Phyc ologia (1978) Volume 17 (4), 413-41 7

Janieae and Lithotricheae: two new tribes of articulated Corallinaceae (Rhodophyta)"

H. WtLLIAM JOHAN SEN AND P A UL C. SILVA

Biology Department , Clark University , Worcester, Ma ssachusett s 01610, U.S .A., and Department of Botany , Univers ity ofCalifornia, Berkeley , California 94720, U.S .A .

Evidence no w ava ilab le wa rra nts seg rega ti ng the genera of two su bfa milies of ar ticu lated Cora llinaceae ( Rhodo­ ph yta) into tribes. Wi thin the su bfa m ily Corallinoi deae, the Iribe Ja nieae (co mpri sin g Jan ia , Holip tilon, a nd ChcilasraJ"I1I ) is d istinguished from th e Coralline ae prim arily by thick, com pact ca rpo spo ro phy tic fusion ce lls bearing o nly marginal carpo sporangial fila ments, by male co ncepracles wit h na rrow ch ambers and short ca nals, and by a relatively sma ll n umber of spo rangia in each tetraspo ran gial co ncep rac le. W ithin the sub fami ly A rnphiroi­ de ae , t he tri be Lith otricheae (co m prising Only th e rnonotypic genus Lithothrix ) is d isti ng uished from the A m­ phiroeae on the basis of its un iq ue de velopmental pattern by wh ich lon g-celled gen icul ar tiers and sho rt-celled inter genicu la r tiers a lte rn ate regularly, eac h ma ture geni culum being co vere d by a cortex p rod uced by the in ter­ ge niculum dis ta l to it. In th e equally un ique A mphiroa , by contra st, alter nating gro up s of cortica red tier s, so me o f wh ich a re sho rt-celled a nd ot her s long-cell ed , remain calcified to fo rm inie rge nicu la or become decalcified to form gen icula . Halip tilon is sho wn to be the correct spelling an d to dale as a generic name from 1846 (Lindl ey). Halipt ilon cuvieri (La mou re ux) co m b. n ov. is designated lectotype.

Introduction Cora llino ideae The su bfa mily is cha racter ized by In rece nt years a sha rply increased interest in the genicula each co nsisting of a sing le un corticated and Co rallinaceae (R hodophyta) has bro ug ht fo rth a uncalcified tier of medulla ry cells an d by lateral cellular large bod y of new infor mation rega rding their fusi on s (rather than seco ndary pit-connections). structure and reproduct ion. This information, in The twelve gen era fall into two seem ingly natural turn, has evo ked interest in int rafamilial classifica ­ groups. , Haliptilon,t a nd Cheilospo rum form tion , Tw o schemes covering the en tire fam ily are the smaller of the two groups a nd a re distinguished those of Jo hansen (1969a, elabo rated up o n by Adey from the rem aining members of the subfamily & Johansen, (972) an d Cabioch (1971 , 1972), pr imarily by thick, co mpact ca rposporo phytic fusio n Difference s in the two schemes, which are d iscu ssed cells bea ring only ma rgina l corpos pora ngia l fila­ by Adey & Johansen, reflect the grea ter taxonom ic ments, male con ceptacles with narrow chambers and significance accorded to genicula by Johansen. In short ca nals, a nd a rela tively small nu mb er of the sc heme ut ilized in the pre sent paper, a ll a rticu­ sporangia In each tet rasporangial co nce p tacle. lat ed co ra lline algae a re distributed am ong three Ot her different iating characters, which appea r to be subfamilies : Metagonioli thoideae, comprising only of onl y seco ndary importa nce, are listed in Table 1. M etagoniolithon, a genus of un ique morphology ; We prop osed to esta blish the tribe Ja nieae to receive Corallinoideae, with twelve genera ; and Amphiro­ these th ree genera in contrast with the Co rallineae, ideae, comprising onl y a nd Lithothrix. Th e whi ch will ret ain the rema ining nine genera of geni culum probably evolved independently in eac h Co ralli noideae. of these three su bfam ilial lines. In the pre sent pa per the Corallino ideae an d Amphiroid eae are newly su b­ • Ded icat ed to Mrn e M a rie Lemo ine on the occ asion of her 90th birthday on 29 D ecem ber 1977 . divided into tribes. t See the nomenclatural not e a t the en d o f thi s pape r.

0031-8884/78/1200-0413 $02.00 ~: 1978 Blackwell Scientific Publications 413 414 Phycologi a, Vo l. 17 (4), 1978

T A BLE J. C ha ra cters d istinguishing C oralline ae fro m J an iea e

Ch aracte r Corallineae Ja nie ae

P rim ar y Carpos porophyti c fusio n ce lls th in ( ., 12 /-L m), expanded (90­ th ic k (up to 35 /-L lll ). compac t a nd ca rposporangial filamerus 300 /

Secondary Num be r of supporting cells per ma ny, 200 Iew, . 200 p rocarpic co nce pt aclc N u m be r of retrasporan giat ini­ man y, > 200 rials pe r conceptacle Paraphyses int er spersed among pres e nt abse nt tet rasporangia Tetraspores rela tively small, w ith thin m uc i­ relativel y lar ge, with thi ck laginous coat ing mucilaginou s coating Sp o re germination and resulting slow ; cru st ex tens iv e rap id : cru st reduced c rust Bra nch in g of mai n a xis pin nate o r d ich o to mous d ich o tomous Bra nc hes on tetrasporangia! rare pr esent in J ania a nd Hclipt llon co nce ptac les Heigh t of int e rge n icul ar medul­ sho rt (50- 90 I"m) long (80-170 /-L m ) lar y cells In fecti on by Chorconerna no yes

Janie ae trib, nov. R arn ificatio principali s dicho­ ( 194 1b) a nd Jo hansen (1 977). Some o f the seco nda ry to ma cellula coalescens carpos po rophyt ica usque ad cha racters listed in Table 1 require comment. 35 Jl m cr ass., et minus quam 130 ,um Iat.: co nc ep ­ Se ver a l difference s between the tet raspores o f tacu la rnascul a lon ga a ng us ta q ue, loculis 90 ad Coral/ina offic ina/is L. a nd th ose o f Ja nia rubens (L.) 250 I" m lat. , can a le m inus quam 120 f-

Calliarth ron by Segawa, 1941c, as Cheilosqr'gJm ; and A mp hiroideae in Coral/ina by G a nesa n, 1968). However, the T he subfamily Amp hiroideae as esta blished by universa lity of par aphyses in Co ra llineae remain s to Johan sen ( 1969a) is characterized by genicula each be dem onstrate d an d some studies, in fac t, have been consisting of one or more tiers of a t least partly negative. On the other ha nd, parap hyses ha ve never uncalcified or deca lcified medulla ry cells a nd by been reported for Janieae. secondary pit-connections (ra ther tha n lateral Of the three genera of Janieae, Hal iptiion and cellular fusion s). Tn add ition to the type genus Jania a re so closely relat ed that certain species may A mphiroa, it com prises Lithothrix , a monotypic be difficult to ass ign to o ne gen us or the othe r. genus long know n for its unusual mor phology. Haliptilon has pro minen t percurrent, often dichoto­ De ta ils o f the development an d structure of Litho­ mous axes with regular pinn a te bra nches origi na ting thrix have been supplied by Segawa (1947), Ganesan at the apices. All species of Jania are dichotom ous, & Desikachary (1970), Cabioch (1972), Chihara but so me (c .g . J. co rn icula ta (L.) Lamour.) have (1972), and Gittins (1975). Cabi och ( 1971, 1972), pinnate branches that appear to be accessory and stressing the similarity of the cru stose bases of perh aps may be interpreted as vestigial. Cheilo­ A mphiroa a nd L ithothrix to adu lt thalli of Litho­ spor um, with marginal rather than axial co nceptacles phyllum a nd Derma tolithon, respectively, placed the and pronounced intergenicular lo bes, stands at a two genera of articu lated cora llines in differen t clear phyloge net ic dista nce from both Ha liptilon and tri bes, namely, Arnphiroeae an d Der mat o litheae. In Jauia . Monographic studies are bad ly needed to what seems to us an incon sistency, however, she clarify the species of each of the th ree genera. recogn ized the Amphiroeae (with the single genus Und oubtedly man y species o f Haliptilon ha ve been A mphiroa) sepa ra te from the Lithophylleae (in which erro neously referred to Corollina becau se of their she included only crusto se members), while comb in­ pinna te bra nching without rega rd for their repro ­ ing crustose for ms with Lit hothrix in the Der mato­ ductive fea tures. litheae. We prefer to ascribe grea ter taxon omic im­ In connection with the Janieae, mention sho uld portance to the evolution of genicula by placi ng be made of the par asite Choreone ma, which infects Lithoth rix in its ow n tribe apart from the cr ustose only members o f this tribe. From what is known membe rs of Cabioch's D ermatolitheae. a bout red a lgal parasites, and especially corallina­ ceous parasite s such as Kvaleya (Adey & Sperapan i. Lithotriclieae Irib. nov. Meristerna apicale strata 1971) a nd Ezo (A dey, Masa ki & Akioka, J974), cell ularurn a lterne genicularia intergenicu lariaq ue it is possible to consider Choreonema a grea tly efficiens, cellulae st ra ti genicularis ma nifeste se redu ced ade lphop ar asite deri ved fr om a ncestral extendentes et part ibus in in ferioribus decal cifactae Janieae. factae ; cellulae strati inte rgenicularis no n extenden-

T A OLl~ 1. C ha racte rs distinguishin g A rnph iroea e f ro m Li th ot ri ch cae

Character Amphiroeae Lithotricheae Number of tiers of medullary one or (in most speci es) several one; cells elongating to as cells in genicula cells becomin g decalcified much as 600 ,..m but not elongating markedly Number of tiers of med ullary several on e cells in intergenicula Ratio of length of gen icular 1-1 as much as 40 cells to int er gen icu lar cells Origin of cortex from both genicula and inter­ from intergenicula only genicula Thickness of cortex several cells thick unis tratose (sometimes pro­ liferating with age) Calcined cortex covering geni­ none , or cracking awa y irregu­ inrergenicular co rt ex gro wing cula larly downover genicula

C rU ::H Ll ~ l,,: ba~L' ce lls ncu rly isod iu m c tr ic cell s elongate 416 Phycologia, Vol. 17 (4),1 978 I I

F IG. l. Lon gitudinal sec tion throu gh br a nch apex of Amphiroa bowerbank ii Har vey co llec ted a t Ken ton-on Sea, South Africa. Only intergenicular cells are present. The line is 100 I' m long. FIG. 2. Long itud ina l sec tion thr ou gh bra nch a pex o f L itltothrix aspcrgillum co llected in Sa nta Barbar a Co ., Ca lifornia. The lon g-celled tie rs a re genicula . T he line is 100 I' m lon g. FIG . J. The type specimen o f Hn liptilon cuvlcri, T he scale is 5 em long. tes, cellulae novas, autern, per me ris tem a ma rginale activity leaves the tiers in a su bapica l posiuon, ce r­ efficientes ; hae cellulae novae de or surn crescentes et tain of them elongate, forming a n irregul a r seq uence cellulas geniculares obtegentes ut hae se extendunl. of long and short tiers. Alt ernating groups o f tiers Genus typificum: Lithothrix J. E. Gray 1867. remain calcified to form intergenicul a or become Apical meristem producing a lternating genicul ar decalcified to form geni cul a (Joh an sen , ]969b). A a nd intergenicular tiers of cells; cells of gen icul ar cortex is produced aJl along the bran ch , becoming tier elongating markedly a nd becoming dec alcified decalcified when forming part of a geni culum. in lo wer parts ; cells of intergenicu lar tier not elo n­ In Lit'iothrix (Fig. 2), by contrast, two kinds of gat ing but producing new cells by a marginal regularly alternating tiers o f cells are pr oduced at meri stem, these new cells growing do wn wa rd a nd bra nch apices, one beco ming in terg en icula r a nd the coveri ng the geni cular cell s as the y elongat e. other ge nicula r. In the intergenicul ar tiers the cells The c ha racters that we ha ve used to d istinguish rem a in sho rt and calcified, with those a t the surface Amphiroeae from Lithotricheae a re summa rized in producing a downward growing co rtex. The cells of Table 2. Ca bioc h ( 197 1, (972) gives as a cha rac ter of the gen icula r tier, on the o ther hand, elongat e the Amphiroeae the germination of spo res (o f ma rkedly but do no t di vide fur ther, being covered by Amp hiroa) to form a filamentous j uvenile with in th e the intergeniculurn-derived co rtex. The distal parts tissue s o f other Corallinace ae. C hiha ra (J 972), o f the first-formed genicula r ce lls remain ca lcified, so however, obtained crusts when he germ ina ted spores tha t a ma tur e geniculum, defined as a n u ncalcified of three Japanese species in culture. Mo reover, for area between two intergenicula, is co mposed of o nly many species the ontogeny is not yet known . part of the genicular tier (Sega wa , 1947 ; Ganesa n & The ontogeny of the frond s o f Amp hiroa a nd Desikachary, 1970; Cabioch , 1972 ). Lithothrix are so striking compared with o ther articula ted Corallinaceae and at the same tim e a re so Nomenclatural note on Haliptilon different from each other that a summary o f eve nts This taxon was first established by Dec aisne ( 1842) seems appropriate. as Jania 'groupe' [i.e. section] Haliptylon, distin­ In Amphiroa (Fig. l ) tiers of medullary cells ar e guished from Jania proper by the pinnate branching pro d uced by apical meristerns with th ose dest ined of its members. Six species were assigned to the to beco me gen icula not di fferentiate d unt il they a re gro up: J, elegans Deca isne (no men nudum), J. su bapical. When in itiated, each medul lary tier is cuvieri (Larnour.) Decaisne, J. po niculata (Lamour.) co mp osed of short cell s, but, as Fur ther mcristcrna tic D ccaisnc, J. crisp at a (Larnour.) Dccaisnc, J . ro sc a Johansen and Silva : Tw o new tribes of a rticulated Co rallinaceae 417

(Lama rck) Decai sne, a nd J. granife ra (Ell. et Sol.) CHIHAR A, M. ( 1972) [Reprod uctive cycles and spor e ger mina­ Decaisne. M ontagne (1845) added three speci es to tion of the Co ra llinaceae and their possible re levance in the systematics ( I). A mphiroa. M arginisponun a nd Lit ho ­ the gro up and used the co rrect spelling Haliptilon Ihrix .] .1. Jap , Bot ., 47, 239-249. (Japa nese with English J' (fro m ailrj, the sea , and 1T"ifli6v, a fea ther from summa ry). the under plumage of a bird .) (The co rrect spelling D£CAI SNE. J. (1842) Essai s sur une class ification des Algues et des Polypi ers calcif'eres de La mouroux. A nn. S c. Na t . had been used pre viou sly by Decaisne ill the 'Ta ble' BOI. , ser. 2, 17, 297-380 : 18, 96-1 28. a ppen ded to the the sis version of his 1842 pa per.) D UCKER, S.c.. LEfiLANC, J.D. & JOH ANSEN, H.W . (1976) A n ep iphyt ic species of Jania (Co rallina ceae: Rhodophyta) Joh ansen (1970) elevated the gro up to gene ric rank end emic to sout hern Au stra lia. Contrib . H erb. Austra!., 17, as Haliptylon (D ecaisne) Johan sen , but, wh ile sta ting 1-8 . that probabl y well Over 30 named taxa may be found GANESA N, E.K. (1966) Stu dies o n the mo rpho logy and repro ­ d uction of the a rticulated co rallines-l. Phyko s, 4, to belong to it, he explicitly assigned to it only 43-60, Corollina subulata Ell. et Sol., not o ne of Decaisne's G ANE SA N, E.K. (1968) Studies o n the mo rphology and rep ro­ du ction of the a rt iculated co rallines- II. Coral/ina Lin­ o rigina l species. U nknown to Joh an sen , ho wever , naeus emend . Lamoureux. Bol. l nst . Oceanogr. Univ. was the work by Lindley (1846, p. 25) in which he Ori ent e, 7, 65- 97. elevated Decaisne's gro u p to gene ric rank, correct ing GANESAN, E.K . & D ESI KA CHARY, T .V. (1970) St ud ies o n the morp hology and reproductio n of the articulat ed co ra llines the spelling to Haliptilon bu t not giving a descri ption - v. Lithotlirix G ray. Phykos. 9, 41-5 1 an d not listin g the included species. Thus, accred iting G ITTINS, B.T. (1975) The bio logy of L ithoihrix asperg illnm the generic na me to (Deca isne) Lin dley, we m ust JE. Gray (Corallinaceae, Rhod ophyta). Ph.D . th esis, Uni versity of Califo rnia. Irvine. select one of D ecai sne's o rigina l species as type . We HAMEL, G . & LEMOINE , M me. P. (1953) Corallinacees de hereby designate H aliptilon cuvieri (Lamouroux) France ct dAfriq uc du N ord. Ar ch. M us , Natl, Hist. Nat . [Pari s], ser. 7, 1, 17-13 6. comb. nov. (CorallinG cuvierl Lamoure ux, 1816, p. JOHANS EN, H.W. (1969a) Morphology an d sys tematics of 287, pI. I X : fig. 8) lect ot ype species. Th e holo type co ralline algae, with special reference to . specimen of Corallina cuvieri (F ig. 3) was collected VII i \'. Calif. Publ. BOI ., 49, i-viit+ ) - 78. JOHANSE N, H.W. (1969b) Patterns of genicu lar develop ment in A ustralia a nd is ho used in Herb. Lamour ou x, in A m phiroa (Co ra llinaceae). J. Phycol., 5,11 8-1 23. Laboratoire de Bot anique, F aculte des Sciences, JOHANSEN, H .W .(1970) The diagnostic value of reprod uctive Caen , Calvad os, F rance. o rgan s in some genera of ar ticulated co ralline . Brit. Pliyco t. .1. . 5, 79-86. JUHANSEN, H .W . (1977) T he arti cul ated Co ra llinaceae ( Rhodo ph yta) of South Africa : l . (D eca isne) Acknowledgements Za na rd ini. J. S AIr. s«, 43, 163- 185. JONES. W ,E . & l'vf oORJANI, S.A . (1973) T he att achment and We wish to thank Dr Phillip A. Lebednik for his ea rly develo pment of the tet raspo res of some co ralline red critical read ing o f the manuscript , result ing in help­ a lgae. Sp ec. Publ, Ma r Bioi. Ass . India, 239-304. LAMo uRoux. J .V.F. ( 18 16) Histoire des Polypiers cr ra /l ig~l1 e s ful suggestio ns, a nd Dr H a nnah Croasda le fo r fiex ibles, vulgairement nom mes Z oophytes. ..E. Pois son , prep aring the Latin diagnoses. Caen . LINDLE Y, J. ( 1846) The vegetable k ingdom . . . Lo ndon . MONTAGNE, C. (1845) Plates cellulaires. Voyage all Pale sud References et dans F'Oceanie sur les corvettes l 'Astrolabe cl io Zelee . . . Bot anique . 1, i-xiv + 1-34 9. ADEY , W.H . & JOHANSEN, H .W . ( 1972) Mor phology and SEGAW A, S. (l94 Ia) [System at ic ana tom y of th e a rticulated taxono my of Co rallin aceae with specia l reference to corallines V. Amphiroa erelacea (Pos tels et Ru prech t) Cla tliro morplunn , M esophyllnm, an d Neopolypo rolitlton gen. End licher .].1. Jap , Bot ., 17, 348-355. (Ja panese with Engli sh nov. (Rhod ophyceae, C ry pto nern iales). Phyrolog ia. 11, sum mar y.) 159- 180. SEGAWA. S. ( 1941b) [Systematic anatom y o r the articulated ADEY , W . H., M ASAKI. T. & A KIOKA, H. ( 1974) Ezo epiye s­co rall ines. V l . Cheilos po ru m jungermonnioides ( Ru prec ht) soense, a new pa rasitic genus and species of Co rallinacea e Are schoug.] .1. Jap , Bot.. 17, 450-456. (Jap anese with (R hodo phyta, Crypton emiales). Phy ro logia, 13, 329-344. Engli sh surnrnary .) ADEY, \V.H . & SHRAPANf, c.r. (1971) Th e biol ogy of SEGAWA . S. ( 194 Ic) [Systemat ic anat o my of the a rticula ted Kvalcya epilaeve , a new par asitic genus and species of co ra llines, VIr. Clieilospo rum ye sso euse Yen do .] .1. Ja p , Co ra llinaceae. Pliy cologia, 10, 29-42. Bot., 17, 563-572. (Ja panese with English su mma ry.) CABIOCH, J. (1966) Sur le mod e d e for mat ion du th a lle SEGAWA , S. (1946) [Systematic anatomy of the art iculated articule chez que lqu es Corallinees, C. R. A cad. S c. [Paris], corallines, X. Jania radiate Yen do.] Seibuts u, 1, 15[-156. 263D, 339- 342. (Japanese with Eng lish surn rnary .) CAB IOCH, J. (1971) Essai d'u ne nouvelle classificat ion des SEGAWA, S. (1947) [Systemat ic anato my of the art iculated Co rallinacees actuelles. C. R. A cad S c. [Paris], 2720, corall ines. XL Lithothrix asp erg illnm G ray.] Se ibutsu, 2, 1616-1619. 87-90. (Japanese with Engli sh su mma ry.) C AB IOCH, J. (1972) Etude sur les Corallinacees, rr. La SUNESON, S. (193 7) Studicn uber die En twick lun gsgeschich te morphogenese: con sequ ence s systernatiq ues et phy lo­ der Cor all ina ceen . l. unds u»:« A rsskr. N. F. A vd, 2, genet iq ues. Cah. Bioi. M ar., 13, 137-288. 33(2) , 1- 101

(Accepted 19 Ma y 197 8)