1176

J. Phycol.

38,

1176–1189 (2002)

MORPHOLOGY AND SYSTEMATICS OF

SCIUROTHAMNION STEGENGAE

GEN. ET SP. NOV. (CERAMIACEAE, RHODOPHYTA) FROM THE INDO-PACIFIC

1

Olivier De Clerck

Research Group Phycology, Biology Department, Ghent University, Krijgslaan 281 S8, 9000 Ghent, Belgium

Gerald T. Kraft

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

and

Eric Coppejans

2

Research Group Phycology, Biology Department, Ghent University, K. L. Ledeganckstraat 35, 9000 Ghent, Belgium

A new ceramiaceous alga,

Sciurothamnion stegengae

De Clerck et Kraft, gen. et sp. nov., is describedfrom the western Indian Ocean and the Philippines.

Sciurothamnion

appears related to the tribe Calli-thamnieae on the basis of the position and composi-tion of its procarps and by the majority of post-fertil-ization events. It differs, however, from all currentmembers of the tribe by the presence of two periax-ial cells bearing determinate laterals per axial cell.Additionally, unlike any present representative ofthe subfamily Callithamnioideae, no intercalary footcell is formed after diploidization of the paired aux-iliary cells. The genus is characterized by a terminalfoot cell (“disposal cell”), which segregates the hap-loid nuclei of the diploidized auxiliary cell fromthe diploid zygote nucleus. The nature of three typesof foot cells reported in the Ceramiaceae (interca-lary foot cells containing only haploid nuclei, inter-calary foot cells containing haploid nuclei and a dip-loid nucleus, and terminal foot cells containing onlyhaploid nuclei) is discussed.

Key index words:

algae; Ceramiaceae; cytology; mor-phology; Rhodophyta;

Sciurothamnion

gen. nov.;

Sci-

urothamnion stegengae

sp. nov.; systematics; taxonomy

During recent studies of the marine benthic florasof South Africa and eastern Africa in the western In-dian Ocean, numerous specimens of a conspicuousceramiaceous alga were collected at several localities.Because of its distinctive features it was recognized asidentical to tetrasporophytes and female gameto-phytes collected by the second author in the Philip-pine Islands in 1968 and filed as “Callithamnieae gen.nov?” in the Kraft Herbarium at the University of Mel-bourne. This entity was later recorded as “

Callitham-nion

(?) sp. nov.” and characterized as “a likely newgenus” by Kraft et al. (1999) in a survey of Rhodo-phyta from the collection locality in southeastern Lu-

zon. Detailed examination of the recent southeasternAfrican collections reveals that they do indeed repre-sent a new genus and species with affinities to mem-bers of not only the tribe Callithamnieae but also thetribe Ptiloteae. For these algae we propose the newgenus

Sciurothamnion

, containing at present a singlehighly disjunct species,

Sciurothamnion stegengae.

Some features of

Sciurothamnion

are unique andseemingly at odds with what is known about membersof both the Callithamnieae and Ptiloteae, particularlyin regard to early post-fertilization events. This has ledus to consider carefully the defining features of ceram-iaceous tribes. At present these are mostly based on acombination of vegetative and reproductive charac-ters, the latter particularly involving the position ofthe procarp, the number of periaxial cells per fertileaxial cell, the presence and configuration or absenceof sterile cell groups on the supporting cell, the orien-tation of the carpogonial branch, and early events af-ter diploidization of the auxiliary cells (Kylin 1956,Hommersand 1963, Itono 1977). Detailed reports onthe immediate post-fertilization events at both ana-tomical and cytological levels tend to be very incom-plete or inconsistent (Hommersand 1997), particu-larly in regard to how a derivative of the zygotenucleus reaches the auxiliary cell and how the segre-gation of the haploid and diploid nuclei take place,which causes a persistent difficulty in adequately de-fining ceramiaceous tribes and properly placing newlydiscovered taxa within them. Consequently, the abso-lute taxonomic importance of characters relating tothe diploidization of the auxiliary cell remains uncer-tain, and it seemed appropriate to investigate and re-view these events in detail in the present study.

materials and methods

Morphological observations were made on specimens pre-served in 5% formalin-seawater. Whole mount and sectioned ma-terial was stained either with aniline-blue and mounted in Karosyrup or stained with Wittmann’s aceto-iron-hematoxylin-chloral-hydrate and mounted in Hoyer medium as described in Hom-mersand et al. (1992). Drawings were made with a camera lucidaand photographs were taken with an Olympus DP50 digital cam-era (Melville, NY, USA) mounted on a Leitz Diaplan compound

1

Received 26 December 2001. Accepted 22 June 2002.

2

Author for correspondence: e-mail eric.coppejans@rug.ac.be.

1177

S. STEGENGAE

FROM THE INDO-PACIFIC

microscope or Leica Wild M10 (Wetzlar, Germany) stereo micro-scope. Herbarium abbreviations follow Holmgren et al. (1990).

results

Sciurothamnion

De Clerck et Kraft, gen. nov.

Plantae ceramiaceae plurimis cellulis axialibus centralibusprocreantibus duas cellulas periaxiales lateralia determinatapseudodichotoma ecorticata ferentes, paribus lateralium suc-cessivis, decussatis. Axes primarii et indeterminati dense corti-cati usque ad cellulas paucas infra apices; axes indeterminatiex augmente renovato ad apices lateralium determinatorumexorientes. Tetrasporangia in tetrahedro divisa, sessilia singu-laque in cellulis lateralium determinatorum. Spermatangia inaxibus nanis spermatangialibus, axibus 1–2 in quaque cel-lula proximali lateralium determinatorum portatis, prope ba-sin semel vel bis ramosis, ad 8 cellulas longis, cellula omni procellula spermatangiali materna fungenti et 2–4 spermatangiaovoidea statim producenti. Procarpia in cellulis intercalaribusaxium indeterminatorum portata, quaque cellula axiali fertiliefferenti laterale singulum determinatum vegetative et cellulasduas periaxiales perpendiculariter plano lateralis vegetativiabscissas, una cellula periaxiali pro cellula sustinenti fun-genti et ramum carpogonialem 4-cellulum ferenti, altera era-mosa remanenti et cellulam auxiliarem secundam sub fecun-dationem carpogonii facienti; cellulae auxiliares gemellae edivisione inaequali cellulae sustinentis et periaxialis fertilis ex-orientes, diploideae factae a cellulis duabus connectentibus inlateribus oppositis carpogonii fecundati abscissis; cellulae pe-dis intercalares nullae, nucleis haploideis cellularum auxiliar-ium in cellula abiectionis segregatis; initia gonimoblastorumdeinceps efferentia usque ad 5 gonimolobos simul matures-centes; gonimoblastus maturus circumcinctus ab involucrobene evoluto e cellulis 2–3 proximalibus et 2 distalis cellulaeaxiali fertili oriundo.

Species typicum: Sciurothamnion stegengae

De Clercket Kraft

Ceramiaceous plants with two periaxial cells bear-ing pseudo-dichotomous uncorticated determinatelaterals on most central-axial cells, successive pairs oflaterals being decussate. Primary and indeterminateaxes densely corticated to within a few cells of the api-ces, indeterminate axes being formed by renewedgrowth at the tips of determinate laterals. Tetraspo-rangia tetrahedrally divided, sessile and single on cellsof determinate laterals. Spermatangia on dwarf sper-matangial axes borne 1–2 per proximal cell of deter-minate laterals, the axes once or twice branched prox-imally, to eight cells in length, every cell acting as aspermatangial mother cell and producing 2–4 ovoidspermatangia directly. Procarps borne on intercalarycells of indeterminate axes, each fertile axial cell pro-ducing a single determinate vegetative lateral and twoperiaxial cells cut off perpendicular to the plane ofthe vegetative lateral, one periaxial cell functioning asthe supporting cell and bearing a four-celled carpogo-nial branch, the other remaining unbranched andgiving rise to a second auxiliary cell upon fertilizationof the carpogonium; paired auxiliary cells formed byunequal division of the supporting cell and fertile

periaxial cell; diploidization of the auxiliary cells bymeans of two connecting cells cut off on oppositesides of the fertilized carpogonium; intercalary footcells not formed, haploid nuclei of auxiliary cells be-ing segregated in a disposal cell; gonimoblast initialssequentially producing up to five synchronously matur-ing gonimolobes; mature gonimoblast surrounded by awell-developed involucrum derived from the 2–3 cellsproximal as well as the 2 cells distal to the fertile axialcell.

Type species: Sciurothamnion stegengae

De Clerck etKraft

Etymology:

From the Greek word

skiouros

, in refer-ence to the resemblance of the ultimate branches ofthe alga to the tail of a squirrel, and the Greek word

thamnos

, for bush (Backer 2000).

Sciurothamnion stegengae

De Clerck et Kraft, sp. nov.

Thalli erecti, singuli vel caespitosi ex haptero discoideo,usque ad 15 cm longi, rosaceo-rubri, splendide iridescentes invivo; axes primarii irregulariter dichotomi, valde corticati afilamentis descendentibus e cellulis proximalibus lateraliumdeterminatorum, prope basin ad 1.5 mm in diametro; latera-lia determinata ad 700–800

�

m longa; lateralia adventitiae cellulis corticalibus superficialibus axium determinatorumexorientia, plerumque rudimentalia remanentia. Structuraereproductionis ut in genere.

Thalli erect, single or in clusters from a discoidholdfast, to 15 cm in length; color pinkish-red, brightlyiridescent when living; main axes irregularly dichoto-mously branched, heavily corticated by downgrowingfilaments derived from the proximal cells of determi-nate laterals; to 1.5 mm in diameter near the base; de-terminate laterals to 700–800

�

m in length; adventi-tious laterals arising from surface cortical cells ofindeterminate axes, usually remaining rudimentary.Reproductive structures as for the genus.

Etymology:

The specific epithet honors a fine indi-vidual and dedicated student of the marine algae ofSouth Africa, Dr. Herre Stegenga, whose critical stud-ies of African Ceramiaceae are a major contributionto our understanding of the diversity and complexityof this family.

Holotype:

GENT, KZN 695, collected by E. Coppe-jans, O. De Clerck, J. J. Bolton, R. J. Anderson, F. Leli-aert, J. Muylle, and I. De Smet on 15 August 1999 (Fig.1A). Isotypes are deposited in BOL and MELU.

Type locality:

Linkia Reef, Ingwavuma District, Kwa-zulu-Natal, South Africa.

Distribution:

At present, known from Tanzania,Kwazulu-Natal (South Africa), and the island of Lu-zon in the Philippines.

Material examined:

South Africa, Kwazulu-Natal. Ing-wavuma District, Sodwana Bay, 1/4 Mile Reef, epilithicon scattered rocky outcrops at

�

9 m,

O. De Clerck andE. Cocquyt

, 15.viii.2000, GENT KZN 1717; IngwavumaDistrict, Sodwana Bay, 9 Mile Reef, epilithic on coraldebris at

�

4 to

�

11 m,

O. De Clerck, H. Engledow, S. Fred-ericq, W. Freshwater, F. Leliaert, A. Millar, T. Schils, and E.Tronchin

, 12.ii.2001, GENT KZN 2160; Port Shepston

1178

OLIVIER DE CLERCK ET AL.

District, Protea Banks, Northern Pinnacle, growing onrocky substrate at –37 m.

O. De Clerck, H. Engledow, S.Fredericq, W. Freshwater, F. Leliaert, A. Millar, T. Schils,and E. Tronchin

, 5.ii.2001, GENT KZN 1937. Tanzania,Mtwara area, Mnazi Bay, Mana Hawanja Island,epilithic on the seaward slope of the reef, –20 m,

E.Coppejans, O. Dargent, and G. Bel

, 5.viii.2000, GENTHEC 14163. Zanzibar Island, Cairo (East coast), grow-ing in tide channel of the fringing reef,

O. Dargent

,21.viii.1997, GENT HEC 12190. Zanzibar Island, Uroa(East coast), back side of the reef, –1 m at spring lowtide,

E. Coppejans and O. De Clerck

, 20.viii.1994, GENTHEC 10492. Philippines, Bulusan, Sorsogan Province,southeastern Luzon, brightly iridescent fronds epilithicat 5–6 m depths on the floor of a channel through thebasaltic reef.

G. T. and C. U. Kraft

, 22.ii.1968, MELUK435.

Habit and vegetative morphology.

Plants grow from asmall discoid holdfast from which one to several erectaxes arise (Fig. 1, B and F) and reach lengths of 7–15cm. Fronds consist of repeatedly and irregularly di-chotomously branched indeterminate axes that aredensely beset with decussate pairs of determinate lat-erals (Fig. 1, B and E). Freshly collected plants are softin texture but not gelatinous, pinkish-red in color,and exhibit a bright-bluish iridescence

in situ.

Determinate laterals reach 15–20 cells and 700–800

�

m in length and are inserted at angles of 55–75 de-grees to the parent axes. They are aligned in fourorthostichous rows, are completely uncorticated, andbranch subdichotomously at a 30–50 degree diver-gence in a more or less single plane (Fig. 1, D and E).The final branch order at maturity consists of 20–35 di-visions that are five to six cells in length and that arethe result of four to eight basal subdichotomies sepa-rated by a single unbranched cell and laxer branchingdistally, where two to seven cells separate successivesubdichotomies (Fig. 2D and 3A). The first determinatelateral initial originates as a protrusion from the highside of the axial cell immediately subtending the apicalcell and is offset by 90 degrees from the lateral on thepreceding and subsequently succeeding contiguous ax-ial cells. Three to six axial cells proximal to the apicalcell a second lateral is formed opposite the first, result-ing in the orthostichous opposite-decussate branchingpattern. Growth of the laterals proceeds through trans-verse divisions of their apical cells (Fig. 2D) and elon-gation of the derivatives. The periaxial cells of maturelaterals are generally shorter (20–30

�

12–15

�

m) andmore rounded than other cells, the epibasal cells reach-ing 50–60

�

16–21

�

m and tapering gradually towardultimate cells 12–18

�

9–12

�

m. The ultimate cells of-ten produce a long rapidly deciduous hair (Fig. 3B).Adventitious determinate laterals frequently issue fromperipheral cortical cells in the lower parts of the thallusand usually remain rudimentary.

Growth of indeterminate axes takes place by ob-lique divisions of the apical cells, with the high sidesof successive axial cells spirally offset in a 1/4 diver-gence (Figs. 2A and 4A). Axial cells in the distal parts

of the thallus are cylindrical (sometimes with a slightmedian constriction) and measure 18–25

�

m in widthby 40–65

�

m in length (L/B: 2–2.5) (Fig. 2, B and D).Mature axial cells are more broad than long (80–125

�

40–60

�

m; L/B: 0.4–0.7), linked by stout primary pitconnections with conspicuous torus-shaped pit plugs,and usually contain several conspicuous globular in-clusions that stain prominently with aniline blue (Fig.2E). Proximal axial cells reach 485

�

m in diameterand are connected by slender lengthy pit-connections(Fig. 2I).

Indeterminate laterals form at irregular intervalsalong primary axes by direct conversion of determi-nate laterals, the transition from determinate to inde-terminate lateral being at the point where paired,rather than single laterals are borne on an axial cell(Fig. 2C). The new indeterminate axis then forms cor-tication that extends to and merges with that of theparent primary axis, although the basal cells of theconverted determinate lateral remains distinctive inthat it still bears only a single lateral.

Primary and indeterminate axes are terete, heavilycorticated to within a few cells of the apices, andreach diameters of 1–1.5 mm near the thallus base,which is mostly denuded of branchlets (Fig. 1F). Cor-ticating filaments initially arise singly from the basalcells of determinate laterals approximately 14–22 cellsproximal to the apices (Fig. 2B). Within a few axialsegments proximal to the site of cortex initiation, asecond and third corticating filament then issuesfrom each of the basal cells, the filaments branchingirregularly and initially enveloping the axial cells in asingle layer (Fig. 2D). Cortication thickens basipetallyand differentiates into an inner tissue to 550

�

m inwidth (Fig. 1G) composed of narrow rhizoidal cells 3–10

�

m wide by 110–220

�

m in length. This layer issurrounded by a consolidated surface covering ofsmall isodiametric cells, which divide by oblique andlongitudinal divisions (Fig. 2, F and H). All vegetativecells are uninucleate.

Reproductive features (Figs. 4–6).

Tetrasporangia are tet-rahedrally divided, sessile, and formed singly and mostlyadaxially at the distal ends of cells of determinate later-als (Fig. 3, B and C). When fully mature they are ovoidand 20–25

�

m in width by 25–35

�

m in length.Gametophytes are dioecious, the spermatangia form-

ing on dwarf fertile axes borne singly or in pairs at thedistal ends and mostly adaxial sides of determinate lat-erals (Fig. 3, D–F). Each cell of the fertile axis functionsdirectly as a spermatangial mother cell and producestwo to four ovoid spermatangia 3–4

�

5–7

�

m.Carpogonial branches form in series near the api-

ces of short relatively young indeterminate axes, al-though only one ever produces a carposporophyte(Fig. 6, A and B). Procarps in varying stages of devel-opment are usually separated by two or three seg-ments on any given lateral but may also develop onadjacent segments (Fig. 6C). Unlike sterile indetermi-nate-axis cells, fertile axial cells bear only one ratherthan an opposite pair of determinate laterals.

1179

S. STEGENGAE

FROM THE INDO-PACIFIC

Fig. 1. Habit and vegetative morphology. (A) Habit of the holotype (GENT KZN 695). Scale bar, 1 cm. (B) Habit of a wet-pre-served highly branched frond. Scale bar, 1 cm. (C) Detail of the apical portion of the thallus. Scale bar, 1 mm. (D) Detail of a branchapex of a relatively sparsely branched axis under dark-field conditions. Scale bar, 1 mm. (E) A densely branched portion of a thallusunder dark-field conditions. Scale bar, 5 mm. (F) Detail of a small discoid holdfast giving rise to two erect axes. Scale bar, 1 mm. (G)Transverse section of an axis near the base of the thallus. Scale bar, 250 �m.

1180

OLIVIER DE CLERCK ET AL.

Fig. 2. Vegetative morphology. (A) Detail of a lightly squashed apex showing the opposite decussate arrangement of the determi-nate laterals. Scale bar, 25 �m. (B) Initials (arrowhead) of the first-formed rhizoidal filaments growing down the abaxial side of thebasal cells of determinate laterals. Scale bar, 25 �m. (C) Transition between a determinate lateral with each cell bearing a single lat-eral (arrows) and an indeterminate axis with opposite branching (arrowheads). Scale bar, 50 �m. (D) Aspect of a corticated axes ap-proximately 2 mm below the apex, with rod-shaped axial cells. Scale bar, 100 �m. (E) Axial cells in the mid-thallus region with prom-inent inclusions. Scale bar, 50 �m. (F) Longitudinal section of an axis showing the differentiation of the corticating filaments,consisting of long and rhizoidal-like cells toward the center of the axis and small isodiametric cells in the outer layers. Scale bar, 50�m. (G) Detail of rhizoidal-like inner corticating filaments. Scale bar, 50 �m. (H) Detail of isodiametric outer corticating filaments.Scale bar, 50 �m. (I) Aspect of the axial cells near the base of the thallus with prominently elongated pit connections (arrowheads).Scale bar, 100 �m.

1181

S. STEGENGAE

FROM THE INDO-PACIFIC

The procarp arises by a concavo-convex division atthe middle of the fertile axial cell. This results in afirst periaxial cell, which arises at 90-degree angle tothe plane that the determinate lateral would occupy ifa second was cut off opposite it, as normally happenson sterile axial cells. The first periaxial cell becomesthe supporting cell with the progressive developmentof a four-celled, L-shaped, carpogonial branch, ofwhich the first (cb1) and second (cb2) cells are ellip-soid; the third cell (cb3) is more angular and bearsdistally the much smaller carpogonium. The carpogo-nium, very much the smallest cell of the carpogonialbranch (Figs. 4, B and C, and 6C), lies opposite thedeterminate lateral borne on the fertile axial cell. The

trichogyne is long (to 500

�

m). The mature secondand third cells are usually binucleate, whereas the firstcell and the carpogonium itself are uninucleate. Inmost instances the carpogonial branch is fully formedbefore a second fertile periaxial cell is cut off from thefertile axial cell opposite the supporting cell. No fur-ther cells are cut off from the supporting cell or thefertile pericentral cell, sterile cell groups being com-pletely absent from the procarp.

After presumed fertilization, the carpogonium ex-pands laterally and the trichogyne breaks down com-pletely. Zygote formation results in an enlargement ofthe supporting cell and fertile pericentral cell, both ofwhich soon divide by an uneven and oblique cross-

Fig. 3. Tetrasporangial and spermatangial morphology. (A) A profusely branched determinate lateral bearing tetrasporangia atvarious stages of development. Scale bar, 100 �m. (B) Tip of determinate lateral, terminating into a hair cell, bearing a lateral tetrahe-drally divided tetrasporangium. Scale bar, 25 �m. (C) Detail of sessile tetrasporangia on a determinate lateral (hematoxylin stain).Scale bar, 25 �m. (D) Spermatangial branches in a lateral position on a determinate lateral. Scale bar, 25 �m. (E) A young sperma-tangial branch, which branches at the base. Scale bar, 25 �m. (F) Detail of a mature spermatangial branch with numerous spermatia.Scale bar, 10 �m.

1182

OLIVIER DE CLERCK ET AL.

wall into a small basal cell and a large auxiliary cell.The diploid nucleus in the carpogonium undergoes asingle mitotic division that is unaccompanied by cy-tokinesis (Figs. 5A and 6D). Instead, two small protru-sions are formed on each side of the carpogonium,adjacent to the auxiliary cells (Figs. 5B and 6E). Thisis followed by a second division of both carpogonialnuclei that results in the formation of two connectingcells. Both division products then migrate to the twosmall protrusions formed on each side of the carpogo-nium adjacent to the auxiliary cells. They are thensegregated into two connecting cells that are not pit-connected to the carpogonium (Figs. 5C and 6F),each consisting of a densely compacted nucleus sur-rounded by a narrow hyaline region. Concurrently,both auxiliary cells become pyriform and their hap-loid nuclei migrate toward the base (Figs. 5B and 6, Eand F). Adjacent to the pit connection between theauxiliary cell and its subtending cell, a darkly stainingproteinaceous body starts to form (Fig. 7A) that laterbecomes a well-developed plug separating diploid andhaploid tissue (Fig. 7D). Diploidization of the auxil-iary cells is followed by an immediate mitotic divisionof the diploid nucleus. One of the daughter nucleimigrates toward the center of the auxiliary cell,whereas the other is extruded in the form of a persis-tent “residual cell” (

sensu

Hommersand 1997) (Figs.5D and 6G). The original haploid nuclei, which at thisstage are situated at the pyriform bases of the auxiliarycells, are cut off by a cleavage perpendicular to thelongitudinal axes of the auxiliary cells to form a “dis-posal cell” (

sensu

Huisman and Kraft 1992) in whichthe haploid nucleus may divide once mitotically (Figs.5D, 6G, and 7, A and B). The carpogonium and hy-

pogynous cells have fused by this stage, but the basaland epibasal cells of the carpogonial branch remaindiscrete (Fig. 7C). As events proceed, the entire car-pogonial branch withers.

The auxiliary cell, which acts as the gonimoblastinitial after segregation and removal of its haploidnucleus, divides apically to form the first gonimolobeinitial (Fig. 7, A and B), after which a second lateralgonimolobe initial soon arises. Eventually each goni-molobe initial can produce up to five rounded sec-ondary gonimolobes that mature sequentially and arecomposed of synchronously maturing carposporangia(Fig. 7, F and G). All gonimolobe cells become car-posporangia except for the basal cells, which elongateinto distinctive stalk cells. Mature carposporangia areirregularly contoured and 10–16

�

m in diameter.Directly after a fertilization event, the two to three

axial cells proximal to and two axial cells distal to thefertile axial cell initiate involucral filaments fromtheir distal poles, there being as many as seven borneon the hypogenous cell (Fig. 7E). Unbranched andfive to six cells long when young, each mature involu-cral filament branches ternately from the distinctiveovoid to obovoid basal cell and pseudo-dichotomouslyfrom the cells above it. Elongation of the indeterminatebranchlet ceases with initiation of the gonimoblast, re-sulting in subapical cystocarps borne on stunted heavilycorticated laterals (Fig. 6, A and B).

discussion

The huge diversity of ceramiaceous algae, as well asthe cryptic and esoteric features that one often needsto observe to classify them, necessitates close attentionto the precise details of procarp position and makeup

Fig. 4. Aspects of the vegetative apex and mature procarp. (A) Detail of a vegetative apex, showing the obliquely dividing apicalcell and the relative formation of the first and second determinate laterals. Scale bar, 10 �m. (B) Lateral view of a nearly mature pro-carp, with the carpogonium placed opposite the vegetative lateral. Scale bar, 10 �m. (C) Lateral view of a mature procarp with fullyextended trichogyne (supporting cell and fertile pericentral cell not illustrated). Scale bar, 10 �m.

1183

S. STEGENGAE

FROM THE INDO-PACIFIC

Fig. 5. Post-fertilization stages of Sciurothamnion stegengae. (A) Early post-fertilization stage showing a fertilized carpogonium (cp)with divided diploid nuclei, the auxiliary cell and fertile pericentral cell have divided to produce a basal cell (bc) and a distal auxiliarycell (au). Scale bar, 10 �m. (B) The fertilized carpogonium has initiated a small beak (arrowhead) directed toward at least one auxil-iary cell (au); the latter have become pyriform and their haploid nuclei (hn) have migrated basally. Scale bar, 10 �m. (C) Two smallconnecting cells (cc) are cut off from the carpogonium but have not fused yet with the auxiliary cell. Scale bar, 10 �m. (D) The auxil-iary cells are diploidized and have subsequently cut off each a residual cell (rc), a disposal cell (dc), and a terminal primary goni-molobe initial (gi1); in one disposal cell the haploid nucleus has undergone a mitosis; one auxiliary cell has already cut off a secondlateral gonimolobe initial (gi2). Scale bar, 10 �m.

1184

OLIVIER DE CLERCK ET AL.

Fig. 6. Female reproductive structures of Sciurothamnion stegengae. (A) Portion of an axis bearing several mature gonimoblasts, situatednear the distal end of short axes. Scale bar, 500 �m. (B) Detail of a maturing gonimoblast placed distally on a short axis. Note the well-devel-oped involucral filaments subtending the gonimoblast. Scale bar, 10 �m. (C) A mature procarp with a four-celled horizontally oriented car-pogonial (cp) branch (the supporting cell and trichogyne are not in focus; the determinate lateral of the fertile axial cell is situated on thesite directly opposite the carpogonium). fpc, fertile pericentral cell. Scale bar, 10 �m. (D) Early post-fertilization stage showing a fertilizedcarpogonium (cp) with a diploid nucleus that has divided; the fertile axial cell has divided to produce a basal cell (bc) and a distal auxiliarycell (au). Scale bar, 10 �m. (E) The carpogonium has initiated a small beak (arrowhead) directed toward the auxiliary cell; the latter has be-come pyriform and its haploid nucleus (hn) has migrated basally. Scale bar, 10 �m. (F) The carpogonium has cut off two connecting cells(cc, only one in focus), which have not fused with the auxiliary cells. Scale bar, 10 �m. (G) A diploidized auxiliary cell with a residual cell(rc) cut off at the site where the connecting cell fused; the haploid nuclei of the auxiliary cell are cut off in a disposal cell (dc).

1185S. STEGENGAE FROM THE INDO-PACIFIC

whenever putative new genera and species are en-countered (Hommersand 1963, Itono 1977, Huismanand Kraft 1992, Athanasiadis 1996). Important also isthe complex series of events succeeding zygote forma-tion, although these are presently less taxonomicallycritical because so few detailed studies have beenmade of them.

Procarp features of Sciurothamnion strongly indicateplacement in the tribe Callithamnieae as defined bySchmitz and Hauptfleisch (1897), Feldmann-Mazoyer(1941), and Kylin (1956). Procarps in this group aresituated on intercalary axial cells of indeterminate lat-erals and have carpogonial branches that are orientedhorizontally to the long axis of the bearing indeter-

minate lateral. They consist of two initially undividedperiaxial cells, of which the first-formed functions asthe supporting cell and the second, arising oppositethe first, mirrors it by cutting off a second auxiliarycell after fertilization. In addition to carpogonial andauxiliary cell features, another consideration that canbe an important tribal attribute is whether or notsterile cell groups are associated with the supportingcell, and if so of what kind. Sciurothamnion lacks anysterile cell groups, a further feature allying it with theCallithamnieae, although a number of other tribes(Crouanieae, Rhodocallideae, Spyridieae [Feldmann-Mazoyer 1941, Hommersand 1963, Wollaston 1968,Hommersand et al. 1998]) and some members of the

Fig. 7. Female reproductive structures of Sciurothamnion stegengae. (A) Detail of a single developing gonimoblast showing the ter-minal primary gonimolobe initial (gli), the gonimoblast initial (gi), a withering disposal cell (dc), and the residual cell (rc). Scale bar,10 �m. (B) Paired gonimoblasts in an early stage of development. Scale bar, 10 �m. (C) Detail of a withering carpogonial branchshowing a carpogonium (cp) which is fused with the third carpogonial branch cell (cb3); the first and second carpogonial branchcells remain discrete (arrowheads). Scale bar, 10 �m. (D) Detail of the basal cells and gonimolobe initials that are separated by aprominently staining proteinaceous body (arrowheads). Scale bar, 25 �m. (E) Transverse section of the hypogenous cell showing thepresence of seven involucral filaments. Scale bar, 25 �m. (F) Detail of a maturing gonimoblast with several gonimolobes at differentstages of development; note the elongate basal cell in each gonimolobe. Scale bar, 25 �m. (G) A fully mature gonimoblast. Scale bar,50 �m.

1186 OLIVIER DE CLERCK ET AL.

Ptiloteae (Moe and Silva 1983, Hommersand andFredericq 2001) are similar in this regard. As a conse-quence the vegetative structure of Sciurothamnion be-comes important to consider when eliminating alltribes but the Callithamnieae and Ptiloteae from seri-ous consideration, the other tribes all being charac-terized by whorled periaxial cells to greater or lesserextents and additionally lacking the paired auxiliarycells and horizontal alignment of their carpogonialbranches.

A procarp structure nearly identical to that of theCallithamnieae is reported for mostly southern hemi-sphere members of the Ptiloteae such as Euptilota, Di-apse, Falklandiella, and Georgiella (Itono 1977, Moe andSilva 1979, 1983, Hommersand and Fredericq 2001),although not for other mostly northern hemisphererepresentatives. This apparent disparity, however, islikely to reflect the polyphyletic nature of the tribe asindicated by both morphological and molecular evi-dence (Hommersand 1989, Hommersand et al. 1998,Saunders and Kraft, unpublished data).

Sciurothamnion also relates to the Callithamnieaeand most southern hemisphere Ptiloteae in regard toimmediate post-fertilization events. In Callithamnioncorymbosum ( J. E. Smith) Lyngbye (Oltmans 1898) andAglaothamnion halliae (Collins) Aponte, Ballantineand J. N. Norris (Hommersand 1997), the transfer ofthe diploid nucleus from the carpogonium to the aux-iliary cell by means of small connecting cells and thesubsequent formation of a residual cell on the auxil-iary cell mirrors these processes as they occur in Sci-urothamnion. Unlike Aglaothamnion and Callithamnion,however, the fertilized carpogonium of Sciurothamniondoes not undergo a mitosis followed by cytokinesis(O’Kelly and Baca 1984, Hommersand 1997), al-though this is also true for Seirospora (Aponte and Bal-lantine 1991, 1995, Kraft 1988) and Carpothamnion(Wollaston 1992, as Thamnocarpus). The carpogoniaof two representatives of the Ptiloteae, Georgiella andEuptilota, apparently also do not divide after fertiliza-tion (Moe and Silva 1983, Hommersand and Fredericq2001). This linking feature appears to have taxonomicimplications that, in combination with anatomical andmolecular studies to be reported separately (M. H.Hommersand, personal communication), will resultin the alliance of Sciurothamnion with Seirospora, Carpo-thamnion, and some former Ptiloteae into a tribe, sis-ter to but distinct from both the Callithamnieae andPtiloteae.

In most Ceramiaceae, diploidization is followed bya division of the auxiliary cell into an intercalary, sub-tending foot cell and a terminal gonimoblast initial.Three different types of cell apparently “designed” tosegregate extraneous nuclei from the gonimoblasthave been identified. The first type contains only theoriginal haploid nucleus of the auxiliary cell (Hom-mersand 1997) or two haploid nuclei in cases where asingle mitosis has taken place after diploidization bythe connecting cell. This type arises from the basalpart of the auxiliary cell and is segregated from the

latter by an incomplete septum (Hommersand 1997).The foot cell, placed eccentrically between the goni-moblast initial and the basal cell, remains pit con-nected to the basal cell and is accompanied by the for-mation of a distinct residual cell, containing a diploidnucleus. The second type contains one or two haploidnuclei and a diploid nucleus. The foot cells are usu-ally slender, attached to the gonimoblast initial by anincomplete septum, and two-lobed, one lobe contain-ing either one or two haploid nuclei, the other a sin-gle diploid nucleus. It seems reasonable to hypothe-size that the diploid nucleus in such foot cells ishomologous to the one that becomes segregated intothe lateral residual cell in type 1 species, becausenone of the authors illustrating this type of structurehas observed a separate residual cell. Well-docu-mented examples include Callithamnion corymbosum ( J.E. Smith) Lyngbye (Oltmans 1898), Spyridia filamentosa(Wulfen) Harvey (Hommersand 1963), Seirospora ori-entalis Kraft (1988), Seirospora occidentalis Børgesen(Aponte and Ballantine 1991), and Rhodocallis elegansKützing (Hommersand et al. 1998). The third typecontains the haploid nucleus of the auxiliary cell butwhich is cut off completely and terminally from theproximal pole of the latter. This type was named a“disposal” cell by Huisman and Kraft (1992) whenthey introduced the genus Guiryella, a representativeof the Monosporeae (Huisman and Gordon-Mills1994). Such cells had been previously observed insome tribes of the subfamily Compsothamnioideae asdefined by Itono (1977) (e.g. the Spermothamnieae,Sphondylothamnieae, and Spongoclonieae [Gordon1972, Stegenga 1986, as “rest” cells, Gordon-Mills andNorris 1986]), but Huisman and Kraft (1992) werethe first to directly attribute their function to the elim-ination of extraneous haploid nuclei from diploidizedauxiliary cells. Possession of a disposal cell may, as inthe case of Sciurothamnion, also be accompanied bythe production of a residual cell, unlike the case ofspecies with two-lobed foot cells in which a separateresidual cell is never present. It also appears thatmany Ceramiaceae have lost the ability to produceany type of cell that rids the auxiliary cell of superflu-ous nuclei. In such cases the haploid nuclei appear tobecome quiescent in the auxiliary cell as it goes on toproduce the wholly diploid cells of the gonimolobeinitials.

Huisman and Kraft (1992) questioned the stricthomology of residual, foot, and disposal cells, but weconsider that all three types are possibly more thanjust analogous structures even though it is thoughtthat the family Ceramiaceae as presently constituted ispolyphyletic (H.-G. Choi, G. T. Kraft, I. K. Lee, and G. W.Saunders, unpublished data). This is because theyequally function to eliminate haploid nuclei from thegonimoblast initial, leaving it and succeeding cells ofthe carposporophyte wholly diploid. Differences be-tween the three types can be reduced to the orienta-tion of the initial cleavage plane of cytokinesis in theauxiliary cell. If the cleavage plane is more or less per-

1187S. STEGENGAE FROM THE INDO-PACIFIC

pendicular to the longitudinal axes of the auxiliarycell, the resulting cell will be a foot cell only contain-ing the haploid nucleus/nuclei, positioned eccentri-cally between the auxiliary cell and basal cell. The dip-loid nucleus resulting from the mitosis of the fusingconnecting cell is extruded simultaneously and formsa distinct residual cell (Hommersand 1997). In caseof a cleavage plane more parallel to the longitudinalaxes of the auxiliary cell, the resulting foot cell will betwo-lobed. In the extreme case, where the cleavageplane does not include the pit-connection betweenthe auxiliary cell and basal cell, a disposal cell isformed.

The different types of cells that eliminate extrane-ous nuclei from auxiliary cells appear to be geneti-cally fixed within species, but their value as a diagnos-tic character at the genus and tribal levels in theCallithamnieae/Ptiloteae complex remains to be de-termined. Most representatives of the genus Seirosporapossess two-lobed foot cells (Feldmann-Mazoyer 1941,Aponte and Ballantine 1995), but both foot and resid-ual cells have been reported for Hirsutithallia (Wom-ersley and Wollaston 1998, Fig. 121E, J), Aglaotham-nion and Callithamnion (Oltmans 1898, Hommersand1997).

Development of the carposporophyte in Sciuro-thamnion is typical of the Callithamnieae, the mor-phology of the gonimolobes and carposporangia beingsimilar to most Aglaothamnion, Callithamnion, Carpotham-nion, and Hirsutithallia species. The elongate sterilecells that subtend each gonimolobe in the new genus,however, have only been reported for the South Afri-can Carpothamnion molle (Wollaston) Silva (Wollaston1992, as Thamnocarpus mollis Wollaston) and appear tobe a specialization, one independently arrived at inunrelated genera such as Dasyphila (Kraft and Wilson1997) and Hirsutithallia (Womersley and Wollaston 1998).Despite similarities between Sciurothamnion and Seirosporain procarp and early gonimoblast features, their ma-ture carposporophytes differ significantly, Sciurotham-nion having multiseriate rounded gonimolobes whereasthose of Seirospora are composed of uniseriate chains(Miranda 1932, Feldmann-Mazoyer 1941, Kraft 1988,Maggs and Hommersand 1993). This appears to be anautapomorphic feature of Seirospora, one finding roughlyparallel expression only in the genus Ardrenema of theCeramieae (Norris and Abbott 1992).

Male structures of Sciurothamnion are similar to thoseencountered in many tribes of the Ceramiaceae, in-cluding the Callithamnieae and Ptiloteae. Two formsof spermatangial branchlets are known in the formertribe, erect filaments and hemispherical cushions. Be-cause it is easy to visualize the pulvinate type being de-rived from erect filaments through reduction of fertileaxial cell numbers and their reorientation, perhapsmore phylogenetic importance should be attached tothe location of the spermatial nuclei. In Aglaothamnion,Callithamnion (Feldmann-Mazoyer 1941), and appar-ently also in Carpothamnion and Hirsutithallia (Wollas-ton 1992, as Thamnocarpus, Womersley and Wollaston

1998), the nucleus lies in a median position, whereasin Seirospora and Sciurothamnion it is located distally(Aponte and Ballantine 1995, this study). The absolutetaxonomic significance of this distinction is not clear,but it does constitute yet one more way in which Sci-urothamnion and Seirospora share a feature that otherCallithamnieae apparently lack.

Although in many ways secondary to reproductiveprocesses in the higher level taxonomy of the Cerami-aceae, vegetative construction is important to estab-lish tribes and, as a practical matter, largely guides thetribal placement of most genera. Patterns of divisionof the apical cell are correlated with the primarygrowth patterns that tend to be diagnostic of tribes(Moe and Silva 1979). A 1/4 spiral branching patternin species that form only one or two periaxial cells perindeterminate-axial cell seems to be encountered onlyin some genera of the Callithamnieae and Spongoclon-ieae (Itono 1977, Norris 1985, Wollaston 1990), a 1/2spiral being the norm in many Callithamnieae, mostSpongoclonieae, and all Compsothamnieae and Ptilo-teae. Although several unrelated groups exhibit a de-cussate branching pattern when bearing opposite de-terminate laterals, the combination in Sciurothamnionof 1/4 spiral first-lateral phyllotaxy followed by the de-velopment of a second periaxial cell directly oppositethe first is unique among the Ceramiaceae. The abso-lute phylogenetic value of this character is probablylimited, however, because it seems likely that varioustypes of apical divisions and resulting primary branch-ing patterns have arisen several times independently.Assuming that the most primitive structure in Cerami-aceae is a primary-axial filament bearing whorls of lat-erals (Hommersand 1963, Wollaston 1971), the branchstructure of the Callithamnieae can perhaps best beexplained by the loss of the second-formed lateral, afeature that Sciurothamnion has relictly retained.

Apart from the number of laterals per axial cell, theentire vegetative thallus of Sciurothamnion is very Calli-thamnion-like. In Sciurothamnion, the Callithamnieaegenerally (e.g. Dixon and Price 1981, Coomans andHommersand 1990), the Rhodocallideae (Hommer-sand et al. 1998), and possibly other genera such asGymnothamnion, Plumaria, and some species of Ptilota(M. H. Hommersand, personal communication), inde-terminate axes are formed by direct transformation ofthe apical cells of determinate laterals, although thisfeature is difficult to determine in the Callithamnieaebecause the branching pattern of determinate and in-determinate branches is virtually identical. In Sciuro-thamnion, on the other hand, it is possible to see wherethe pseudo-dichotomies of determinate laterals un-dergo a transition to opposite-decussate branching andthus the precise point at which the indeterminate lat-eral has been produced. This sort of phenomenon al-lowed Millar and Kraft (1984) to establish the analo-gous process of indeterminate-axis transition in thegigartinalean genus Acrosymphyton.

A further vegetative character linking Sciurotham-nion to the Callithamnieae is its cortical morphology.

1188 OLIVIER DE CLERCK ET AL.

Wollaston (1992, as Thamnocarpus) described a nearlyidentical cortex for both the Australian Carpothamniongunnianum (Harvey) Kützing and the South AfricanC. molle, for in all three a thick cortex envelops all butthe extreme tips of the indeterminate laterals and isproduced by means of downward growing rhizoidalfilaments that originate from the proximal cells of de-terminate laterals. As in Carpothamnion, the peripheralcorticating filaments of Sciurothamnion cut off smallisodiametric cells that form a continuous mosaic overthe axes.

Based on the combination of reproductive and veg-etative characters detailed above, we believe that Sci-urothamnion is distinct from any described genus ofthe Ceramiaceae. Its closest affinities in most respectsappear to lie with some of the Callithamnieae, partic-ularly the genera Seirospora and Carpothamnion, al-though there are sufficient differences in branchingand processes by which haploid nuclei are eliminatedfrom auxiliary cells to suggest that the present genericmakeup of the Callithamnieae needs reassessment.Challenges to the monophyly of the present Ptiloteae,some members of which show reproductive and vege-tative similarities to Sciurothamnion, are soon to be re-ported (M. H. Hommersand, personal communication)and will include molecular data on Sciurothamnion. Be-cause those studies will determine the final tribalplacement of our new genus, we limit our presenttreatment to its description and consideration of itsmost distinctive features.

We thank the researchers and students who helped to collectthe material over the years along the East African coast as wellas in Kwazulu-Natal. We offer our sincere gratitude to JeanHarris, Nonhlanhla Nxumalo, Bridget Armstrong, CloverlyLawrence, and John Dives, of the Kwazulu-Natal Nature Con-servation Services, for their full support in organizing every-thing, every time, everywhere. We also extend our thanks to Pe-ter Timm from Triton Divers for his expert services. Fundingfor this project was provided by the International Scientific andTechnological Cooperation (BIL98/84) between the GhentUniversity and the University of Cape Town and FWO ResearchProject (3G002496). G. T. K. greatly appreciates the support ofhis Philippine studies by the late Professor Max Doty, the Ma-rine Colloids Corporation, and his cherished collecting part-ner, the late Carolyn Kraft. We all especially thank Dr. AlanMillar (National Herbarium of New South Wales) for organiz-ing and directing the publication on Philippine algae by Kraftet al. (1999) that resulted in the meeting and note comparingof the second and third authors during the latter’s Distin-guished-Visitor Fellowship to The Royal Botanic Gardens, Syd-ney. We also thank Professor Max Hommersand for the lengthydiscussions and critical comments, which definitely helped toshape our ideas. Latin diagnoses were kindly provided by Mr.Mark Garland whose professional services are much appreci-ated.

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