HELGOL,5,NDER MEERESUNTERSUCHUNGEN Helgol~inder Meeresunters. 52, 243-258 (1999)

Red algal exot ics on North Sea coasts

Christ ine A. M a g g s 1 & Herre S t e g e n g a 2

I School of Biology and Biochemistry, Q u e e n ' s University of Belfast, Belfast BT9 7BL,

UK

Rijksherbarium, Van Steenis Gebouw, Einsteinweg 2, P.O. Box 9514, 2300 RA Leiden, The Netherlands

ABSTRACT: A total of ten red seaweed species are recognized as introduced into the North Sea from other parts of the world. These are Asparagopsis armata and Bonnemaisonia hamifera (Bon- nemaisoniales), Grateloupia doryphora (Halymeniales), Antithamnionella spirographidis, An- tithamnionella ternifolia, Anotrichium furcellatum, Dasya baillouviana, ?Dasysiphonia sp., Polysi- phonia harveyi and Polysiphonia senticulosa (Ceramiales). The oldest of these is B. hamifera, in- troduced prior to 1890, while the most recent, ?Dasysiphonia sp., was first found in 1994 and still requires taxonomic investigation. A variety of distribution patterns is seen, with geographical ranges varying from general within the North Sea to very restricted. The diversity of introduced red algae on eastern coasts of the North Sea is much greater than in the west. The most likely ex- planation for this pat tern is that French coasts were the initial site of introduction for many of the seaweeds, which were then distributed northwards by the residual surface currents. Their increas- ing success in the Nether lands has probably been promoted by the drastically changed local hy- drodynamic conditions which have also permitted the recent introduction of many native European species. Of the biological features of species that may favour their success as introductions, clonal vegetat ive propagation, often with specialized propagules or fragmentat ion mechanisms, is almost ubiquitous. Low-temperature tolerances can be inferred, but data are sparse. Many of the alien red algae in the North Sea contain anti-grazing compounds such as bromophenols, which may con- tribute to their invasive potential by deterr ing grazing sufficiently to permit es tabl ishment of an in- oculum.

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

T h e first i n t r o d u c t i o n s of exo t ic s e a w e e d s in to n o r t h e r n E u r o p e w e r e r e c o g n i z e d in

t he la te n i n e t e e n t h a n d ea r ly t w e n t i e t h c e n t u r i e s ( F a r n h a m , 1980). T h e s u b s e q u e n t

s p r e a d of t h e s e s e a w e e d s w a s fo l l owed k e e n l y b y p h y c o l o g i s t s in t h e 1930s a n d 1940s.

D u r i n g t he 1970s t h e r e w a s a r e s u r g e n c e of i n t e r e s t in i n t r o d u c e d a lgae , p r o m p t e d by

t h e r e c o g n i t i o n of s e v e r a l n e w a l i ens ( F a r n h a m , 1980), w h i c h c u l m i n a t e d in d e t e r m i n e d

a t t e m p t s to e r a d i c a t e t h e f u c o i d b r o w n a l g a Sargassurn rnuticum f rom t h e s o u t h coas t of

E n g l a n d . T h e fa i lu re to e l i m i n a t e or e v e n s low t h e s p r e a d of S. rnuticum p r o b a b l y con-

t r i b u t e d to a d e c l i n e in t h e a t t e n t i o n p a i d to a l i e n s e a w e e d s . O v e r t h e l a s t f e w y e a r s

t h e r e h a s b e e n a r e n e w a l of i n t e r e s t in m a r i n e i n t r o d u c t i o n s ( S i n d e r m a n e t al., 1992;

B o u d o u r e s q u e et al., 1994; R i b e r a & B o u d o u r e s q u e , 1995). Ba l las t w a t e r h a s b e e n t h e

m a i n focus, h o w e v e r , a n d as it c o n t a i n s v e r y f e w m a c r o a l g a l p r o p a g u l e s t h e m a r i n e

m a c r o a l g a e h a v e o f t e n b e e n i g n o r e d ( C a r l t o n & Gel ler , 1993). Now, h o w e v e r , co mp re~

�9 Biologische Anstalt Helgoland, Hamburg

244 C. A. M a g g s & H. S t e g e n g a

Fig. 1. Map of north-west Europe showing oceanographic features and broad-scale distribution of introduced red algae. British Isles and Solent lists were derived from l=arnham (1980) and Maggs & Hommersand (1993). Designated boundaries of the North Sea are indicated by dashed lines. Ar- rows indicate residual currents (from Lee & Ramster, 1981). Dotted lines are 5~ February

isotherms; sudace temperatures in shaded area are below 5 ~

Red algal exotics on North Sea coast 245

hensive lists of introduced seaweeds have been produced for European waters. The Joint Nature Conservat ion Committee has publ ished a directory of non-na t ive marine organisms in British waters (Eno et al., 1997) and a comprehensive European list is cur- rently being revised (S. Gollasch, personal communication).

This paper will be confined to red macroalgae bel ieved to have been introduced into the North Sea by human activities. The North Sea is here regarded as ex tending from the Dover-Calais constriction of the English Channe l northwards to a l ine be tween the Shetland Islands and Bergen, Norway (Fig. 1), and eastwards to its junct ion with the Baltic Sea at the Skagerrak-Kattegat line. In order to put the total numbers of invad- ing red algae in the North Sea into context, they are compared with those in another well-studied and ecologically diverse geographical region, the British Isles (Fig. 1). Al-

though some species are present in only one area or another, the total numbers in both regions are similar. However, a comparison with the Solent region of England, which has long been regarded as a 'hotspot ' for introductions (Farnham, 1980), shows that nearly as many species of alien red algae are found in the Solent as in the whole North Sea.

Each of the introduced red algae found in the North Sea will now be considered separately, in taxonomic order. For each species, the reasons for recognizing it as intro- duced will be discussed briefly, with some ment ion of the vector of introduction if known, and we summarize its geographical distribution and habitat in the North Sea. We will then concentrate on the biological features of each species that may have favoured its success as an invader. The type of data we cover include morphological and biochemical features, physiological results and life-history data from culture stud- ies where available; we will also refer to relevant, mostly unpubl ished, molecular data. Although Porphyra yezoensis Ueda was reported from Helgotand (Kornmann, 1986), we exclude it here on the basis of a comparison of nucleotide sequence data (of the Rubisco large subuni t-small subuni t spacer region) with that of authentic material from Japan (J. Brodie, personal communication). Mastocarpus stellatus (Stackhouse) Guiry has been introduced to Helgoland by scientific activity (Kornmann & Sahling, 1994), but it cannot be regarded as an exotic in the North Sea, be ing native to many North Sea coasts. Fi- nally, we will summarize the information for different species and draw conclusions concerning features of red algae that may be important in ensur ing their success as in- vaders of the North Sea.

RESULTS AND DISCUSSION

Asparagopsis arrnata H a r v e y ( B o n n e m a i s o n i a c e a e , B o n n e m a i s o n i a l e s )

Western Australia is the type locality of both Asparagopsis armata Harvey and its morphologically dissimilar te trasporangial Falkenbergia phase. A. armata is very dis-

tinctive, the only red seaweed to form barbed harpoon-l ike spines. The first Atlantic populat ion appeared in 1925 at Gu6thary in the Bay of Biscay (Irvine et al., 1975), and it was discovered almost s imul taneously at two Medi te r ranean localities. The Falken- bergia phase was noticed first in the British Isles (at Galway) in 1939; gametophytes

were found at Galway 2 years later. The Falkenbergia phase is now widespread in the

246 C.A. Maggs & H. Stegenga

Table 1. North Sea distribution of exotic red algae, with totals recorded in each area

Species Shetland E Scot- E & SE S Nor- Den- Nether- Belgium Orkney land England way mark lands NE France

NE W Swe- Get- England den many

A s p a r a g o p s i s a r m a t a +

(Drift only)

B o n n e m a i s o n i a h a m i f e r a + + + + +

(Drift only)

G r a t e l o u p i a d o r y p h o r a - - - + -

A n t i t h a m n i o n e l l a - - - + +

s p i r o g r a p h i d i s

A n t i t h a m n i o n e l l a terni fo l ia - + - - - + +

A n o t r i c h i u m f u r c e l l a t u m - - + -

D a s y a b o i l l o u v i a n a - - + + + -

? D a s y s i p h o n i a s p . - - - - + -

P o l y s i p h o n i a h a r v e y i - + + + + + +

P o l y s i p h o n i a s e n t i c u l o s a . . . . +

Total 2 3 2 3 3 8 4

British Isles, al though rare on east coasts, while the gametophyte appears to be con- fined to southern and south-western coasts (Farnham, 1980).

The gametophytic and tetrasporangial phases o f A . a r m a t a are bel ieved to have been introduced to Europe, possibly separately, from Australia. A second species, A. f a x i f o r m i s (Delile) Trevisan, is widespread in the tropics and in the Medi te r ranean; its key morphological character is the absence of barbed spines. The origins of A . a r m a t a

in northern Europe have been invest igated using 24 F a l k e n b e r g i a strains from Atlantic and Medi te r ranean Europe, the Car ibbean, and the North and South Pacific inc luding Australia (Ni Chualain, 1997; F. Ni Chualain, C. Maggs & M. Guiry, unpub l i shed data). Upper and lower temperature limits for growth and reproduction were de te rmined and restriction analysis of chloroplast DNA was carried out. All seven isolates from Atlantic Europe were identified as A . a r m a t a because they were identical to a strain of A . a r m a t a

collected at the type locality. They survived temperatures of 5-25 ~ and grew at 9 ~ to 21 (-23) ~ No restriction site mutat ions were found among these isolates, which ap- peared to be genetical ly uniform at this level of resolution.

In the North Sea, A . a r r n a t a ( F a l k e n b e r g i a phase only) is apparent ly k n o w n only from Orkney and Shet land (Table 1; Irvine et al., 1975). In Orkney it was found at two localities, growing epiphytically in intert idal pools, and it was also collected twice in Shet land (once intertidally, once subtidally). In the Nether lands only drift mater ial of both phases has been seen, p resumably originat ing in northern France as it does not oc-

cur in Belgium. The tempera ture tolerances of F a l k e n b e r g i a show unequivocal ly that A. a r m a t a is the only A s p a r a g o p s i s species that can colonize the coasts of the British Isles; isolates of A . t a x i f o r m i s s e n s u l a t o have lower survival limits of (9) 11-17 ~ The very

Red algal exotics on North Sea coast 247

restr ic ted dis tr ibut ion of Falkenbergiu in the North Sea is exp la ined by its in to lerance of winter t empera tu re s be low 5 ~ which are expe r i enced throughout the southern and eas te rn North Sea (ICES, 1962).

Severa l key fea tures of A. armuta seem to be associa ted with its g rea t success as an invader in the British Isles, where the t e t rasporophy te forms monospecif ic s tands in sui table habitats .

1. It has a high capaci ty for clonal reproduct ion. Both phases reproduce vege ta t ive ly (Dixon, 1965); the Falkenbergia phase spreads easi ly as floating balls whi le the ga- me tophy te hooks onto floating material . Rapid clonal sp read in Europe is ref lected in the genet ic ident i ty of all European Atlant ic populat ions .

2. It survives lower t empera tu res than other Asparagopsis species, a l though not low enough to permit it to colonize most of the North Sea.

3. Asparagopsis forms large amounts of ha logens and organic ha logen-con ta in ing ke- tones (Fenical, 1975), which are closely re la ted to the tear gas componen t monobro- moace tone and toxic to bacter ia , fungi and humans (despite this A. tuxi[ormis is ea ten in Hawaii!) . Asparagopsis species inc luding the Fa]kenbergia phase of A. ar-

matu also p roduce the noxious compound bromoform (Norris & Fenical , 1982). These h a l o g e n a t e d compounds are effective an t i -g raz ing agents , and A. tuxiformis is not ea ten by fish or urchins (Norris & Fenical , 1982).

B o n n e m u i s o n i a h u m i f e r u H a r i o t ( B o n n e m a i s o n i a c e a e , B o n n e m a i s o n i a l e s )

The te t rasporophyt ic (Trai]liella) and gametophy t i c phases of Bonnemaisonia hum-

iferu were first found in Europe (southern England) in 1890 and 1893 respec t ive ly (Farn- ham, 1980). Both phases are easi ly recognizable , the game tophy te by its hooks and the Truilliella phase by the presence of g land cells in a dist inctive a l ternate a r rangement . The Trailliellu phase has sp read nor thwards to Ice land and southwards to the Canaries , and from Labrador to Virginia (Breeman et al., 1988). Bonnemuisoniu hamifera is thought to have been in t roduced from Japan; plast id DNA restriction f ragment length po lymorphisms (C. Maggs & M. Guiry, unpub l i shed data) are identical in European and J a p a n e s e isolates. Today, it is so w i d e s p r e a d and a b u n d a n t in Europe that it can be re- g a r d e d as fully es tabl ished, with no possibi l i ty of eradicat ion.

The Trailliella phase occurs th roughout the North Sea, growing subt ida l ly in Scot- land and eas te rn England, and from nor thern Norway to France, a l though it is known in the Ne the r l ands only as drift. The gametophy t i c phase is absent from nor thern Nor- way but occurs southwards from southern Norway (Breeman eta] . , 1988). The differen- t ial dis t r ibut ion of the gametophy t ic and sporophyt ic phases of B. hamfferu results from complex in terac t ive responses to t empera tu re and day leng th in this spec ies (Lfining, 1980; Breeman et al., 1988). Reproduct ion in Traillie]lu requires a combina t ion of high t empe ra tu r e and short days, resul t ing in an au tumn "reproduct ive window" before the t empe ra tu r e becomes too low (Liining, 1980). In nor thern Norway, the window is closed. Matura t ion of game tophy t e s is also tempera ture-sens i t ive . B. hamifera is protan- drous, and in the nor thwest Atlantic males finish rep roduc ing before females a re fertile, so the life history is not comple ted there (Breeman et al., 1988); sporophytes survive by asexua l propagat ion . The species is much be t te r a d a p t e d to condit ions in J a p a n than

248 C. A. Maggs & H. Stegenga

those in the North Atlantic, consistent with other evidence that it has been introduced from Japan.

The features of B. hamifera that suit it to life as an invader of the North Sea are sim-

ilar to those already considered for the related Asparagopsis armata. Its wider distribu- tion and Japanese rather than Austral ian origins are correlated with greater physiolog- ical tolerances, however. It is more eurythermal than A. armata, surviving 0-28 ~ (Lfin- ing, 1984): of 23 Helgoland red algae tested by Lfining, only two tolerated higher tem- peratures. Both gametophytes and sporophytes can grow at 0~ but gametophytes

have a distinct growth optimum of 15 ~ whereas Trailliella grows well at 25 ~ (Bree- man et al., 1988), consistent with summer temperatures of 25 ~ at Shimoda, central Japan. Trailliella thrives under a wide range of envi ronmenta l conditions in the British Isles, inc luding those associated with very muddy and sheltered, almost anoxic habitats, where it forms beds up to 100 cm thick (Connor et al., 1997). Trailliella is particularly a b u n d a n t in impoverished communit ies such as those heavily grazed by sea urchins. The gland cells of Trailliella accumulate halogens (bromine is concentrated 30-fold, iodine 3-fold, relative to the ordinary cells), as shown by X-ray fluorescence electron micro- probe spectroscopy (Wolk, 1968). Like A. armata, both life-history phases spread rapid- ly by vegetat ive reproduction. The gametophyte attaches itself by its hooks to other ma- terial, such as Zostera fragments, and it is frequently found among drift material.

Grateloupia doryphora ( M o n t a g n e ) H o w e ( H a l y m e n i a c e a e , H a l y m e n i a l e s )

A large foliose species of Grateloupia discovered in 1969 in the Solent was attrib- uted by Farnham (1980) to G. doryphora on the basis of its morphological similarity to this Pacific alga and presumed to be an introduction. Marginal expansion in the Solent was slow initially, and after a decade it had colonized only about 20 km in both direc- tions from the original site. It took more than 20 years to reach the Isle of Wight, 8 km offshore (Farnham, 1997). However, in the meant ime (by 1984) it had spread to Milford Haven, Wales, growing near an oyster farm where it was still present in 1996. It was also found in the Medi te r ranean at Messina, Italy (de Masi & Gargiulo, 1982). Rapid ex- pansion is now taking place in the eastern North Atlantic. Grateloupia doryphora was found in the Channe l Islands in 1995 (Farnham, 1997), and is now well es tabl ished on the coasts of Brittany (Cabioch et al., 1997) and nor thern Spain (Farnham, 1997).

The only known North Sea site for this species is in former oyster ponds near Yerseke, in the tidal Oosterschelde, the Netherlands, where single thalli were found twice, on 18 August 1993 (tetrasporangial: S tegenga & Otten, 1997) and 15 November 1996 (cystocarpic: specimens in Leiden herbarium, L, collected by H. Stegenga).

Most of the newly discovered European populat ions are in the vicinity of shellfish farms, sugges t ing that this species has been transported with commercial molluscs. G. doryphora has recently appeared at Rhode Island, USA (Villalard-Bohnsack & Harlin, 1997), but the vector involved is unknown.

Antitharnnionella spirographidis Sch i f f ne r ( C e r a m i a c e a e , C e r a m i a l e s )

The earliest known British collection of Antithamnionella spirographidis was made in 1906 at Plymouth, but it was first described in 1911 from the Medi te r ranean (Maggs

Red algal exotics on North Sea coast 249

& Hommersand, 1993). Lindstrom & Gabrielson (1989) placed several North Pacific species in synonymy with A. spirographidis, and suggested that the species is of North Pacific origin. Culture studies support this conclusion, as Japanese, Californian and Eu- ropean isolates an in terbreed freely (Maggs, unpubl i shed data). It appears to have been introduced to Australia subsequent ly by shipping. A. spirographidis is small and incon- spicuous, and confusion with A. ternifolia (see L'Hardy-Halos, 1986) obscured its initial spread. In southern England, it is particularly common in yacht marinas, and margina l dispersal in Europe probably involves small boats.

In the North Sea, A. spirographidis is known only in the Netherlands, where the first record is from 31 July 1974, in an oyster pond near Yerseke (collected by H. Ste- genga, in L), and Belgium (Ostend in 1992: Coppejans, 1995). From 1993 onwards it has become rather common in the Nether lands in the tidal Oosterschelde, with a few col- lections from the s tagnant saline Grevel ingen. Plants occur year-round but are most a b u n d a n t during the second half of the year. Tetrasporangia are formed throughout the year, and gametangia in May to November. Temperature tolerances of this species are unknown, but its presence in the Nether lands suggests that it could colonize suitable habitats in most of the North Sea.

Both introduced Ant i thamnionel la species, A. spirographidis and A. ternifolia, have gland cells (Maggs & Hommersand, 1993). Gland cells of ant i thamnioid algae contain large amounts of halogens such as the brominated compound eosine and other bromo- phenols (Fenical, 1975), and al though these algae have not been subjected to grazing tests, it can be assumed that, as in the Bonnemaisoniaceae, they are grazing deterrents.

A n t i t h a m n i o n e l l a t e rn i fo l ia (J. D. H o o k e r & H a r v e y )

Lyle ( C e r a m i a c e a e , C e r a m i a l e s )

The first European record of Ant i thamnionel la ternifolia was [rom nor thern France in 1910; it was found in the Channe l Islands in 1921, was common in south Devon by 1926-1929, and was then reported from Ireland and the Isle of Man and later from west- ern Scotland (Maggs & Hommersand, 1993). When Lyle (1922) described her collections as a new species, A. sarniensis, she noted that the only similar plants were from the southern hemisphere, and assumed that the European populat ion was introduced. The origins of this introduction are still u n k n o w n - the situation is complex as there are a n u m b e r of morphologically similar and probably fairly closely related species in various parts of the world. Magne (1991) reported it as an introduction to Australia. L'Hardy- Halos (1986) found that the length and diameter of axial cells of tetraspore progeny from France vary. Some plants are short and stocky while others are more slender. This feature was genetically controlled - potential evidence of interspecific hybridizat ion

dur ing the evolutionary history of this species. In the North Sea, A. ternifolia is known from the SE coast of Scotland (St Abbs),

where it was common on sublittoral bedrock at 4-14 m (Hiscock, 1984), and as single records from the Nether lands (specimen in L collected by Den Hartog, 21 October 1951,

near Yerseke) and Belgium (Coppejans, 1995). This species is common in the British Isles, spreading clonally by vegeta t ive repro-

duction. It grows particularly well on artificial substrata such as ropes and mar ina pon-

250 C. A. Maggs & H. S t e g e n g a

toons, facil i tat ing its spread. Te t rasporang ia are formed in the autumn, but r e l eased te t raspores fail to ge rmina t e or grow into de fo rmed gametophytes . French isolates, by contrast, can undergo normal sexua l reproduc t ion a l though they also recycle tetra~ sporophytes apomict ica l ly (L 'Hardy-Halos , 1986).

Anotrichiurn furcellaturn (J. A g a r d h ) B a l d o c k ( C e r a m i a c e a e , C e r a m i a l e s )

Anotrichium furcellatum is be l i eved to have been in t roduced from the Medi ter - r anean to nor thern France prior to 1922 but the a lga now presen t in the M e d i t e r r a n e a n may not be ident ica l to that or ig inal ly found by J. Aga rdh ( F e l d m a n n - M a z o y e r & Mes- lin, 1939). Mode rn Med i t e r r anean popula t ions r e semble Monospora tenuis O ka mura from the Pacific, so they might have b e e n de r ived from the introduct ion of a (possibly conspecific) Pacific form into the r ange of the or iginal Med i t e r r anean a lga (Fe ldmann- Mazoyer & Meslin, 1939). In the North Sea, A. furcellaturn is known only from the Nether lands (S tegenga & Mol, 1983). Mate r ia l in L (six sheets in all) is from only two lo- calities, Yerseke oyster ponds (five collections) and Sas van Goes (one collection), and was usually found in the form of f ree-f loat ing "pompons" . All collections were m a d e in the per iod 1968-1977 (first record 2 Oc tober 1968 at Yerseke), dur ing the s u m m e r (July- October) , with the only t e t rasporang ia l s amp le ob ta ined in August . This spec ies has not been found in the Ne ther lands in recent years desp i te a ra ther in tensive sea rch at the original locations. In southern England, whe re the first collections were m a d e in 1976, A. furcellatum seems to be spreading . It rarely forms te t rasporangia but r ep roduces vig- orously by secondary a t t achment and f ragmenta t ion (Fe ldmann-Mazoye r & Meslin, 1939).

Dasya bail louviana (S.G. G m e l i n ) M o n t a g n e ( D a s y a c e a e , C e r a m i a l e s )

Dasya baillouviana is widely d is t r ibu ted in the Medi te r ranean , wes twards to Cadiz, and on the Atlantic coast of North America , from Nova Scotia to the C a r i b b e a n (Den Hartog, 1964; Dixon & Irvine, 1970; Richardson, 1981); it appea r s to be na t ive to both of these areas. In the North Sea a t t ached spec imens were first col lected on 6 A u g u s t 1950, in the "Kanaal door Zuid-Beveland" in SW Nethe r l ands (Den Hartog, 1964, as Dasya pedicellata). The origin of this popula t ion is unknownl but Den Har tog (1964) no ted that it was found only a few ki lometers from oyster ponds. Dasya baillouviana is a ve ry con- spicuous species, g rowing to 175 cm in height , and is easi ly recognizab le by its dense coat of p i g m e n t e d hair- l ike monos iphonous fi laments; soon (1953) it was no ted on the west coast of S w e d e n and was p resen t by 1961 in Denmark (Den Hartog, 1964) and 1969 in Norway. It now occurs qui te wide ly in D e nma rk (Nielsen & Kris t iansen, 1994). In the Nether lands , D. baillouviana was col lec ted regular ly for severa l years af ter its ini- t ial discovery, but only at the or iginal site and at "Gat van Ouwerke rk" , a no the r stag- nant sal ine or brackish locality. The popu la t ion in the Kanaal door Z u id -Be ve l a nd has pers i s ted even though this canal was exposed to a t idal reg ime in 1994. Recen t ly (since 1993), it has e x p a n d e d its distr ibution, b e c o m i n g es tab l i shed in the Veerse M e e t (stag- nan t and brackish), Greve l ingen (saline and s tagnant) and, less abundant ly , in the t idal Oos te r sche lde (near Yerseke).

Red algal exotics on North Sea coast 251

In the Ne the r l ands Dasya baillouviana is a summer annual , occurr ing in July to Oc- tober (to December) . Both te t rasporophytes and ga me tophy t e s reproduce in July to Oc- tober. The pheno logy of D. baillouviana in Nova Scotia, whe re this spec ies is restr ic ted to warm embaymen t s , is very similar to that in the Nether lands . Large vege ta t ive and reproduc t ive thall i a p p e a r in Augus t (when the t empera tu re is ca. 25 ~ and survive until N o v e m b e r when the t empera tu re drops to 5 ~ only juveni les a re p resen t in July and D e c e m b e r (Novaczek et al., 1987). By contrast, in North Carol ina macroscop ic thall i occur in win te r and spring, Feb rua ry to May, reproduc ing in Apri l and May (Richard- son, 1981).

The most s ignif icant biological features account ing for the success of this species on eas te rn North Sea coasts are (1) its phys io logica l tolerances, par t icular ly those of the spec ia l ized pe renna t ing pad- l ike holdfasts, and (2) its abil i ty to p ropaga t e vege ta t ive ly from f ragments as small as s ingle monos iphonous laterals.

In Europe D. baillouviana is euryhal ine , be ing able to grow throughout a salinity range of 10-30 psu, and it can also to lera te pol lut ion and high concentra t ions of hydro- gen su lph ide (Den Hartog, 1964). A cul ture from Nova Scotia was highly eu ry the rmal (Novaczek et al., 1987). Mature thalli were clear ly w a r m - t e m p e r a t e in their t empera tu re optima, g rowing and reproduc ing at 15-28 ~ and surviving 10-31 ~ However , spe- c ial ized pe renna t i ng pads composed of s tarch-f i l led cells survived at 0 ~ for 4 months and to lera ted all t empera tu res up to 34 ~ the wides t t empera tu re r ange of the four Nova Scotian species tested. Te t rasporophytes g rew rapidly and ma tu re d in only 6 weeks at 20 ~

After reproduct ion has finished, the monos iphonous f i laments that c lothe the thalli are shed as f i laments or s ingle cells and act as propagules , giving rise to numerous new indiv iduals (Novaczek et al., 1987). These p ropagu le s can deve lop into pe renna t ing pads, which also form direct ly on the thal lus from a t tached fi laments. In Nova Scotia, and p r e sumab ly the Ne ther lands also, D. baillouviana overwinters in the form of these pads, while in North Carol ina it persis ts dur ing the summer, when t empera tu re s can ex- ceed 30 ~ as pe renna t ing discs which are res is tant to gra iz ing by sea urchins and fish (Richardson, 1981). Probably the most en igmat ic aspect of the dis t r ibut ion of D. baiflou- viana in Europe, in view of its phys io logica l to lerances and rapid reproduct ion, is why it has fai led to colonize the east coast of England. The answer may lie in its r epor ted in- to lerance of wave action (Den Hartog, 1964). On Nor th Amer ican coasts, in the Medi te r - ranean, and in wes te rn Europe, it a p p e a r s to be res t r ic ted to w a v e - p r o t e c t e d areas (somet imes with fairly s trong t idal currents) . A l though she l t e red e m b a y m e n t s a re gen- eral ly absen t from south-eas t England, the crea t ion of n e w yacht mar inas dur ing the last d e c a d e could provide this species with a favourable habi ta t there. However , resid- ual currents a long the east coast of Britain flow southwards (Fig. 1) so these coasts may not receive drift material .

Dasysiphonia sp. ( D a s y a c e a e , C e r a m i a l e s )

Dasysiphonia sp. is a large red a lga (up to 30 cm high), first r eco rded in Europe on 28 June 1994, in former oyster ponds nea r Yerseke, The Ne the r l ands (S tegenga , 1997) and in May 1995 was col lected twice, independen t ly , in the in ter t idal zone nea r the

252 C. A. Maggs & H. Stegenga

marine station at Roscoff, Brittany. An apparent ly identical red alga corresponding to this species is now rather common on the Galician coast, especially "in areas strongly

inf luenced by human activities (i.e. mariculture)" (J. Cremades, personal c o m m u n u n i - cation), and may have been introduced there as early as 1990. Its generic affinities are uncertain: the formation of the four pericentral cells in an opposite/ transverse pat tern appears to be un ique within the family Dasyaceae. In NE Asia, from where this alga has presumably been introduced, this species has often mistakenly been identified as Het- erosiphonia japonica Yendo (H. Stegenga, unpubl i shed data; see de Jong et al., 1998).

It is now a common, sometimes abundant , species in most of the tidal Oosterschelde and occasionally in the s tagnant Lake Grevel ingen. Thalli occur throughout the year if the winter is mild. Only tetrasporophytes have been found to date, bear ing stichidia in June to November. The initial introduction may have been into France, perhaps, like

many other invading algae, with oysters. A factor in its success may be that, like Dasya baillouviana, this species regenerates easily from small fragments. As te t rasporangia are the only reproductive structures observed to date, it seems likely that this alga has an apomictic life history similar to that of many other Dasyaceae (Maggs, 1998).

Polysiphonia harveyi Bai ley ( R h o d o m e l a c e a e , C e r a m i a l e s )

Polysiphonia harveyi was described from Connect icut in 1848 and occupies the east coast of North America from Newfoundland to South Carolina. Recently, it was reported by Maggs & Hommersand (1990, 1993) to be widespread and a b u n d a n t in the British Isles. In Europe it can be identified readily by the key feature of the position of chloro- plasts. They are only on radial walls of the periaxial cells, so that the cells appear trans- parent, whereas in other European members of the genus chloroplasts also lie against the outer walls. In the Pacific, by contrast, there appears to be a group of species with this character (Yoon, 1986). Its systematic and nomencla tura l position is extremely prob- lematic. This plastid feature was later reported for a Polysiphonia species described from Brittany in 1867, P. insidiosa, which is bel ieved to be conspecific with P. harveyi. In Japan and Korea, P. harveyi-l ike algae, known as P. japonica Harvey and m a n y other synonyms, are common and widespread. Northwest European populat ions may repre- sent the last step in a cascade of introductions that started in the North Pacific. Speci- mens collected at Weymouth, Dorset, by A. D. Cotton in 1908 (in the Natural History Museum herbarium, BM) represent the first known British material of P. harveyi. Its eastern Atlantic distribution appears to be en larg ing rapidly at present, and it is now known from Norway (Rueness, 1994) to the Canary Islands (Rojas-Gonzalez et al., 1994).

In the North Sea, P. harveyi has been collected in eastern England and SE Scotland (Bradwell, Essex, July 1992; and St Andrews, Fife, 17 April 1992), the Nether lands, Hel- goland (Kornmann & Sahling, 1978, as P. violacea), Norway (Rueness, 1994), Denmark (Koch, 1986, as P. fibrillosa) and Belgium (Coppejans, 1995, as P. fibrillosa). It is mostly intertidal on a wide range of substrata such as the algae Codium fragile, Sargassum mu- ticum, Chondrus crispus, Mastocarpus stellatus and the ascidian Styela clava. It also grows on artificial surfaces such as ropes and pontoons and is particularly a b u n d a n t in marinas. The first definite North Sea record dates back to 1960 (The Nether lands, spec-

Red algal exotics on North Sea coast 253

imens in L). In the Nether lands P. harveyi is now very common and often a b u n d a n t in Oosterschelde and Grevel ingen, occurring over a fairly wide range of wave exposures and substrata. It is also found in the northern Netherlands (Texel), where it appears to be the only establ ished red invader. It occurs year-round, but is less a b u n d a n t in winter

(December to March) when tetrasporangia are absent. In many localities on North Sea coasts, P. harveyi is now the dominan t small sea-

weed dur ing much of the year. It has a wide range of biological features that have given it an advantage as an immigrant. These will be discussed under the categories (1) pre- ferred substratum, (2) habitat, (3) physiological tolerances, (4) life-history features, and

(5) inferred unpalatabi l i ty to grazers. Polysiphonia harveyi grows most abundan t ly on algae that float and drift well, par-

ticularly Codium fragile and Sargassum muticum. It is possible that it was in t roduced from Japan with Codium, since it grows on this species in Japan also. Sargassum rnu- ticum, as it undergoes vigorous marginal dispersal, may carry hitch-hiking P. harveyi with it. Polysiphonia harveyi occupies a wide range of intertidal and subt idal habitats, both in Japan and in Europe. Its a b u n d a n c e on artificial substrata such as fish cages and yacht moorings facilitates its movemen t along the coast. It can exploit a wide range of temperatures - an isolate from Denmark grew well and reproduced at 4-22 ~ (Koch, 1986). Male thalli are usually smaller than females and tetrasporophytes, sometimes re- producing when only 5 mm high, and are often ephemeral . Unusually, they form vege- tative propagules abundan t ly from modified male trichoblasts; the clonal propagat ion of further male thalli from these may be a mechanism that compensates for the fragility of males. Finally, we have observed that in heavily Littorina-grazed pools, P. harveyi is one of the few surviving seaweeds. Members of the Rhodomelaceae are perhaps the most prolific algal synthesizers of ha logena ted metaboli tes (Fenical, 1975). Many species of Polysiphonia form a wide range of bromophenols (Fenical, 1975) which are toxic to mi- croalgae; al though grazing tests have not been carried out on Polysiphonia species, their bromophenols presumably are grazing deterrents as in the Bonnemaisoniaceae .

Polys iphonia sent iculosa H a r v e y ( R h o d o m e l a c e a e , C e r a m i a l e s )

Polysiphonia senticulosa Harvey was originally described in 1862 from Washington State, and later from Alaska, as P. pungens Hollenberg. The correct name for this species is likely to be P. morrowii Harvey, described from Hokkaido, Japan (Yoon, 1986), a l though the proposed conspecificity of P. morrowii and P. senticulosa has b e e n ques- tioned (Kudo & Masuda, 1988). It is apparently native to a large area of the north-eastern and nor th-western Pacific and is bel ieved to have been introduced into Australia and New Zealand, possibly by shipping (Womersley, 1979; Nelson & Maggs, 1996). This four periaxial-celled species resembles the common native European species Polysiphonia stricta (Dillwyn) Greville, but can be dis t inguished by a un ique feature, sharply pointed

vegetat ive tips. It was first found in Europe on 4 May 1993 at Gorishoek, The Nether lands (col-

lected by H. Stegenga; specimen in L), and is now common in a large part of the Oost- erschelde, where it is locally a b u n d a n t in the oyster ponds of Yerseke Oesterbank. It oc- curs there in winter and spring, from October to June, and tetrasporangial and sexual

254 C. A. Maggs & H. Stegenga

reproduction both take place in November to June. Its phenology in Europe closely re-

sembles that of P. morrowii in Korea, which first appears in January and reproduces from the end of January to May, when it disappears (Kim et al., 1994). At present it is not known whether it was introduced independen t ly into Australia, New Zea land and

now the North Sea, but it seems likely that this species will spread further in Europe. We have no information on which features might make P. senticulosa successful as

an alien, but it is notable that several Polysiphonia species that have been int roduced have become seriously invasive. In North Carolina, P. breviarticulata (C. Agardh) Za- nardini has become a nuisance (Kapraun & Searles, 1990), washing up in quant i t ies on beaches, and in the Medi te r ranean one of the mostly rapidly spreading seaweeds is P. (= Womersleyella) setacea Hollenberg, which forms dense carpets on all sublit toral sur- faces (Athanasiadis, 1997).

CONCLUSIONS

North Sea aliens show a variety of distr ibution patterns (Fig. 1, Tables 1, 2), with ge- ographical ranges varying from general within the North Sea to very restricted. The di- versity of introduced red algae on the eas tern coasts of the North Sea is much greater than that on western coasts. Only one species, Asparagopsis armata (Falkenbergia phase), is confined to British coasts, and this is restricted to the offshore islands which have milder winters than the ma in land of eastern Scotland. The most likely explanat ion for this pat tern involves (1) the initial site of introduction of the seaweeds and (2) the residual surface currents. The great majority of seaweed introductions to Europe were first observed in France, including both Atlantic and Medi te r ranean coasts (Boudouresque, 1994). This may be partly due to the long and diverse coastline, but is probably also related to the extensive French aquacul ture industry. The diversity of alien seaweeds established in France provides a supply of propagules that drift north- east with the surface currents. Their success in The Nether lands (Table 2) has probably been promoted by the drastically changed local conditions as a result of the "Delta Hy- drotechnical Works", which have also permit ted the recent introduction of m a n y native European species (Stegenga, 1998).

Comparison of the biological features of each species that may favour their success as introductions (Table 2) shows that clonal vegetat ive propagat ion is almost ubiqui tous amongst North Sea red algal aliens. Only one species, Grateloupia doryphora, lacks any particular means of vegetat ive spread, while several of the aliens have specialized propagules or f ragmentat ion mechanisms. Unfortunately, temperature tolerances have been invest igated for less than half of the species, even though these are probably an important considerat ion for predictions of future spread. Finally, it is notable that many of the alien red algae in the North Sea contain ant i -grazing compounds. The high bro- mophenol content of many members of the Ceramiales (Fenical, 1975) may contr ibute to their invasive potential by deterr ing grazing sufficiently to permit es tab l i shment of an inoculum, and sometimes the deve lopment of a bloom.

The impact of exotic red algae on nat ive species is almost completely unknown.

Several of the North Sea aliens can become extremely abundant , part icularly the tetrasporophytic phases of Bonnemaisonia hamifera (Trailliella) and Asparagopsis ar-

R e d a l g a l exo t i c s on N o r t h S e a c oa s t 2 5 5

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256 C. A. M a g g s & H. S t e g e n g a

mata (Falkenbergia). T h e g r e a t e s t a b u n d a n c e of Trailliella is f o u n d on s e d i m e n t s in im-

p o v e r i s h e d c o m m u n i t i e s , so t h e r e is no o b v i o u s ef fec t on na t ive a lgal s p e c i e s . H o w e v e r ,

w h e n Trailliella a n d Falkenbergia are ep iphy t i c , t h e y mus t af fect p h o t o s y n t h e s i s of the

s p e c i e s on w h i c h t h e y a re g r o w i n g , a l t h o u g h a n y po ten t i a l ef fect has n e v e r b e e n eval -

ua t ed . T h e majo r i ty of t h e a l iens f avour art if icial s u b s t r a t a in m a n - m a d e hab i t a t s , s u c h

as m a r i n a s a n d h a r b o u r s , a n d t h e r e f o r e do no t i mp ac t on n a t u r a l c o m m u n i t i e s . Overal l ,

t he e f fec t of i n t r o d u c e d r ed a l g a e in t he N o r t h Sea has b e e n to i n c r e a s e s p e c i e s r ich-

ness .

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