'' BULLETIN DE L'INSTITUT ROYAL DES SCIENCES NATURELLES DE BELGIQUE, BIOLOGIE, 75: 8 I- 87, 2005 BULLETIN VAN HET KONINKLIJK BELGISCH INSTITUUT VOOR NATUURWETENSCI-IAPPEN, BIOLOGIE, 75: 8I-87, 2005

A new species of Caulibugula (Bryozoa: Cheilostomatida) from France

by Hans DE BLAUWE

Abstract MATERIAL EXAMINED

A new species of the genus Caulibugula (C. arcasounensis sp. nov.) Holotype is described from the Bay of Arcachon (France) and compared with A colony stored in alcohol (KBIN n° 30481 ), August I I, other species. 2003, collected on pontoons at Arcachon, east of Quai De Goslar. Key words: Bryozoa, Caulibugu/a, taxonomy, France. Paratypes Several colonies stored in alcohol (KBIN n° I. G. 3048 I), Resume August I I, 2003, collected from between drifting seaweeds at Arcachon, north of Quai De Goslar. Une es pece nouvelle du genre Caulibugula (C. arcasounensis sp. nov.) est decrite du Bassin d' Arcachon (France), et comparee avec d'autres especes. Other material Two ancestrulas with succeeding zooids, marginal vesicles, Mots-des: Bryozoa, Caulibugula, taxonomie, France. branch with ovicellated zooids, fans with pseudo-ancestrula, all stored dry and coated for SEM., August 11, 2003, col­ lected from between drifting seaweeds at Arcachon, north of Introduction Quai De Goslar. (KBIN no I.G. 30297)

Presently 28 species of Caulibugula are known around the ETYMOLOGY world, especially in warmer waters, some species may be in­ vasive taxa outside their native range. The new species With reference to the type locality, Arcachon. Arcasoun is the Caulibugula arcasounensis, hereby described, extends the Celtic name for resin pot referring to the nearby pinewoods di stribution of the genus to the coast of Europe. The new spe­ from which the name of the village is derived. cies was probably introduced with shellfish import. Pres­ ently, its known distribution is the Bay of Arcachon, a centre DIAGNOSIS of aquaculture at the Atlantic coast of France. Stalk-kenozooids with lateral thickenings. Branch zooids Bugula-like, with 0-1 spine on inner and 0-2 spines on outer Systematics di stal corner. Spines jointed or replaced by a triangular sharp point. Bifurcation of type 4 (HARMER, 1923). Pseudo­ Order Cheilostomatida ancestrula a turbinate autozooid, opesia in distal half with a Family Bugulidae GRAY, 1848 slit-like proximal prolongation, bordered by 5 jointed spines, Genus Caulibugula VERRILL, I 900 2 at one side, 3 at the opposite. Avicularia common , attached proximal to the zooids. Ancestrula with 6 spines, first suc­ ceeding zooid bearing also 6 spines. Caulibugula arcasounensis sp. nov. ' .. (Figs. 1-10) DESCRIPTION

TYPE LOCALITY Colonies attached with rootlets to various substrates. Colony erect, 2-3 em in height consisting of very slender stalks with Atlantic coast of France, Bay of Arcachon, Lat.: delicate Jlabellate branches of zoo ids arising at the distal end 44°39 '28"N, Lon .: OI 0 08'34"W, collected on pontoons and of some stalk-kenozooids. The pseud o-ancestrula is continu­ on piles in the shall ow sublittoral. ous on the last stalk-kenozooid . The stalk may continue with II 82 HANS DE BLAUWE

Plate 1 Fig I. Fan of a colony (KB IN n° l. G. 30297) Fig 2. Fan of a colony (KB IN n° l.G.30297) Fig 3. Close up of zooids (KBIN 11 ° l.G.30297) A new species of Caulibugula (Bryozoa: Cheilostomatida) from France 83

a side-branch. Stalk-kenozooids about 1.4 mm long or is a kenozooid with 3 short spines at each side of the opesia shorter, slender, with lateral thickenings. The proximal end (LI U, 1985). In the new species, the outer distal corner of the of the stem gives rise to rootlets. In·egular tubular vesicles zooids is strongly angulated and the pseudo-ancestrula is a with a white content occur single or in groups on the rootlets zooid with 5 spines around the opesia. but are rare. Bifurcation of type 4, tufts about 3 mm long In Caulibugula occidentalis (ROBERTSON, 1905) from the originating from a pseudo-ancestrula. Branch zooids are eastern Pac ific, the stalk-kenozooids grow noticeably shorter Bugula-like with the opesia occupying almost the complete towards the distal end of the stalk. A kenozo6id from the frontal surface. Branch zooids are biserial, alternate, zooids lower part of the stalk is twice as long and twice as thick of bear distal spines; 0-1 on the inner corner, 0-2 on the outer those of the upper part of the stalk; this is not the case in the corner. If the outer corner bears two spines, then one ori gi­ new species. The pseudo-ancestrula of C. occidentalis is not nates on the corner, the second spine is placed a little bit to described, but figure 73 of ROBERTSON (1905) shows a the middle of the distal border of the zooid. Spines are jointed pseudo-ancestrul a with 5 spines, as in the new species. Zo­ at their base, they may be as long as four zooids. The spines oids of C. occidentalis are turned outward, the distal end is may be replaced by a triangular sharp poi nt. rounded with 2 or 3 outer distal spines and I inner distal Pseudo-ancestrul a turbinate, with the opesia in the distal half spine. In C. arcasowzensis the zooids are hardly turned out­ and a slit-like proximal prolongati on, bearing 5 jointed ward, the distal corners are strongly angulated and the outer spines, 2 at one side, 3 on the other side. The pseudo­ corner bears no more than 2 spines. ancestrula has in some specimens a polypide or a brown Caulibugula zan zibariensis (WATERS , 19 13), from the West body, which means it is not a kenozooid but a zooid. Indian Ocean and also occurring in Chinese Seas (Llu, The avicularium is attached prox imally on the zooid on a tu­ 1985), has a pseudo-ancestrula with sometimes a slit-like bercle on the outer lateral gymnocyste. The avicul arium is of prolongati on surrounded by a variable number of long the bird 's head-type, about 125 f.Un long, the head not very spines: 9-11 (WATERS , 1913), 8 or more (HARMER, 1926); convex. The position is invariable and every zooid (except opposed to 5 spi nes in the new species. Polypide with 14- 15 zooids E and F in a bifurcati on) bears an avicul arium. tentacles while 12 in the new species. In C. zanzibariensis the Ovicells are attached by a short stalk to the inner di stal corner zooids have usually only one stout spine at the distal inner of the zooid. Embryos pale yell ow or white. Polypide with 12 corner and occasionally one at the outer corner. In the new tentacles. Ancestrula with 6 spines, first succeeding zooid species the zooids have one spine on the inner corner and 0-2 bearing also 6 spines. spines at the outer corner; spines may be replaced by a trian­ gular sharp point. DIMENSIONS In Caulibugula hastingsae (MARCUS, 1941) described fro m Brazil , zooids are distally twice as broad as proximall y, while Zooid length : 390 f.UTI , SD = SO f.Un , n = 40 in the new species zooids are Bugula-like. The pseudo­ Avicul arium length : 125 f.UTI , SD = 7 1Jll1, n = 14 ancestrula of C. hastingsae bears 6 spines opposed to 5 in the Pseudo-ancestrula length: 439 f.Un , 468 f.UTI , n = 2 new species. The zooid succeeding the ancestrula has 4 Ancestrula length : 690 fll11 , n = I spines around the opesia in Caulibugula hastingsae in con­ trast to 6 in the new species. In my opinion, the new species is cl osest related to C. Discussion hastingsae. Both species differ, however, in the amount of spines in the pseudo-ancestrula and in the first zooid suc­ Including the new species, the genus Caulibugula VERR ILL ceeding the ancestrul a. counts 29 species. Caulibugula arcasounensis is similar to C. californica (ROBERTSON , 1905), C. hastingsae (MARCUS, Before the di scovery of Caulibugula arcasounensis sp. nov. 1941) , C. irregularis (Ll u, 1985), C. occidentalis there were no recognised eastern Atlantic species from this (ROBERTSON, 1905) and C. zanzibariensis (WATERS, 1913) genus. Four species are known from the western Atlantic: C. in sharing a combinati on of the fo llowing characters: I) armata VERRILL, 1900; C. pearsei MATURO; 1966, C. stalk-kenozooids with lateral thickenings, 2) bifurcation type hastingsae (MARCUS , 1941) and C. dendrograpta (WATERS , 4, 3) zooids Bugula-like and/or bearing 1 inner and 2 outer 19 13). distal spines and 4) pseudo-ancestrul a with slit-li ke prolon­ For the comparison of C. arcasounensis with C. hastingsae gation. (MARCUS, 1941) see above. Caulibugula californica (ROB ERTSON, 1905) is known from C. armata and C. pearsei are two of the four species known the north-eastern Pacific. In this species the colony is at­ to possess type 5 bifurcations (MATURO, 1966); the other two tached to the substrate by a membranous rootlet-disc, the are C. exilis (MAC GILLIYRAY, 1890) known from Australia head of the avicul arium is very convex (LIU, 1985) and the and C. tuberosa HASTINGS , 1939 described from New Zea­ pseudo-ancestrula has onl y two spine-like processes without land. Other species as well as the new species possess type 4 joints at their base (LIU, 1990). The new species is attached bifurcati ons or the type of bifurcation is not determi ned. to the substrate by rootl ets, the head of the avicul arium is not Caulibugula armata VERR ILL ( 1900), descri bed from the raised and the pseudo-ancestrula bears 5 long spines, jointed Bermudas is a species that mi ght be in vasive. For example at their base. the species is very common in Fort Pierce (Florida, USA) onl y In Caulibugula irregularis (LIU, 1985) from China, the outer since about 1989 (pers. com. Dr. Jud ith E. WINSTON, YMNH di stal corner of the zoo ids is round and the pseudo-ancestrula Martinsville USA). The zooids of C. armata are di fferent '' 84 HANS DE BLAUWE

Plate 2 Fig 4. Pseudo-ancestrula and succeeding zooids (KBIN 11 ° I.G.30297) Fig 5. Pseudo-ancestrula and first pair of succeeding zoo ids (KBIN n° I. G.30297) Fig 6. Stalk-kenozooid (KBIN no I.G.30297) I I

A new species of Caulibugula (Bryozoa: Cheil os tomatida) fro m France 85

from the new spec ies in the fac t that they are turned toward waterway draining the Landes pl ateau. Coloni es \.vere at­ the middl e of the branch in such way th at the frontal areas of tac hed to wooden piles and pontoons near the marina of two neighbouring zooids form a nearl y ri ght angle with one Arcachon (east of Quai De Goslar). Presumabl y the new spe­ another. The zooids do not have di stal spines on the corn ers cies is qui et common in tidal pool s on oysters and wooden but only one spine may occur in the middle of the di stal mar­ piles in the bay, and consequentl y it is strange that the species gm. was not found earli er, as it is not small nor crypti c. The Caulibugula pearsei MATURO, 1966 is kn ow n from the present author had not the opportunity to check tid al pools in southueastern United States. Its pseud o-ancestrul a is spine­ the bay, but in 2003 sampl es were shown to local oyster less and is characteri zed by one to fo ur prox imal annul ati ons, fa rmers and to local scienti sts (Institut de Biologie Marine, a feature never seen in the new spec ies. The zooid s bear 0-4 Arcachon). Both affirmed that similar specimens are com­ spines depending on their posit io n in the fa n, opposed to 0-3 mon in ti dal pools. There is a lot of scientific research in cen­ in the new spec ies . As in C. armata the fro ntal areas of two tres of shellfish culture in Euro pe, but bryozoans are in vesti ­ neighbouring zooids form a nearl y ri ght angle with one an­ gated onl y sporadicall y or locall y. Dr. Jean-Loup o'HONDT other. (MNHN, Pari s) took observati ons on Bryozoa in the bay in C. dendrograpta (WATERS, 1913) described from Zanzibar, May 1994 and did not report Caulibugula. This does not is widely di stributed in wa rmer waters, occurring on the east­ mean th at the new species was absent, since full grown colo­ ern Atl anti c coast as far north as Cape Lookout , North Caro­ ni es mi ght perhaps appear by August. The present author too lin a (MATUR O, 1966). Furthermore · the species is also did not find Caulibugula arcasoun ensis in April 2002. One re ported from China (LI U, 1985), Australi a and Hawa·i. colony was coll ected in August 2001 and some more in Au­ Although the opes ia generall y exceeds half the zooid length , gust 2003. In August 2003 tens of loose coloni es dri fted the zooids of C. dendrograpta look Bicellariella-like in be­ as hore on the beach north of Quai De Gos lar, indicating th at in g ra ther strongly curved out ward with a di stal gro up of 3-4 the spec ies must be quite common. di stal outer spin es, 1 di stal medi an spine and I inn er spine It cannot be rul ed out that Caulibugula arcasoun ensis is an near the middle of the opes ia; while the zoo ids of C. endemic species, but give n the absence of any other Euro­ arcasounensis are Bugula-like. pean member of the genus, it is tempting to conclude this The pos iti on of an avicul arium is, if present, situated on the might be another alien species. Most likely cun·ent vectors of prox im al gymn ocyste in all spec ies except for C. introd ucti on of marine spec ies in Europe are: ballast water, dendrograpta . In C. dendrograpta the avicul arium is at­ hull foulin g and aqu ac ulture (MI NC HI N & GOLL ASCH, 2002). tac hed near the prox im al end on the lower zooids of a fan, Ball ast water can be rul ed out as vector of introducti on in the while progressively more di stall y on the nex t few zoo ids and Bay of Arcachon as there is no intercontinental nor coastal on the di sto-l ateral corner of all succeeding zooids. The shipping in thi s region. pseudo-ancestrul a of C. dendrograpta has an opes ia a little Hull fo uling could be a possible route of secondary introduc­ more than half the length of the fro ntal surface, sometimes ti on to the marin a of Arcachon. Marinas on the Atl antic coast with a slit-like prolongati on surrounded by a variable of France and the southern bi ght of the North Sea have a number of spin es: 8 (WATERS, 191 3), 6-8 (MATUR O, 1966) or faun a with a typi cal exoti c character. Exampl es of these 10- 12 (HARMER , 1926) opposed to 5 spines in the new spe­ exoti cs are give n in d'UDEKEM o' Acoz et al. (2005). Many Cies . of these species are found fo r the first time near harbours with intensive intercontinental shipping or near centres of Some species have been descri bed havin g a pseud o­ shell fish culture (pers. observati ons). Furthermore, some of ancestru1 a with a slit-like prolongati on in the opesia, but in the newcomers are rapidly spreading to marin as on the onl y 4 species the pseudo-ancestrula has the same morphol­ neighbouring coast using hull fo uling as vector of introduc­ ogy. In C. arcasounensis, C. dendrograpta, C. hastingsae ti on (pers. observations) . and C. zanzibariensis the slit-like prolongati on is abrupt and Likewise Bryozoa ariive in marinas as (secondary) introduc­ very narrow, the spines are not bil ateral, except for C. ti ons via ship 's hulls. Bugula simplex (HI NCKS , 1886) was hastingsae (3-2 in the new species, 6-4 in C. zanzibariensis, fo und fo r the first time in the Bay of Arcachon in May 1994, 5-3 in C. dendrograpta and 3-3 in C. hastingsae). In C. onl y at the mos t oriental part of the marin a (D 'HONDT & californ ica and C. occidentalis the opesia of the pseudo­ CAZAUX , 1994). This species was still prese nt with 3 colo­ ancestrula is not descri bed and the slit-like prolongati on in C. nies at the same locati on during my visit in April 2002. An­ irregularis is clearl y different, the opesia is proximall y nar­ other recent immi grant in Europe, Tricellaria inopinata rowing evenl y. D' HONDT & OCC HI PINTI AMBROG I, 1985 , has successfull y coloni zed most of the marin as at the Atlanti c coast of France, Belgium and the Netherl ands and is in some pl aces Occurrence spreading into the shall ow sublittoral (DE BLAUWE , 2002). Tricellaria inopinata was observed in the marin a of Caulibugula arcasounensis sp. nov. is presentl y only kn own Arcac hon and on the pontoo ns east of Quai De Goslar during fro m its type locality, the Bay of Arcachon, an inl and tidal my visits in August 200 I , April 2002 and August 2003, and sea of 155 km2, at low tide revealing 11 5 km2 of mud-fl ats was not found in other pl aces in the Bay. Although thi s spe­ and a network of ti dal-c hannels. The bay was formed during cies is the most comm on bryozoan in the marin a, it was not the Quatern ary peri od by the movement of coastal sediments yet fo rme rl y reported fro m thi s locati on. transform ing the es tu ary of the Ey re, the onl y signi ficant Tricellaria in opinata and Bugula simplex are typi call y fo und II 86 HANS DE BLAUWE

Plate 3 Fig 7. Ancestrula and succeeding zooids settled on zooids (KBIN n° I. G.30297) Fig 8. Zooids and ovicell s (KB IN n° I. G.30297) Fig 9. Avicul arium (KB IN n° I. G.30297) Fig 10. Rhizoid and vesicles (KBIN n° I. G.30297) '' A new species of Caulibugula (Bryozoa: Cheilostomatida) from France 87 in marinas, the former species is now also spreading into the References shallow sublittoral of some other marinas. In spite of inten­ sive search C. arcasounensis sp. nov. was not found in the DE BLAUWE, H, 2002. Determinatie en verspreidi ng van Tricellaria marina of Arcachon, nor in other marinas along the Atlantic inopinata D' HONDT & OCCHIPI NTI AMBROGI (Bryozoa, and Mediterranean coast of France, the English Channel and Cheilostomati da), een recente immi grant uit het noorden van de the southern bight of the North sea, so introduction in the bay Stille Oceaan. Het Zeepaard, 62:3, p '73-88. by hull fouling is not likely. HARMER, S.F., 1923. On Cellularine and o t~e r Polyzoa. Journal of The new species was found in tidal pools in a centre of oyster the Linnean Society, 35: 293-36 1. culture bringing us to a more likely route of introduction to HONDT, J.-L. o', 1984. Un nouvel immigrant dans le Bassin the Bay of Arcachon: import together with shell fis h. d' Arcachon, Watersipora aterrima (ORTMANN, 1890) Between 1964 and ca 1980 the Japanese or Pacific oyster (Bryozoaires, Cheilostomes). In : I 09° Congres national des socie­ Crassostrea gigas (L.) was imported to Europe on a large ti es savantes, Sciences, 2, Dijon. Ministere dei'Education nationale, Pari s (ed.): 237-245. scale from Japan, British Columbia in Canada and the NW Pacific coast of the USA (WOLLF & REISE, 2002). The HONDT, J.-L. o' & CAZAUX, C. , 1984. Presence de Bugula simplex bryozoan Watersipora aterrima (ORTMANN, 1890) was intro­ (HINCKS, 1886) (Bryozoaires, Cheilostomes) dans Je Bassin d' Arcachon. Bulletin de Ia Societe Linneenne de Bordeaux, 22 (3): duced in the Bay of Arcachon wi th Crassostrea gigas be­ 141-143 . tween 1968 and 1973 (o ' HONDT, 1984) and settled on Fucus serratus at "LaVigne" along Cap Ferret. "Later, all avail able LI U, X., 1984. On the species of fa mily Bicellariellidae (Bryozoa) fro m the Chinese seas. Studia marina sinica, 22: 255-314. substrates got covered with Crassostrea gigas and the alien sea-weed Sargassum muticum (YEN DO) FENSHOLT appeared LI U, X. , 1985. On genus Caulibugula Verrill , 1900, collected fro m and replaced Fucus serratus. As a consequence \¥. aterrima the Chinese Seas. Sw dia marina sinica, 25: 127-151. disappeared again from the settlement place (o'HONDT & LIU, X., 1990. Three new cheilostome bryozoans from the coast of CAZAUX, 1994). Shandong and Zhej iang Provinces. Studia marina sinica, 31: 12 1- As Caulibugula arcasounensis sp. nov. has onl y been found 128. in the Bay of Arcachon, a centre of aquaculture, it is tempting MARCUS, E., 1941. Sobre Bryozoa do Brasil. Boletim da Faculdade to conclude this would be yet another introducti on with Japa­ de Philosophia Sciencias e Len·as. Universidade de Sao Paulo Zoologia, 5: 3-208. ' nese oysters (Crassostrea gigas). Oyster import is indeed considered to be an important vector for the introduction of MAC GI LLI YRAY, P. H., 1890. Description of new, or littl e-known, alien species in Europe (WOLLF & REISE, 2002). The find ing Polyzoa Part XIII. Proceedings of the Royal Society of Victoria (n.s.), 2: I 06-110, pis 4,5. of the new species in the Bay, but not in the marina, supports the theory of introducti on with shell fi.sh. If the new species MATURO, F. J. S. , Jr. ,J966. Bryozoa of the southeast coast of the was endemic, it is strange that it did not coloni ze the wooden United States; Bugulidae and Beanii dae (Cheilostomata: Anasca). Bullet ill. of Marine Science, 16(3): 566-583, 18 text-figs. piles nor other substrates in the marina. If exoti c, it is likely that the marina and ship hulls will be colonized in the future MI NCHI N, D. & GOLLASCH, S. , 2002. Vectors - How exotics get and that this will lead to secondary introducti ons in other ma­ around. In: Leppakoski , E., Goll asch, S. & Olenin , S. (eds). Inva­ sive aquatic species of Europe. Distribution, impacts and manage­ rinas. Although there are no more intercontinental importa­ ment. Kluwer, Dordrecht, p. l83-191. tions of oysters in Arcachon, large quantities of shellfish are still being transported from one culture to another. For exam­ ROBERTSON , A. , 1905. Non-incrusting cheil ostomatous Bryozoa of the west coast of No rth America. Proceedi11.gs of the California ple, there is an exchange of oysters between Arcachon, Ire­ Academy of Sciences, Zoology, 2(5): 235-320, pis 4-16. land and Sete (Mediterranean coast of France) (BACHELET, G., Station MarineArcachon, pers. comm.). It is possible that UDEKEM D' ACOZ, D', C., M. FAASSE, DUMOULIN E. & H. DE BLAUWE, 2005. Occurrence of the Asian shrimp Palaemon the new species has been or will be introduced from or to macrodactylus in the so utl~ern bight of the North Sea, with a key to those places. the Palaemonidae of north-western Europe (Crustacea: Decapoda; Caridae). Nederlandse Faunistische Mededelingen, 22: 95- 111. WATERS, A. W., 19 13. The marine fauna of British East Africa and Acknowledgements Zanzibar, form coll ections made by Cyril Crossland, M.A., B. Sc. , F. Z. S. , in the years 1901-1902. Bryozoa- Cheilostomata. Zoologi­ Marc TERMONT is acknowledged for his research to the ori­ cal Society of London, Proceedings, 1913: 458-537, pis LXIV­ gin of the name of the vill age of Arcachon. The SEM photo­ LXX II I. graphs were taken by Julien CILLIS (lnsti tut royal des Sci­ WOLLF, W.J. & REIS E K. , 2002. Oyster imports as a vector for the ences Naturelles de Belgique). introducti on of alien species into northern and western European coastal waters. In : Leppakoski, E. , Gollasch, S. & Olenin, S. (eds). In vasive aquatic species of Europe. Distribution, impacts and man­ agement. Kluwer, Dordrecht, p.l93-205.

Hans DE BLAUWE Watergang 6 8380 Duclzele, Belgium E-mail: cleblauwehans@ hotmail.com