Vegetative and reproductive development of Laurencia venusta (Ceramiales, Rhodophyta)

Cryptogamie, Algal., 2000, 21 (2): 97-110 0 2000 Adacll?ditions scientifiques et mCdicales Elsevier SAS. Tous droits r&ervCs S0181156800001094/FLA

Vegetative

97

and reproductive development of Lauren&z venusta (Ceramiales, Rhodophyta)l

Ki Wan NM*,

Han Gil CHOI”, SoonjeongLEE”, Eun Jeong PARKa, Kyong Hwa KANG” & Yong Sik KIMb

a Department of Marine Biology, Pukyong National University Nam-gu, Pusan 608-737, Korea b Department of Marine Living Resources,Kunsan National University, Kunsan 573-701, Korea (Received 2 September1999, accepted 19 January 2000)

- The previously unknown vegetative and reproductive development of Laurencia venustaYamada (Ceramiales, Rhodophyta) were studied based on specimens collected from Korea Abstract

and Japan. Each vegetative axial segment bears a trichoblast and four pericentral cells; the first of the latter is always produced below the basal cell of the trichoblast; the second pericentral cell is formed at some distance from the first, followed by the third and fourth pericenh-al cells in an alternating sequence. Spermatangial branches are produced from one of two laterals on the suprabasal cell of a trichoblast in cup-shaped spermatangial pits. The procarp-bearing segment of the female trichoblast has five pericentral cells, of which the fifth becomes the supporting cell of the carpogonial branch. Mature cystocarps are ovoid with a non-protuberant ostiole. Tetrasporangia, with two pre- and one post-sporangial cover cells, are produced abaxially from the existing third and fourth pericentral cell, or occasionally only the fourth pericentral cell, and are parallel to the stichidial axis. Two pre-sporangial cover cells are aligned transversely to the stichidial axis in surface view. These features confirm the placement of L. venusta in the revised Lauren& Lamouroux. Laurencia venustais characterized by a loosely intricate, small thallus without percurrent axis, numerous holdfasts from the creeping and coalesced basal branches, and abundant medullary lenticular thickenings. Furthermore, it seems to be distinct from other species in having a sing!e, comparatively large (2&3Opm diam.) corps en cerise per epidennal cell. 0 2000 Adac/Editions scientifiques et medicales Elsevier SAS anatomy I Laurencia venustaI morphology

I Rhodophyta

I taxonomy

R&urn6 - DCveloppement reproductif et v6gktatif de Luurencia venusta(Ceramiales, Rhodophyta). Le dCveloppement de l’appareil vtgCtatif de LaurenciavenustuYamada (Ceramiales, Rhodophyta) et celui de son appareil reproducteur, inconnus jusqu’g p&sent, ont Btt CtudiCs B partir de spCcimens rCcolt& en Co&e et au Japon. Chaque segment axial vCgCtatif Porte un trichoblaste et quatre cellules pkricentmles ; la premikre de ces quatre cellules est toujours produite sous la cellule basale du trichoblaste ; la deuxiitme cellule pericentrale est formCe ?I une certaine distance de la premikre, suivie, suivant une disposition alteme, par la troisibme et la qua&me. Les rameaux males sont produits & partir de l’un de deux rameaux lat&aux situ& sur la cellule suprabasale d’un trichoblaste, ti l’int&ieur d’une cavitC mdle en forme de coupe. Le segment du trichoblaste femelle portant le procarpe possbde cinq cellules pkricentrales. La cinquikme devient la cellule support du * Correspondence and reprints: [email protected] ’ This paper is dedicated to Professor Francis Magne to honour his 75th birthday.

98

K.W. Nam et al.

rameau carpogonial. Les cystocarpes matures sont ovoYdes, avec une ostiole non protuberante. Les tetrasporocystes, accompagnes par trois cellules qui les recouvrent, deux sit&es avant et une sit&e apres, sont produits de manibre abaxialle, soit a partir des troisieme et quatribme cellules pericentrales deja existantes, soit, occasionnellement, seulement a partir de la quatribme cellule pericentrale, et sont parallbles a I’axe des stichidies. Les deux cellules situees avant le sporocyste sont alignees transversalement par rapport a l’axe des stichidies observe en we superficielle. Ces caracteristiques confirment le placement de L. venustudans le genre Lauren& Lamouroux tel qu’il est maintenant defini apres sa revision. Laurencia venustu est caracterist par un thalle petit, lachement intrique et saris axe principal discernable, par de nombreux crampons issus des rameaux rampants et coalescents de la base, ainsi que par des tpaississements medullaires lenticulaires abondants. En outre, cette espece semble distincte des autres en ce qu’elle presente un unique corps en cerise, comparativement, grand (20-30 pm de diambtre), par cellule Cpidermique. (Traduit par la Redaction.) 0 2000 AdaclEditions scientifiques et medicales Elsevier SAS anatomie I L.uurencia

venusta I morphologie

I Rhodophyta

I taxinomie

INTRODUCTION The Luurencia Lamouroux (18 13) complex (Ceramiales,Rhodophyta) includes more than 150 species.Recent studieshave examined the fundamental vegetative and reproductive morphology of several species,from various localities in the world (Nam, 1990, 1994; Nam & Saito, 1990, 199la, 1991b, 1994, 1995; Nam & Sohn, 1994; Nam et al., 1991, 1994). Basedon this, OsmundeaStackhouse(1809), which had been a nomen rejiciendum as an earlier facultative synonym of Laurencia (Papenfuss, 1947), was resurrected (Nam et al., 1994). The subgenusChondrophycus Tokida et Saito in Saito (1967) was also elevated to generic status (Garbary & Harper, 1998). Therefore, the Luurencia complex now comprisesthe three genera, Laurencia, Chondrophycus(Tokida et Saito) Garbary et Harper and Osmundea.As a result, an examination of the species previously placed in Laurencia is required to confirm their generic position. Luurencia venusta Yamada (1931) was described initially from Japan, but has been subsequentlyreported from the western Pacific and Indian Ocean regions (Yamada, 1931; Cribb, 1958, 1983; Kang, 1966; Saito, 1967; Jaasund,1970, 1976; Zhou & Chen, 1983). This species is similar in habit to L. intricata Lamouroux, L. mariannensis Yamada, L. nidi$ca J. Agardh and L. chinensisC.K. Tseng, and is occasionally confused with them. In this paper, previously unknown vegetative and reproductive features of L. venusta are described, and its generic position is confirmed. Comparisonswith similar Laurencia speciesare made.

MATERIALS

AND METHODS

Data for this study were obtained from liquid-preserved and herbarium specimenscollected from Korea and Japan.Methods for microscopic examination are the same as those described in Nam & Sohn (1994). Measurements are given as length x diameter. Voucher specimenshave been depositedin Herbarium of Department of Marine Biology, Pukyong National University (formerly National FisheriesUniversity of Pusan), Korea.

Morphology

of Laurencia

venusta (Rhodophyta)

Figs l-6. Laurencia venusta Yamada. Fig. 1. Details of male branches (N860024). Fig. 2. Habit of tetrasporangial plant (N860012). Fig. 3. Herbarium mounted female plant (N860024). Fig. 4. Details of female branches with cystocarps (arrowhead) (N860024). Fig. 5. Details of tetrasporangial branches (N860024). Fig. 6. Habit of male plant (N860021).

100

K.W. Nam et al.

Details of the examined specimensare asfollows: SAP (Sapporo) 13873(type; type locality: Kyushu, Japan). Korea: Sungsanpo (Num, 21 .v. 1985, N8600228 $; Num, ?.viii.1985, N860202@; Num, 19.vi.1986, N860023@, N860024@q), Ilgwang (Num, 2.5.ix.1983, 860021@6 9, N860020@; Num, 23.x.1983, N820905-820913@, N830116@, N831019-831022), Tong baeksum, Pusan (Num, 6.xi.1982, N860017@), Yonhwado (Num, 24.i.1985, N860010@, N860009 sterile; Num, ?.x.1985, N860012860013@6), Sohuksando (Num, ?.viii.1982, N860019@ sterile), Hojangdo (Num, 18.viii.1983, N83 1018@), Samchunpo (Num, ?.v.1984, N860018@), Tolsando (Num, ?.iv.1983, N831017), Pohang (Num, 28.vi.1986, N860014@), Taedongbaedong near Pohang (Num, 14.vii.1984, N860016d), Kanggu (Num, ?.vi.1986, N860015 sterile), Yongdeuk near Pohang (Num, 14.vii.1986, N860025@), Sinsudo (Nam, 24.x.1984, N860204 sterile; Num, 22.xi. 1984,N860203 6 sterile; Num, 22.xii. 1984, N860207 sterile; Num, 24.i.1985, N860205 sterile). Japan: Moheji (S&to, 27.viii.1962, S860505@; Suitu, 5.ix.1963, S860490@, S8604946, 27.viii.1963, S8604959, S860499CB; Suito, S860498@; Suite, 13.ix.1963, S8604910, S8604938, S860496@, S860503 sterile, S860504G3;Suite, 3O.ix.1963, S860497@, S860500@,S860502@), Takarashima(Suito, 30.v.1953, S860492).

RESULTS Luurenciu venustu grows on rocks in the lower eulittoral and hasbeen reported from Japan, Korea, China, Australia and Tanzania (Yamada, 1931; Cribb, 1958, 1983; Kang, 1966; Saito, 1967; Jaasund,1970, 1976; Zhou & Chen, 1983).

Habit Plants are 4 to 8 cm high (Figs 2, 3, 6), terete, occasionally slightly compressed, forming erect and loose clumps with intricate basalparts. Colour is usually brown, deep brown or purplish brown, with pink branch tips. Texture is subcartilaginous,adheringwell to paper. Thalli are attached to the substratumby numerousholdfasts from the creeping and coalescedbasalbranches,and are usually without percurrent axes (Fig. 2). Branching is irregularly alternate, subopposite or subverticillate, often fastigiately distichous in subcompressedparts of erect branches(Figs l-6). Ultimate branchlets are cylindrical or subcylindrical, with obtuseapices,0.4-0.6 mm in diameter.Male branchlets areturbinate, 0.9-l .Omm in diameter (Figs 1, 6). Tetrasporangialbranchletsare cylindrical or clavate, often slightly tapering toward the tip, usually compound,0.4-0.6 mm in diameter (Fig. 5).

Vegetative development The apical cell of branchlets successivelyproducesaxial cells through oblique divisions with three dividing faces. The resulting wedge-shapedaxial segmentsare arranged in a 3/8 spiral, clockwise or counterclockwise as seenfrom the apex (Fig. 7). The axial cell first obliquely cuts off a trichoblast initial at its upper end. Subsequently, the first pericentral cell is produced underneath the initial trichoblast, then the second pericentral cell is produced at somedistancefrom the trichoblast initial, followed by the third and fourth in an alternating sequence(Figs 7 and 8). In a given branch system, the

Morphology

of Luurencia

venusta (Rhodophyta)

Figs 7-15. Luurencia venusta Yamada (N860021). Fig. 7. Sequential development of axial segments. Fig. 8. Two superimposed vegetative axial segments. Fig. 9. Ordinary lateral branch on basal cell of trichoblast at initial stage. Fig. 10. Epidermal cells with secondary pit connections in surface view. Figs 11, 12. Development of secondary rhizoidal cortical cells on epidermal cells. Fig. 13. Epidermal cells with secondary pit connections in longitudinal section of branchlets. Fig. 14. Main branch in transverse section. Fig. 15. Secondary cortex in transverse section of main branch. See p. 107 for abbreviations.

102

K.W. Nam et al

spiral direction of the axial segmentsis always constant, probably being determined alternatively between branchlets and their parent branches. Each pericentral cell produces usually two, occasionally three to four, derivatives, each of which develops into determinate filaments that are radially arranged or occasionally in one plane. Each cell of a filament grows abruptly and considerably in size and forms secondary pit connections with adjacent cells, resulting in a compact pseudoparenchymatousstructure. This developmental processresults in a cylindrical or occasionally slightly compressedthallus with an inner condensedstructure. Young trichoblasts near the apical cell are monopodial, subdichotomously or alternately branched from the suprabasalcells (Fig. 26), and are displacedto the outside of the apical pit. Mature trichoblastsare shednear the periphery of the apical pit, resulting in scarsamongthe epidermalcells. The scars,however, are later buried by the overgrowth of epidermal cells. Ordinary lateral brancheswith indeterminate growth are initiated at the axils of the basal cells of trichoblasts in apical depression(Fig. 9). The developmental sequence of these branchesis the sameas above, but appearsto have a counter spiral system as comparedwith that of the parent branch. Adventitious branchletswith a subcortical origin occasionally occur in erect branches. Secondary cortication by rhizoidal filaments is usually observed in old branches (Figs 11 and 12). The resulting cortex develops more extensively at the base of the thallus (Fig. 15). Near the apex of branchlets, epidetmal cells project slightly, or not, and form lateral secondary pit connections (Figs 10, 13, 27). They are not palisadein transverse section (Fig. 24). Lenticular or occasionally annular thickenings are often found in the walls of medullary cells (Figs 14 and 15) but in somecasesthickenings do not occur at all. Corps en cerise occur in both epidermal cells and trichoblasts in live material, 1 per cell measuring20-30 pm in diameter (Figs 25 and 26).

Reproductive development Male branchlets have cup-shapedapical pits, which contain numerous male trichoblasts. The male trichoblast is derived from the axial cell near the apex of the branchlet (Fig. 16). Spermatangialbranchesare produced from one of two lateralson the suprabasalcell of the trichoblast (Figs 19, 20). The other lateral always remains as a sterile branch. The spermatangialbranchesproduce numerousovoid spermatangia,each with an apical nucleus, lo-12 x 5-7 pm, and terminate in a single large sterile cell, 25-35 x 24-28 pm (Figs 17, 18). Fully developed spermatangial pits are 500-700 x 230-250 pm. Procarps are produced from the second segment (suprabasalcell) of female trichoblasts in the apical pit of branchlets (Figs 28-30). In an alternating sequence,the suprabasalcell cuts off five pericentral cells, of which the fifth (with a somewhatadaxial position) always becomesthe supportingcell of the carpogonial branch (Figs 28-32). The supporting cell subsequentlyproduces a lateral sterile group initial, carpogonial branch initial and basal sterile group initial in the same order as that described for L. obtusa (Hudson) Lamouroux (Figs 29-32). The mature procarp has a four-celled carpogonial branch with a long trichogyne and the two lateral and basalsterile groups(Fig. 33). At this stage,the lateral and basal sterile groups have 9-l 1 cells and 4-6 cells, respectively. The post-fertilization process (Figs 23, 34-39) is essentially the same as that found in L. obtusa (Nam et al., 1994). The critical stageat which the diploid nucleus is transferred from the carpogonium to the auxiliary cell wasnot observed.After presumedfertilization, nuclear transfer seemsto take place by a direct contact between carpogonium and

Morphology

of Luurencia

venustu (Rhodophyta)

103

Figs 1627. Lmrencia Venus&r Yamada (N860021). Fig. 16. Young male trichoblast (arrowhead) in median longitudinal section of branchlet. Figs 17, 18. Young (Fig. 17) and mature (Fig. 18) spermatangial branches with terminal large vesicular sterile cells. Figs 19, 20. Mature male trichoblast with spermatangial (asterisk) and sterile (double arrowhead) branches on its suprabasal cell (arrowhead). Figs 21, 22. Abaxial development of tetrasporangium (double arrowhead) from pericentral cell (arrowhead). Fig. 23. Procarp after presumed fertilization. Fig. 24. Epidermal and medullary cells in transverse section of main branch. Fig. 25. Epidermal cells with corps en cerise in surface view of branch. Fig. 26. Young trichoblast with corps en cerise. Fig. 27. Epidermal cells with secondary pit connections in surface view. See p. 107 for abbreviations.

auxiliary cell. The sterile group cells attain a total of 25-35 cells in fully matured procarps. Mature cystocarps are ovoid without a protuberant ostiole, measuring 0.7-0.8 x 0.6-0.7 mm (Figs 4, 40).

104

K.W. Nam et al.

Tetrasporangiaare usually borne abaxially on the third and fourth, or occasionally only on the fourth pericentral cell near the apical pit of branchlets (Figs 21, 22, 41-43). Two pre- and one post-sporangialcover cells are produced from the stalk cell (fertile pericentral cell), respectively before and after formation of the tetrasporangial initial. The two pre-sporangialcover cells remain undivided, whereasthe post-sporangial cover cell continues to divide, forming a filamentous corticating system around the developing tetrasporangium (Fig. 41). The two pre-sporangial cover cells are arranged transversely to the stichidial axis in surface view (Fig. 44). Mature tetrasporangia are tetrahedrally divided, 75-86 pm in diameter, and show a parallel arrangementto stichidial axis (Fig. 45).

DISCUSSION Recently, Laurencia was separatedfrom Chondrophycus and Osmundeaby the combined features of four pericentral cells in the vegetative axis, epidermal pit connections, trichoblast-type spermatangial development, tetrasporangial production from particular pericentral cells, and the presenceof corps en cerise (Garbary & Harper, 1998, pp. 193, 194, table 4). By contrast, the production of two pericentral cells in the vegetative axis, the trichoblast-type spermatangial development (Nam et al., 1994), tetrasporangial production from pericentral cells, the production of additional tetrasporangial pericentral cells, and the absenceof corps en cerise are found in Chondrophycus (Garbary & Harper 1998). Osmundea has two pericentral cells in vegetative axis, spermatangial development of the filament-type (Nam et al., 1994), tetrasporangial production from random epidermal cells, a parallel arrangementof tetrasporangiaand no corps en cerise (Garbary & Harper 1998). More recently, however, these generic delineations were further refined (Nam, 1999). Laurencia is delimited from Chondrophycus and Osmundea by having four pericentral cells in the vegetative axial segment, spermatangial development of the trichoblast-type (Nam et al., 1994), and tetrasporangial production from particular pericentral cells. Chondrophycus is characterized by the combined features of two pericentral cells in the vegetative axial segment, spermatangial development of the trichoblast-type (Nam et al., 1994) and tetrasporangial production from particular pericentral cells. Osmundeahas two pericentral cells in the vegetative axial segment, spermatangialdevelopment of the filament-type (Nam et al., 1994) and tetrasporangial production from random epidermal cells. Luurencia venusta is placed in Laurencia (as defined by Nam, 1999) by its vegetative axial segmentwith four pericentral cells, spermatangialdevelopment in the trichoblast (trichoblast-type), and tetrasporangial development from pericentral cells as described above. Unlike earlier reports (Kylin, 1923; Hommersand, 1963; Saito, 1967), recent studieshave shown that many speciesof the Laurencia complex [except for 0. hybrida (A.P. de Candolle) Nam, C. intermedia (Yamada) Garbary et Harper, C. capituliformis (Yamada) Garbary et Harper, C. tumida (Saito et Womersley) Garbary et Harper, C. palisada (Yamada) Nam, C. dinhii (Masuda et Kogame) Nam (as Laurencia: Nam & Saito, 1994, 1995; Masuda & Kogame, 1998; Masuda et al., 1998a)] have procarpbearing segmentswith five rather than four pericentral cells (Nam, 1990, 1999; Nam & Saito, 1990; Nam & Sohn, 1994; Nam et al., 1994; Fujii & Cordeiro-Marino, 1996; Fujii et al., 1996). In L. venusta, five pericentral cells alsooccur in the fertile segment.The fifth pericentral cell, which is adaxially positioned, always acts as the supporting cell of a

Morphology

\

of Luurencia venusta (Rhodophyta)

f\ ’ P

105

40um 34-38

i IF’ 40 pm ~\

39

Figs 2840. Luurencia venusta Yamada (N860021). Figs 28-31. Sequential pryc.arpfc development before fertilization. Fig. 32. Sequential procarpic development before fertlhzatlon seen from branchlet apex. Fig. 33. Mature procarp before fertilization. Figs 34-39. Procarpic development after presumed fertilization. Fig. 40. Mature cystocarp. See p. 107 for abbreviations.

106

K.W.

Nam

et al.

carpogonial branch. Other procarpic structures, such as a four-celled carpogonial branch with a long trichogyne, two sterile groups (basal and lateral) and the post fertilization process, were essentially the same as those of other species of the Luurencia complex. However, the delayed formation of the auxiliary cell, which is found in some Chondrophycus species [C. cartilaginea (Yamada) Garbary et Harper, C. kangjuewonii (Nam et Sohn) Garbary et Harper and C. undulatu (Yamada) Garbary et Harper] (Nam & Saito, 1990; Nam & Sohn, 1994; Nam, 1999), was not observed in L. venusta. As originally described (Yamada, 193 I), L. venusta has a loosely intricate, small thallus without main leading branches, and has abundant lenticular thickenings in its medullary cell walls. Gross morphology of our specimens, except for the lack of the occasionally curved branches with secund ultimate branchlets, fits well with the type specimen (SAP 13873) (Yamada 1931, pl. 6, Fig. a). Since presence or absence of the curved branches is variable depending on habitat (Yamada, 1931), we refer our plants to L. vent&a. Some species with intricate thalli, including L. intricata and L. mariannensis, are similar to L. venusta in habit. However, the former species differs from L. venusta in lacking both lenticular medullary thickenings and secondary cortication by rhizoidal filaments (Nam, 1990). The fleshy soft thalli of L. intricata (Saito, 1967; Nam, 1990; Masuda et al., 1998b) distinguish it from L. venusta. Luurencia mariannensis (Saito, 1969; Masuda et al., 1998~) also differs from L. venustu in having fleshy soft thalli rather than subcartilaginous ones, and the conspicuous projection of epidermal cells near the branchlet apices. Refractive globular cell inclusions, which are known as corps en cerise and are considered to be a site of synthesis or storage of halogenated secondary metabolites (Young et al., 1980), have been reported in species of the Laurencia complex (Feldmann & Feldmann, 1950, 1958; Yoshida & Yoshida, 1974; Saito, 1982; Nam, 1990; GilRodriguez & Haroun, 1992; Masuda & Abe, 1993; Masuda et al., 1996, 1997a, 1998b; Abe & Masuda, 1998; Abe et al., 1998; Nam, 1999). Corps en cerise are usually easily observed in living epidermal and trichoblast cells. According to Garbary & Harper (1998), these intracellular structures are found only in Luurencia. However, their presence was reported in liquid-preserved specimens of a Chondrophycus species, C. parvipapillata (Nam, 1999). As previously mentioned (Nam, 1990; Masuda et al., 1998b), their number per epidermal cell may be useful in distinguishing some species of the Laurencia complex. While L. intricatu and L. mariannensis have, respectively, (1)2-3(4) and 2(3) corps en cerise per epidermal cell, only one per cell is found in L. venusta, as in many other species (Tab. 1). Also, their size in epidermal cells appears to be helpful in distinguishing L. venusta from L. intricata and L. mariannensis. While corps en cerise in L. intricata and L. mariannensis are 7-8 pm (in diameter) and 6-11 x 6-10 pm (in long x wide), respectively, in size, those of L. venusta are 20-30 pm in diameter. The size of the corps en cerise in epidermal cells ranges from 6 urn to 30 pm in diameter in the Laurencia complex (Tab. I). Based on these data, L. venusta seems to be distinct in having comparatively large corps en cerise, although a more critical evaluation of this feature is required. In some aspects, L. chinensis described from Hong Kong (Tseng, 1943) is also similar to L. venusta in gross morphology, but the former species differs from the latter in generally having a conspicuous percurrent main axis and a more or less distinctly compressed thallus. Luurencia venusta usually lacks the main leading branches and compressed thallus. Luurenciu nidifica (Saito, 1969) from Hawaii is similar to L. venusta in habit and anatomical features, especially the abundant lenticular thickenings. However, the former differs from the latter in having a coarse robust thallus. Cribb (1958) emphasized the shape of medullary cell wall thickenings, either annular or lenticular, as

Morphology of Lauren& venustu (Rbodophyta)

stk

Figs 41-45. Luurencia venustu Yamada (N860021). Figs 41, 42. Tetrasporangiai development in median longitudinal section of stichidium. Fig. 43. Tetrasporangial axial segment in transverse section near stichidium apex. Fig. 44. Mature tetrasporangium in surface view. Fig. 45. Mature stichidia with parallel arrangement of tetrasporangia. Abbreviations in Figs l-45. a, axial cell; ap, apical cell; au, auxiliary cell; bs, basal sterile group; bsi, basal sterile group initial; bt, basal cell of trichoblast; c, central cell of procarp-bearing segment; cb, carpogonial branch; cg, carpogonium; fp, fertile pericentral cell; fu, fusion cell; gi, gonimoblast initial; gl, gonimoblasts; se, conjunctor cell; Is, lateral sterile group; lsi, lateral sterile group initial; p, pericentral cell; pc, primary epidermal cells; po, postsporangial cover cell; pr, presporangial cover cell; sco, secondary cortex; sg, sterile cell group; sr, secondary cortical rhizoidal cells; stk, stalk cell; su, supporting cell; t, tetrasporangium; ti, trichoblast initial; tr, trichogyne; 1, 2 etc., formation sequence. a distinguishing feature of both species. By this feature, L. venusta can be distinguished from L. nidi$ca in showing the former shape, although only occasionally. However, a critical evaluation of this feature is also required, as both shapes are found in L. venusta. Young thalli of L. okamurae Yamada (Nam, 1990) are also somewhat similar to L. venusta. However, mature thalli of both species are readily discernible. The former has terete thalli with percurrent main axes and is usually greenish in colour, while the latter shows occasionally slightly compressed thalli without percurrent axes and is usually brownish in colour. Thus, L. venusta is characterized by its intricate small thalli without percurrent axes, numerous holdfasts from the creeping and coalesced basal branches, and abundant

K.W. Nam et al.

108 Tab. 1. Comparison

of corps en cerise found in Laurencia

Species

and Chondrophycus

Corps en cerise

Epidermal cells Number

Size (pm)

References

Trichoblast Number

species.

cells

Size (pm)

L. venusta

1

20-30

1

?

This study

L. okamurae

1

8-13

1

?

Nam (1990)

[“I

1

12.5-15.0

1

7.5-10.0

Masuda

et al. (1996)

L. composita

1

7.5-10.0

1

Masuda

et al. (1996)

L. nipponica

1

7-10

1

5.0-7.5 ?

L. japonensis

1

9-19

1

4-6

L. pinnata

1

8-15

1

?

L. brongniartii L. omaezakiana L. saitoi L. similis L. intricata

2 - (3)

(8-l

l-2

(2) (1M3 (1)2-X4) 1-

x 5-8)

Nam et al. (1991) Abe & Masuda Nan

(1998)

(1990)

1

(4-6 x 3-5)

lo-16

1

4-6

Abe et al. (1998) Masuda

6-12

1

4-10

Masuda

& Abe (1993)

6-10

1

2-3

Masuda

et al. (1997a)

(1997)

7-8

?

?

Nam (1990)

2-4

8-13

1

3*

Masuda

ef al. (1998b,

L. majuscula

2-3(4)

8-10

1

8-10

Masuda

et al. (1997b)

I”1 L. mariannensis

8-12

?

2 - (3)

x 6-10)

1

[“I

2-4 (6-11

(4-10

?

Masuda

et al. (1998b)

x 3-8)

Masuda

ef a/. (1998~)

[“l L. obtusa

1

7.1-8.6*

?

?

McDermid

1

IO-12

?

‘?

Nam (1990)

[“I I”1 [“I

1

?

?

?

Saito (1982,

1-3

?

?

?

Gil-Rodriguez

?

?

Maggs (1993,

(1988,

fig. 18)

fig. 8)

figs 7-9) & Haroun

1 - (2)*

7-12.5*

1 1

?

?

?

Gil-Rodriguez

& Haroun

L. viridis

6-8*

1

?

Gil-Rodriguez (1992, fig. 5)

& Haroun

C. parvipapillata

1

6.7-ll.l*

?

?

Nam (1999,

L. minuta

( ), long x wide;

?, unknown.

* Data obtained from jgures

(1992)

& Hommersand fig. 125B) (1992)

figs 33, 34)

in the papers.

lenticular thickenings in the medullary cell walls. Furthermore, it appearsto be distinct from other speciesin having a single, comparatively large corps en cerise per epidermal cell. Acknowledgements. We would like to thank Dr Y. Saito (retired from Hokkaido University, Japan) for providing the Japanese specimens and Dr T. Yoshida (retired from Hokkaido University, Japan) for allowing examination of the type of L. venustu. Thanks are also due to reviewers for their helpful comments and improving English. This study was supported by grant No. KOSEF 961-0509-072-I from the Basic Research program of the KOSEF and BSRI-99-5416.

Morphology

of Laurencia

venusta

(Rhodophyta)

109

REFERENCES ABE T. & MASUDA

Laurencia juponensis sp. nov. (Ceramiales, Rhodophyta). of Phycology 33: 11-24. MASUDA M., KAWAGUCHI S. & KAMURA S., 1998 - Taxonomic notes on Laurencia brongniartii (Rhodomelaceae, Rhodophyta). Phycological Research 46: 231-237. A.B., 19.58 - Records of marine algae from south-eastern Queensland-III. Laurencia Lamx. University of Queensland Papers, Department of Botany, 3: 159-191. A.B., 1983 - Marine Algae of the Southern Great Barrier Reef Part I. Rhodophyta. European

ABET., CRIBB CRIBB

M., 1998 -

Journal

Australian Coral Reef Society, Brisbane, Handbook No. 2, 173 p. FELDMANN J. & FELDMANN G., 1950 - Les 4 corps en cerise >> du Laurencia obtusa (Huds.) Lamour. Comptes rendus des seances de I’Academie des Sciences 231: 1335-1337. FELDMANN J. & FELDMANN G., 1958 - Recherches sur quelques Floridees parasites. Revue GtWrale de Botanique 65: 49-127. FUJI1 M.T., COLLADO-VIDES L. & CORDEIRO-MARINO M., 1996 - Morphological studies of Laurencia gemmtfera and Laurencia poiteaui (Rhodomelaceae, Rhodophyta) from the Nichupte Lagoon System, Quintana Roo, Mexico. Botanica Marina 39: 3 17-326. FUJI1 M.T. & CORDEIRO-MARINO M., 1996 - Laurencia translucida sp. nov. (Ceramiales, Rhodophyta) from Brazil. Phycologia 35: 542-546. GARBARY D.J. & HARPER J.T., 1998 - A phylogenetic analysis of the Laurencia complex (Rhodomelaceae) of the red algae. Cryptogamie, Algologie 19: 185-200. GIL-RODRIGUEZ MC. & HAROUN R., 1992 - Laurencia viridis sp. nov. (Ceramiales, Rhodomelaceae) from the Macaronesian Archipelagos. Botanica Marina 35: 227-237. HOMMERSAND M.H., 1963 - The morphology and classification of some Ceramiaceae and Rhodomelaceae. University of California Publications in Botany 35: 165-366. JAASUND E., 1970 - Marine algae in Tanzania II. Botanica Marina 13: 59964. JAASUND E., 1976 - Intertidal Seaweeds in Tanzania. University of Tromso, 160 p. KANG J.W., 1966 - On the geographical distribution of marine algae in Korea. Bulletin of Pusan Fisheries College 7: l-125, 12 pls. KYLIN H., 1923 - Studien ttber die Entwicklungsgeschichte der Florideen. Kungliga Svenska Vetenskapsakademiens Handlingar 63: 1-139. LAMOUROUX J.V., 1813 - Essai sur les genres de la famille des Thallasiophytes non articulees. Annales du Museum d’tiistoire Naturelle 20: 21-17, 115-139,267-293, pls 7-13. [Note: Also issued as an independently paginated book with an index and list of errata]. MAGGS CA. & HOMMERSAND M.H., 1993 - Seaweeds of the British Isles. Vol. 1. Rhodophyta, Part 3a. Ceramiales. HMSO Books, The Natural History Museum, London, xv+444p. MASUDA M., 1997 - A new species of Laurencia, L. omaezakiana (Ceramiales, Rhodophyta), from Japan. Phycological Research 45: 123-131. MASUDA M. & ABE T., 1993 - The occurrence of Laurencia saitoi Perestenko (L. obtusa auct. japon.) (Ceramiales, Rhodophyta) in Japan. Japanese Journal of Phycology 41: 7-18 MASUDA M., ABE T., SUZUKI T. & SUZUKI M., 1996 - Morphological and chemotaxonomic studies on Laurencia composita and L. okamurae (Ceramiales, Rhodophyta). Phycologia 35: 550-562. MASUDA M., KAWAGUCHI & PHANG S.M., 1997a - Taxonomic notes on Laurencia similis and L. papillosa (Ceramiales, Rhodophyta) from the western Pacific. Botanica Marina 40: 229-239. MASUDA M., ITOH T., MATSUO Y. & SUZUKI M., 1997b - Sesquiterpenoids of Laurencia majuscula (Ceramiales, Rhodophyta) from the Ryukyu Islands, Japan. Phycological Research

MASUDA

45: 59-64.

M. & KOGAME K., 1998 - A taxonomic study of the genus Laurencia (Ceramiales, Rhodophyta) from Vietnam. V. Laurencia concreta Cribb and L. dinhii sp. nov. Cryptogamie, Algologie 19: 201-212. MASUDA M., KOGAME K., ABE Y. & KAMURA S., 1998a - A morphological study of Laurencia palisada (Rhodomelaceae, Rhodophyta). Botanica Marina 41: 133-140.

K.W. Nam et al.

110 MASUDA

M., KOGAME K., ARISAWA S. & SUZUKI M., 1998b - Morphology and halogenated secondary metabolites of three Gran Canarian species of Luurencia (Ceramiales, Rhodophyta). Botunica Marina 41: 265-277. MASUDA M., KOGAME K. & KAMURA S., 1998~ - Taxonomic notes on Luurencia mariannensis (Rhodomelaceae, Rhodophyta). Phycologicczl Research 46: 85-90. McDERMID K.J., 1988 - Section V. Laurenciu (Rhodophyta, Rhodomelaceae) Introduction. In: Abbott LA. (ed.), Taxonomy of Economic Seaweeds, with Reference to Some Pacific and Caribbean Species Vol. 2, La Jolla, California Sea Grant College, University of California, pp. 221-229. NAM K.W., 1990 - Morphotaxonomic Studies of Genus Laurenciu (Rhodomelaceae, Rhodophyta). Unpublished PhD Thesis. Hokkaido University, Japan, 492 p., 49 pls. NAM K.W., 1994 - Vegetative and male reproductive anatomy of Lalrrenciu intercalaris sp. nov. (Rhodomelaceae, Rhodophyta) in Korea. Journal of Plant Biology 37: 421428. NAM K.W., 1999 - Morphology of Chondrophycus undulata and C. parvipupillata and its implications for the taxonomy of the Lauren&a (Ceramiales, Rhodophyta) complex. European Journal of Phycology 34 : 455468. NAM K.W., MAGGS C.A. & GARBARY D.J., 1994 - Resurrection of the genus Osmundea with an emendation of the generic delineation of Luurencia (Ceramiales, Rhodophyta). Phycologia 33: 384-395. NAM K.W. & SAITO Y., 1990 - Morphology of Luurencia cartiluginea Yamada (Rhodomelaceae, Rhodophyta). Bulletin of the Faculty of Fisheries, Hokkaido University 41: 107-120. NAM K.W. & SAITO Y., 1991a Anatomical characteristics of Luurencia pupillosa (Rhodomelaceae, Rhodophyta) from Guam and Palau. Micronesica 24: 87-94. NAM K.W. & SAITO Y., 1991b - Luurenciu similis (Ceramiales, Rhodophyta), a new species from Queensland, Australia. British Phycological Journal 26: 375-382. NAM K.W. & SAITO Y., 1994 - A re-examination of Luurenciu hybridu (Ceramiales, Rhodophyta) from the British Isles: vegetative and reproductive morphology. Phycologia 33: 3441.

NAM

K.W. & SAITO Y., 1995 - Vegetative and reproductive anatomy of some Luurenciu (Ceramiales, Rhodophyta) species with a description of L. maris-rubri sp. nov. from the Red Sea. Phycologia 34: 157-165. NAM K.W., SAITO Y. & SOHN C.H., 1991 - Vegetative structure and reproduction of Lauren& nipponica Yamada (Rhodomelaceae, Rhodophyta). Korean Journal of Phycology 6: 1-12.

NAM K.W. & SOHN C.H., 1994 - Laurencia kangjuewonii sp. nov. (Ceramiales, Rhodophyta) from Korea. Phycologia 33: 397403. PAPENFUSS G.F., 1947 - Generic names of algae proposed for conservation. I. Mudroiio 9: 8-I 7. SAITO Y., 1967 - Studies on Japanese species of Lauren& with special reference to their comparative morphology. Memoirs of the Faculty of Fisheries, Hokkaido University, 15: l-81. SAITO Y., 1969 - The algal genus Luurencia from the Hawaiian Islands, the Philippine Islands and adjacent areas. Pacific Science 23: 148-160. SAITO Y., 1982 - Morphology and infrageneric position of three British species of Luurenciu (Ceramiales, Rhodophyta). Phycologia 21: 299-306. STACKHOUSE J., 1809 - Tentamen marino-cryptogamicum. Memoires de la Societe’ Impe’riale des Naturalistes de Moscou 2: 50-97. TSENG C., 1943 - Marine algae of Hong Kong. IV. The genus Luurencia. Papers of the Michigan Academy of Science, Arts and Letters, 28: 185-208. YAMADA Y., 1931 - Notes on Luurencia, with special reference to the Japanese species. University of Calt$ornia Publications in Botany 16: 185-310. YOSHIDA T. & YOSHIDA M., 1974 - Corps en cerise found in Laurencia nipponica Yamada. Bulletin of Japanese Society of Phycology 22: 156-l 59. YOUNG D.N., HOWARD B.M. & FENICAL W., 1980 - Subcellular localization of brominated secondary metabolites in the red alga Laurencia snyderue. Journal of Phycology 16: 182-185.

ZHOU 2. & CHEN Z., 1983 -A

list of marine algae from Fujian coast. Taiwan Strait 2: 91-102.