a l a n d n o n - c o m m e r c i a l B i v a l v i a in t h e E a s t S c h e l d t , T h e N e t h e r l a n d s . - Bijdr. Dierk. 63, 61-64.

Thiel, H., 1968. Die E i n w a n d e r u n g d e r H y d r o m e d u s e Nernopsis bachei L. A g . a u s d e m os- t a m e r i k a n i s c h e n K f i s t e n g e b i e t in die w e s t e u r o p ~ i s c h e n Gew~isser u n d in d i e E l b m ~ i n d u n g . - A b h . N a t u r w i s s . Ver. H a m b u r g , N.F. 12, 8 1 - 9 4 .