New Zealand Journal of Botany, 1977, Vol. 15: 495-502. 495

Transfer of the New Zealand red alga Tylotus proliferus

(Gracilariaceae, Gigartinales) to the genus Gracilaria

GERALD T. KRAFT

School of Botany, University of Melbourne, Parkville, Victoria 3052, Australia

(Received 8 September 1976)

ABSTRACT

Reproductive material of Tylotus proliferus (Harvey) Kylin from the North Island ofNew Zealand has been examined and found to conform to the genus Gracilaria. Because thename Gracilaria prolifera Reinsch is in current use for an alga from South Georgia in thesubantarctic, the new name G. truncata is proposed, based on a prominent branch featureof the New Zealand species. Details of habit, vegetative morphology, and carposporophytedevelopment of G. truncata are presented. The so-called "nutritive filaments" which charac-terise this and many other species of Gracilaria are discussed, and substitution of the term•'traversing filaments" is suggested to avoid implying an unverified nourishment function ofthese structures. Some speculations on the possible relatives of G. truncata are made.

INTRODUCTION

The red algal genus Tylotus, based on T. obtusatus(Sonder) J. Agardh from southern Australia, has,since its inception, been associated with Gracilariaand related genera (J. Agardh 1876, p. 395; De Toni1900, p. 462: 1924, p. 272; Schmitz & Hauptfleisch1897, pp. 385, 391) in what is today the familyGracilariaceae (Kylin 1932, p. 57). The most recenttreatment of the Gracilariaceae as a whole (Kylin1956, p. 255) divides it into eight genera along linesbased mainly on habit features, and assigns sixbroadly-flattened species with nemathecial, cruciatetetrasporangia to Tylotus.

Dawson (1949, p. 5), in a review of eastern PacificGracilaria species, charges Kylin (1932) with mis-construing and misclassifying Tylotus as a resultof having studied species other than the type. Kylin'sconcepts led him and others to transfer several flat-tened Gracilaria species to Tylotus (Kylin 1932, p.60; 1941, p. 22; Papenfuss 1940, p. 221) or todescribe newly-discovered gracilariaceous taxa asspecies of Tylotus (Joly et al. 1965; Taylor 1945,p. 235).

Dawson's examination of the type species (7*.obtusatus) confirmed J. Agardh's (1876, p. 428)original description of the tetrasporangia as zonate,a fact overlooked by Kylin when he classified Tylotusamong the cruciately-tetrasporangiate Gracilariaceae.Dawson also saw that mature cystocarp sections of

T. obtusatus are unlike typical members of theGracilariaceae, and consequently he proposed thatthe genus be removed to another family. Except forT. obtusatus itself, Dawson found that all the othersupposed Tylotus species that he studied actuallybelonged to Gracilaria, and in this paper (Dawson1949) and in subsequent publications by others (Pap-enfuss 1952, Pinheiro & Joly 1966) almost all thespecies ever placed in Tylotus were either transferredto Gracilaria or returned to it.

The genus Tylotus presently contains, besides T.obtusatus, the two species T. Hchenoides Okamurafrom Japan and T. proliferus (Harv.) J. Ag. fromNew Zealand. This report describes a recent collec-tion of fertile material of the latter species andshows that it too should be transferred to Gracilaria.The type species of Tylotus has recently been re-studied and transferred to the gigartinalean familyDicranemaceae (Kraft 1977).

TAXONOMY AND MORPHOLOGY

Gracilaria truncata nom. nov.

Rhodymenia prolifera Harvey 1855: 249.Calliblepharis prolifera (Harv.) J. Agardh 1876:

432; 1878: 23. De Toni 1924: 278. Laing 1902:342; !927: 156.

Tylotus proliferus (Harv.) Kylin 1932: 60. pi. 22,fig. 56. Laing 1939: 151.

496 New Zealand Journal of Botany 15, 1977

Non Gracilaria prolifera Reinsch 1888: 147; 1890:383. De Toni 1900: 439; 1924: 252. Papenfuss1964: 36.

TYPE LOCALITY: Hawke's Bay, on the east coast ofthe North Island, New Zealand (Colenso).

MATERIAL STUDIED: The specimens of this study(Fig. 1) were collected from gently sloping beachrock north of the river mouth at Bethells Beach onthe North Island west coast near Auckland. Clumpsof plants grew near the low tide mark with theirbases buried in several centimetres of sand. Specimensare numbered Kraft 4769, collected by G. Kraft andDavid Luxton on 21 May 1974. Duplicates aredeposited in the algal herbaria of the University ofMelbourne (MELU), the University of Adelaide(ADU), and the University of Auckland (AKU).

DISTRIBUTION: The species is endemic to NewZealand, where it ranges from Stewart Island (Adamset al. 1974, p. 222) in the south to the Bay ofIslands (Laing 1939, p. 151) and Ahipara (Fig. 2)in the north. A recent record of T. proliferus fromTanzania (Jaasund 1976, p. 87, fig. 175) depictsgracilariaceous plants of rather different habit fromthe New Zealand material and undoubtedly refersto a distinct species. The same is true of Weber-vanBosse's (1913, p. 117, pi. 12, fig. 3) record of Callib-lepharis prolifera from the Amirante Islands off theeast coast of Africa. Her illustration of frond habitshows a pinnate branch pattern and tapering apicesquite unlike the New Zealand species.

Tylotus proliferus is usually reported as being un-common and encountered either in the drift (Adams1972, p. 79; Laing 1939, p. 151), subtidally (Adamset al. 1974, p. 221), or in the lower intertidal (Bev-eridge & Chapman 1950, p. 200; Dellow 1955, p. 80).One ecological study (Beveridge & Chapman 1950,pp. 193, 199, 200) records it as rare and growing onrock with its bases in sand through a 60-cm verticalrange extending upward from the 0.0-m level(E.L.W.S.) to 30 cm below M.L.W.N.

In some herbaria, specimens of T. proliferus havebeen distributed under other names, as in the case ofLindauer exiccaiae number 119 (Fig. 2, ADU, A4735)which is labelled Curdiea engelhartii.

HABIT: Clusters of individual thalli arise from com-mon or coalesced crustose holdfasts and reach 10-15cm long (Figs 1,2). The basal 1-2 mm of the mainaxis are subterete but pass quickly through anapophysis to the linear, flattened axes (Fig. 12). Mostplants tend to have a single primary axis, 5-15 mmwide and 1.5-7 cm long, from which several majorbranches arise, usually at or near the distal end. Inmature thalli, the main axis and most primary

branches are often sharply truncated, giving theman elongatedly wedge-shaped appearance (Figs 1, 2).Thalli are irregularly divided into 3-4 orders ofbranching, most branch proliferations being confinedto the distal portions of major axes where theyarise from narrowly-constricted bases and grow frombroadly-rounded apices. Branchlets also issue (abund-antly at times) both marginally, submarginally, andoccasionally from the broad faces of major branchessome distance behind their apices (Fig. 1).

Although the truncated axes of this species prob-ably result from environmental causes (such asgrazing or mechanical wear) rather than direct geneticpredisposition, they characterise all but the smallestplants in our collections. Since these truncations arealso prominent on the type specimen (Kylin 1932,pi. 22, fig. 56) and on at least some Lindauerexiccatae (Fig. 2), I have chosen a new specificepithet to emphasise this distinct morphologicalfeature.

VEGETATIVE STRUCTURE: Plants have a medulla (Fig.13) of large pseudoparenchymatous cells which gradeperipherally through a rather short series of in-creasingly smaller cells to the 1-2 layered cortex ofcuboidal cells c. 10 /xm in length (Fig. 14). Crosssections average 200-250 ^m in thickness, but reach400-450 /tm in older parts.

CARPOSPOROPHYTE DEVELOPMENT : Carpogonial

branches form within local swellings caused by anti-clinal divisions of the cortex (Fig. 3). The result ofpresumed fertilisation and subsequent diploidisationof a cell or cells adjacent to the carpogonium is aprominent, much-ramified fusion cell (Fig. 4) whichlies at the base of actively lengthening files of cor-tical filaments. Apical growth of the cortical filamentscontinues at the same time that disintegration ofseveral inner cell layers of the cortex begins justdistal to the fusion cell (Fig. 5). Not until a cavityhas thus formed above it does the fusion cell give riseto the first divisions of the gonimoblast. The younggonimoblast is composed of tight lobes of cells whichdivide and protrude into the enlarging cystocarpcavity (Fig. 6). At an early stage of development,some of the gonimoblast cells differentiate intolengthy filaments which grow beyond the gonimo-blast to fuse with cells of the surrounding cystocarpwall (Figs 6, 7).

As the gonimoblast matures, the gametophyticcells lining the floor of the cystocarp chamber divideinto a layer of small-celled tissue over which thecarposporophyte expands as it enlarges (Figs 6-9).Connections are established between gametophyticcells of the cystocarp floor and cells of the gonimo-blast, either by the downward growth of gonimoblast

5/ i6

Figs 1—6 Gracilaria truncata nom. nov.Fig. 1 Habit of a tetrasporangial thallus collected from the lower eulittoral at Bethells Beach (Kraft & Luxton).Scale = 5 cm.Fig. 2 Lindauer exiccatae no. 119 (A4735 in ADU), a cystocarpic thallus from Ahipara. Scale = 5 cm.Fig. 3 A carpogonium (arrow) and surrounding filaments of the actively lengthening cortex. Scale = 25 fim.Fig. 4 A multilobed fusion cell (arrowhead) before the initiation of gonimoblast cells. Scale = 50 nm.Fig. 5 Formation of the cystocarp cavity by progressive breakdown of cells in the cortical layers distal tothe fusion cell (arrowhead). Scale = 50 ,«m.Fig. 6 Early gonimoblast development into the cystocarp cavity. A traversing filament (arrow) has formedbetween the gonimoblast and a cell of the inner layer of the pericarp. A layer of small cells has formed at thefloor of the cystocarp cavity. Scale = 100 /xm.

New Zealand Journal of Botany 15, 1977

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8

Kraft—Tylotus proliferus 499

Figs 7-11 opposite Gracilaria truncata nom. nov.

Fig. 7 A young gonimoblast from which several stout traversing filaments have established links to cells ofthe floor and sides of the cystocarp cavity. Scale = 100 jum.

Fig. 8 Later development of the gonimoblast in which the bases of the traversing filaments become envelopedby the outer layers of the carposporophyte. Traversing filaments are directed towards the base of the cystocarpand laterally where they fuse to cells of the inner pericarp (small arrow). Remnants of the original fusion cell(large arrow) are present. Scale =100 /xm.

Fig. 9 Terminal carposporangia borne on the outermost layer of the carposporophyte. Various traversing fila-ments are fused (arrow) to cells of the inner pericarp. Scale = 100 ji»m.

Fig. 10 The border region between gonimoblast and gametophytic cells in a mature cystocarp. Continuity isestablished between the two tissues by pit connections (arrowhead) and by downward-growing gonimoblast fila-ments. A carposporangium (arrow) is borne on a peripheral gonimoblast filament. Scale = 100 ,um.

Fig. 11 Appearance of a nearly-mature cystocarp, sectioned to one side of the ostiole. Traversing filaments(arrow) are mostly confined to the lower portion of the gonimoblast. Scale = 100 ^m.

filaments into the basal tissue (Fig. 8) or by second-ary pit connections formed between gametophyticcells and short but somewhat elongate gonimoblastcells at the base of the carposporophyte (Fig. 10).

The gonimoblast filaments which penetrate andpartially fuse to cells of the inner pericarp are mostlyinitiated and established with the early developmentof the gonimoblast "parenchyma" (Figs 6, 7). Fur-ther development of the carposporophyte tends toenvelop the basal parts of the filaments with theouter, carposporangial layers of the gonimoblast(Figs 8, 9). Single terminal carposporangia formacross the outer layer of the carposporophyte andrange from 25-40 /im long by 15-25 /im wide. Maturecystocarps consist internally of hemispherical carpo-sphorophytes (Fig. 11) surrounded by a thick peri-carp that is pierced by a conspicious apical ostiole(Fig. 15). Externally, the cystocarps are flask-shaped,basally constricted, and scattered over both sides offertile axes (Fig. 15).

SPERMATANOIA AND TETRASPORANGIA : There are no

male plants in the collections. Tetrasporangia arenot confined to sori or nemathecia, but occur scat-tered over both surfaces of the fronds in the outercortex. Sporangia are cruciately divided and reach30-40 X 20-30 /am.

DISCUSSION

The pattern of cystocarp development in G. trun-cata is virtually identical to that reported by Sjostedt(1926) and Kylin (1920) for species of Gracilaria.As shown elsewhere (Kraft 1977), such a processdiffers in several ways from that displayed by Tylotusand its relatives. The non-nemathecial, cruciate tetra-sporangia of G. truncata also point to this speciesbeing a paradigm of Gracilaria.

The species of Gracilaria seem to be unique amonggigartinalean algae in forming a fairly complex fusioncell well before the initiation of the first gonimoblasts(cf. also Sjostedt 1926, p. 58). In G. truncata thegonimoblast initials apparently await the formationof the cystocarp activity before being cut off.

The gonimoblast filaments which cross from thecarposporophyte and embed themselves in the peri-carp are a striking feature of most Gracilaria species.What to call these structures is somewhat of a prob-lem, as terms used in the past have presumed a nutri-tive function for the filaments which is yet to bedemonstrated. Thus, Sjostedt (1926, p. 61) speaksof "nutrient tubular cells" whose purpose is to "takeup nutrient" from cortical cells and "convey it downto the gonimoblast-parenchyma". This is a some-what debatable interpretation in light of what we nowknow about the ultrastructure of red algal pit con-nections (Ramus 1969). Boergesen (1950, p. 32),Dawson (1949), Ohmi (1958), and others employthe term "nutritive filaments," a usage that is tenta-tively accepted by Yamamoto (1975) pending betterunderstanding of the function of these structures. Amore purely descriptive term, one in line with ourpresent lack of knowledge, seems warranted for thesespecial Gracilaria gonimoblast cells. "Gonimoblasticrhizoids" or "gonimorhizoids" would seem appro-priate and descriptive, but have been applied pre-viously by Abbott & Doty (1960) to filaments whicharise from the carposporophyte in Trichogloeopsisand which grow laxly around and along the carpo-gonial branch cells which subtend the gonimoblast.Such gonimorhizoids have free ends and are notsecondarily fused or connected to any of the game-tophytic cells of the plant, in contrast to the gonimo-blast filaments in Gracilaria.

Perhaps a completely neutral term like "traversingfilaments" would suffice to characterise the struc-tures for the present, for the filaments in Gracilaria

12

50jjm"

Figs 12-15 Gracilaria truncata nom. nov.Fig. 12 The primary axes of several individual thalli showing variations in form and the amounts of prolif-erous branching.Fig. 13 Cross section through the edge of a mature thallus.Fig. 14 Detail of the outer medulla and cortex.Fig. 15 Branch habit with mature cystocarps.

Kraft—Tylotus proliferus 501

unquestionably do traverse the distance, often avery short one, separating the sterile, pseudoparen-chymatous cells of the gonimoblast from the gameto-phytic tissue of the pericarp or floor of the cysto-carp. Whether their function is nutritive, structural,or something else, the traversing filaments of G.truncata appear to be formed very early in the goni-moblast development. They grow both outwards fromthe gonimoblast towards the pericarp and down-wards from the gonimoblast into the floor of thecystocarp cavity.

Gracilaria truncata appears closest in habit affini-ties to the G. textorii group of species which Ohmi(1955; 1958, p. 40) considers to embrace a widerange of forms occurring in Japan and Pacific Mexico.All these plants have flat, linear thalli with broadly-rounded apices, basally constricted marginal branches,and cystocarps that are scattered across both sides ofbroad areas of the frond. As Ohmi describes it, G.textorii tends to be both wider and thicker than G.truncata, with more numerous and regularly disposedlateral branches. The fronds of G. textorii are flabel-late, distinctly dichotomous, and mostly lack branchtruncations, a combination of features that seems todistinguish it specifically from G. truncata. Gracilariasymmetrica Dawson (1949, p. 31) is another speciesshowing habit similarities to G. truncata, although itstype material has few truncations and no lateralproliferations.

The genus Gracilaria is well represented with atleast eight species, both flattened and terete, inAustralia (May 1948). Until now, only two specieshave been regularly reported from New Zealand(Adams 1972, Adams et al. 1974, Naylor 1954), bothof which are terete and non-endemic. The endemic G.truncata is thus a distinctive entity which appears toconstitute the first flat species of Gracilaria to bereliably recorded in New Zealand.

ACKNOWLEDGMENTS

I especially thank David Luxton of the Universityof Auckland and Leigh Laboratory for his hospitality,guide service, and for pointing out the fact (to whichI was oblivious) that I was standing amidst a greatsward of Tylotus proliferus. I thank Karl Johnson(University of Auckland), Tess and Tony Orchard(Auckland War Memorial Museum), and Tatjanaand Murray Parsons (Botany Division, DSIR) fortheir help and interest on several New Zealand visits.Carolyn U. C. Kraft critically reviewed the manu-script, and 1 thank her.

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