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INDIAN COUNCIL OF AGRICULTURAL RESEARCHNEW DELHI

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FIRST PRINTED DECEMBER 1967

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Chief EditorEditor

Subeditor

C. G. RAGHAVAKURuPP. KACHROOM. ARIF

Prodmtion Officer : KRISHAN KUMAR

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@All Rights Reserved ~

1967, by the Indian .Council of Agricultural Research, New Delhi

Printed in India by M. C. Khunnah at the Job Press Private Ltd., Kanpur, and publishedby T. S. Pruthi, Under-Secret~.: Indian Council of Agricultural Research; New Delhi.

PREFACE

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The present account includes all the known Chlorococcales froni the Indianregion comprising India and Sikkim, Pakistan, Afghanistan, Nepal, Burma, andCeylon. It is dealt with in two parts, the first part giving a general' account ofthe order, viz., the morphological, ecological, physiological and applied aspectsand the classification including phylogeny; and the second part dealing with thetaxonomy of forms known exclusively from the Indian region. In writing out thisvolume standard works on algae like Kuetzing (1843, 1845, 1849), Naegeli (1849),Braun (1855), Reinsch (1867), Rabenhorst (1868), Lagerheim (1882), Hansgirg (188.6),De Toni (1889), Wille (1897, 1909), Oltmanns (1904, 1922-23), G. S. West (1904,

. 1916), Brunnthaler (1915), Printz (1927), West and Fritsch (1927), Smith (1933,1950,_1951), Fritsch (1935), Tilc;len (1935), Prescot! (1951), Tiffany and Britton(1952), Korshikov (1953), Fott (1959), and a number of other works dealing speciallywith this order have been fully made use of, mostly in original. For the second part,all possible literature on Indian Chlorococcales has been consulted. Apart fromthese, the author's unpublished observations on the planktonic Chlorococcales of Indian -inland waters collected over a period of 25 years hav~ been incorporated in the generaland taxonomic part. .

. In addition to the genera and species reported from India, a list 'of genera andspecies of the Chlorococcales not yet reported from India but known from other partsof the world is given at the end of each fanuly with, as far as possible, original referenceSfor each.

It is not the object of !his work to attempt any new classification or new inter-pre~tio~ of available, information on the order. The main object as in the case of therest 'of the monographs in the Indian Algae Serits, is to bring togethe.x:all scatteredinformation on t\1e order for the- benefit of post-graduate and research students, fisherybiologists and others interested in the subject.

. The- author wishes to express his indebtedness to :(I) Late Pro£: M. O. P. Iyengar, Madras, his esteemed Professor, who initiated

him into the field of algology and who had been a valuable source of inspirationin the undertaking of this compilation.

(2) .Dr B. S. Bhimachar, Director, Central Inland Fisheries Institute,Barrackpore,. for kindly permitting the author to take up this work, his keen interest,in its completion and for kindly according the necessary permission'to"publish thesame.

(3) Dr M. S. Randhawa, Adviser, Planning Commission, New Delhi, for hiskeen interest in the present work, for many valuable suggestions and encouragementat every step.

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VI CHLOROCOCCALES

(4) Professor T. V. Desikachary, University Botany Laboratory, Madras,for kindly giving the author a number of valuable suggestions and helping witha number of references and photographs.

(5) Dr G. S. Venkataraman, Botanist, Indian Agricultural ResearchInstitute, New Delhi, for help in taking a number of photostats of text-bookillustrations. .

(6) Rev. Fr. Santapau, Director, Botanical Survey of India, for thel.~tintranslations of diagnoses of new taxa included in this monograph.

The author also wishes to express his special gratitude to Prof. B. Fott ofPrague in helping the author to procure a copy of Korshikov's (1953) work, andin generously supplying reprints of a number of his own papers. The author isalso thankful to several European and American authors, notably Prof. H. Printzof Oslo, Prof P. Bourrelly of Paris, Prof F. Chodat of Geneva, Prof T. Hortobilg)6..of Budapest, Prof. R. C. Starr of Indiana, and Dr F. R. Trainor of Connecticutfor being kind enough to supply reprints of some of their valuable papers.

CENTRAL INLANI) FISHERIES

CUTI'ACKM. T. PHILIPOSE

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PrefaceChlorococcales

MorphologyReproductionCytology and life-historyEcology and physiology .,Economic importance

Classification and PhylogenyHistorical

Synopses of the families ..Genera of the Chlorococcales

Indian ChlorococcalesChlorococcaceae

Chlorococcum'Trebouxia .,

CharaciosipnonaceaeCharaciosiPltim

CharaciaceaeCharacium ..Korshikoviella

Schroederia .,

Chlorochytriaceae . .Chlorochytrium

- KentrosphaeraMicractiniaceae

,Trochiscia _' .

Golenkin{a'. . . .Golenkiniopsis

Micractinium

TreubariaceaeDesmatractumTreubaria .,Pachycladon

r' ConococcUS .,Hydrodictyaceae .,

HydrodictyoideaePediastrum ..

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15283151545465 I

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101103103106106107108108III111111 I

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Sorastrum ..Hydrodictyon

TetraedronoideaeTetraedronCiosteridium

PolyedriopsisOocystaceae

LagerheimioideaeLagerhei .,Chodatella ..

DendrocystisChiorelloideae

ChiorellaPaimellococcus

EremosphaeroideaeOocystaenium

Oo~ystoideaeGioeotaeniumOocystisGiaucocystisNePhr.ocytium

Radiococcaceae

Dispora.Botryo'coccaeeae

Botryococcus

Dictyosphaeriaceae

DictyosPhaeriumWestella

DimorPhococcusSelenastraceae

Dactyiococcus -. .Ankistrodesmus

Quadriguia

CiosteriopsisActinastritm

Seienastrum

Nephrochiarrrys

Kirchneriella ..Gloeoactinium . .

Coelas traceaeCoelastrumBurkillia

Scenedesmaceae

Crucigenioideae

H~nia ..

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132133136136161164-166167167168171'72172176177177178178179187189193193195195199199203204208

.208210215216217218221222225227227234236236236

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Crucigenia ..Tetrastrum . .

~enedesmoideaeScenedesmus

Tetrallantos

'enera of Uncertain Systematic PositionElakatothrix

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Order CHLOROCOCCALES March and Orth. mut.et emend. Pascher, 1915

MORPHOLOGY

Members of this order are found mostly in 'freshwater and are free living,tached, endophytic or endozoic. A few forms also Occur in brack':sh water, ~n moist

'OIs,walls and on tree trunks, especially in exudations of sap. Some species of_'oreLl.'1..cJ.[tnochytrium,Characium,Oocystis, and Sykidion are marine. Scotiella has beenordel mainly as a constituent of snow floras, whereas some species of Scenedesmus

known to tolerate temperatures as high as 50-63°C obtaining in hot springs.rely, members of the order are parasitic or live in symbiotic association with fungilower groups of animals. _ _

The predominant phase in the life-history is a non-motile one. Formation of'spores or gametes may take place at the time of reproduction, but these swarmers

short-lived since they come to rest soon after their- liberation and remain p~iveing a prolonged period of vegetative growth before giving rise to motile cell~ again.

:getative-dIvision of cell is absent altogether or occurs only very rarely, the only cellision thar- takes place being at the time of reproduction.

The algae belonging to CWorococcales are unicellular, coenocytic or colonial',g. I, a-p). In its simplest form a CWorococcoid cell is unicellular and uninucleatein Chlorococcum,where sometimes, as in C. -humicolo and C. olivaceum,the swarmerst are liberated come to rest side by side and the resulting cells become crowded and

a stratum which has the false appearance of a colony. Occasionally, the cellalso be multinucleate, as in C. multinucleatum. In Chlorochytrium,PhyLlobium,and

'dochytrium,the.unicell is coenocytic and irregularly lobed or in the tbrm of branchingads. The protocoenocyte of Characiosiphonis usually club-shaped .and a number of

occur in clusters. Sometimes, as in Chlorella and Ank~strodesmus,a number ofare loosely aggregated with or without the aid of mucilage to form regular orlar colonies.. I~ Chlorel~a,which is usually colonial, sometimes solitary, this

egation is with the ~id of mucilage; whereas in Ankistrodesmusit is usually withoutaid of mucilage. In Selenastrumalso, the cells of the colony are in ,contact alongof their surface. In Gloeotaenium,a two to four celled compact colony is formedonnecting mucilage pads. In some others, particularly NePhrocytium, Oocystisallied genera, a simple type of colony is formed by a number of cells becoming

osed within the parent membrane which becomes gelatinized. NePhrochlamysnastraceae), on the other hand, has cells enclosed within a non-gelatinizingt cell membrade. A number of other genera, like Radiococcus,Kirchneriella,

'actin~umand Tetrallantos,are also colonial and enclosed by a mucilaginous envelope,

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FIG. 1. RANGE O' 1'I1"U.\II

a, ChlorocOccumechinozygolum STAJUl; b, C. OIlH"lIm RABENH.; c. SClnetllm1u1,¥lithii TElLiNG VAR. linea~-VAR. NOV.; d, lWllU/rum IIlras (EHl!-') RALJI;... CharluioJiphon rivularis IYSNG.; f. RJwdoe!r1IriNlft'JlI/IlIt/hidiJ LAOERg.; g. ~IIU/tIIJII.~nI VAR. inler7ntdium (B..oHLlN).G...S: Wanl h, GIOlOltunium loilllsbng,,;anum\,"~O.I I, DimorphococCUJ IWUlIUI A.. ISM""I j, $,ltnClJlrum gre"i" RBlNSCII.;

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OCCUJinfusionum NASG.;I, .If:::':::' ~'"'.c'thii LAGERH.:m. Kirch"'""""tor" (SCH)&!DLE)Bo~; p,.If ut._ III /tl.,./tI, VAR.JlipilahU (CilOIJ.)

,.,101.' 0, Nephroeyliumecd.1ns~1SIfI !~, I \), ~clJon r,lifulCJl1llll(1..)\..,('8"'" . j~"4t1

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MORPHOLOGY

. which is usually visible 'Only after staining. In the Dicty'Osphaeriaceae the individualcells 'Ofa c'Ol'Onyare held t'Ogether by filif'Orm branches f'Ormed by the parent cell

'membrane, and the c'OI'Onies-areregular (Dictyosphaerium)'Orirregular (Dimorphococcus),Iwith 'Orwith'Out a c'Omm'Onmucilagin'Ous envel'Ope. In the c'Ol'OnialHydr'Odictyaceae,the c'Ol'Onyis in the f'Orm'Ofa net-w'Ork, as in Hydrodictyon,or in the f'Orm~Ta regular'flat disc, as in Pediastrum,'Orit is a spherical c'OI'Ony,as in Sorastrum. In the C'Oelastraceae,I,thec'Ol'Oniesare usually regular and spherical as in m'Ostspecies 'OfCoelastrum'Orirregular

s in Burkillia. In the Scenedesmaceae, the c'Ol'Oniesmay be quadrate, as in Crucigenia,r rectangular with the cells arranged in a single linear 'Or d'Ouble linear series, as in'cenedesmus. In Crucigenia,Coronastrum,Hofmania, and s'Ometimes in Coelastrum,multiple'OI'Onies,in which a number 'Ofc'Ol'Oniesare held t'Ogether by lateral c'Ontact 'Or byemnants 'Ofthe parent cell membrane, are frequent. In Actinastrum als'O, multiple'Ol'Oniesare 'Occasi'Onallyf'Ound (Fig. I, I) but the individual c'Ol'Oniesin this genus areeld t'Ogether 'Onlyby lat~ral c'Ontact. Pectodutyon(Fig. XVII, I) is an interestingenus in which the c'Ol'Onyhas a cubical frame-w'Ork 'Ofgelatin'Ous strands with a singleherical cell at each 'Ofthe eight c'Orne~ 'Ofthe frame.~w'Ork. A number 'Ofsuch frame-'Orksj'Oined t'Ogether give rise t'Oa multiple c'Ol'Ony'Orsync'Oen'O.bium.

In Botryococcus,the cells are embedded in thimble like envel'Op~st'O f'Ormamewhat radiating c'OI'Ony,and a number 'Ofsuch c'Ol'Oniesmay be held t'Ogether by

.ugh mucilagin'Ous strands.'I}1e c'Ol'Onyin Nephrocytiumecdysiscepanumis in the f'Orm'Offan-shaped aggregates.

ere the membranes 'Ofdividing cells bec'Ome thick and stratified,.with the 'Outer layersmaining~. The outc!r layers then split 'On'One~ide while the inner -layers, whichcl'Osethe'cells, bec'Ome gelatinized. When the daughter cells divide again the same'Ocessis repeated, the entire structurel'O'Oking like a fan-shaped aggregate (Fig. I, '0).is type 'Ofc'Ol'Onyf'Ormati'Onsh'Owss'Omeanal'Ogy t'O th'Osein the Dicty'Osphaeriaceae

d the Chl'Or'Odendrineae(V'Olv'Ocales),particularly t'Othat in Ecballocystis(seeFritsch,'35, p. 160). A dendr'Oid type 'Ofc'Ol'Onyis als'Of'Ormed.in Ankistrodesmusfalcatus var.itatus(Fig. I, n). Iyengar (1962) has recently rec'Orded a new genus, Dendrocystis,which ~he cells are dendr'Oid as in Ecballocystis but many 'Of its: cells p'Ossess

ines as in Lagerheimia. _ .

In Dactylococcus, a number 'Of cells are placed end t'O end t'O farm a branched

ent'Ous c'Ol'Ony(Fig. I, k). -

The s~ape 'Ofthe cell als'Ovaries c'Onsiderably within the Ol:der (Fig. II, a-z, a.-I.).may be spherical (Chlorococcum,Chlorella, Golenkinia, etc.), 'Obl'Ong,ellips'Oid 'Or citri-

(Oocystis, Lagerheimia, Chodatella), 'Ov'Oid-ellipsoid, plan'O-c'Onvex, 'Or renif'Ormtyosphaerium), 'Ob'Ov'Oid,pyrif'Orm, fusif'Orm 'Or lance'Olate (Characium), cylindrical

drodic~on), club-shaped (Actinastrum), fusif'Orm, navicul'Oid, 'Obl'Ong-ellips'Oid"bi-cave, prismatic, 'Orarcuate (Scenedesmus),acicular, spiral 'Orc'Onv'Olute(Ankistrodesmus),

orm 'Orsigm'O,id(Schroederia),cuneif'Orm (Burkillia, Gloeoactinium),'Obl'Ong-cylindrical(a, FROM STARR, 1955; b, AFTER HODGETTS, 1926; c, j, m, ORIGINAL;

d, FROM G. M. SMITH, 1920; e, AFTER IYENGAR, 1936; f, AFTER LAGERHEIM;g, AFTER STOCKIdAYER;e...h. AFTER RICH, 1932; i, AFTERWEST; k, FROM G. M.SMITH. 1950; I, p. AFTERX::;.M. SMITH, 1920; n, AFTER CHODAT; 0, AFTER WEST).c, j (x 725) AND m (X 1500).

N.B.-All figures in this and subsequent pages reduced to about two-thirdthe original lae.

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FIG. II. CELL SHAPES(CONTENTSNOT SHOWN)

a, Chlorococcum (SPHERICAL); b, Coelastrum microporum. (OVOID); c, OO'Y!tis(ELLIPSOID); d, Dictyosphaerium ehrenbergianum (OVOID-ELLIPSOID); c, Characltnn.debaryanum (OBOVOID); f~ C. orissicum (PYRIFORM); g, Hofmania lauterbornn.-(SEMI-SPHERICAL);h, Scenedesm!ls quadricauda and i, Dimorphococcltsfritschii (OBLONG--CYLINDRICAL); j, Hydrodictyon reticulatum (CYLINDRICAL); k, Characium ambiguum(LANCEOLATE); I, Pediastrum ovatum (OVATE); m, Ankistrodesmusfalcatus (ACI?ULAR);n-o, Scenedesmus dimorphus and S. obliquus (FUSIFORM);p, Actinastrum hantzschil (CLUB-SHAPED); q, Scenedesmus perforatus (BICONCAVE); r, S. carinatus (NAVICULOID);s, Burkillia cornuta (CUNEIFORM); t, Dictyosphaerium indicum (p~~O-CONVEX);u, Scenedesmusprismaticus (PRISMATIC);V, Sorastrum spinulosum (CORDATETO REN1FO~M);W, Selenastrum gracile (SICKLE-SHAPED); x, Scenedesmus arcuatus VAR. capt/atus

(ARCUATE); y, Dictyosp~aerium reniforme (iNIFORM); z, Kirchneriella contortaI

4 CHLOROCOCCALESMORPHOLOGY

or cordate (Dimorphococcus),reniform to cordate (Sorastrum), semi-lunar or vermiform

(Kirel/TIeriella),sickle-shaped (Selenastrum), sausage-shaped (Tetrallantos), triangular,Ruadrate, tetrahed!~l, cruciate or polygonal (Tetra~dron)or ovate, polygonal or H-shaped(P,diastrum). In Dlmorphocorcus, as the .na~e Itself suggests, there are two types'o{ce1lsin the same colony, one oblong-cyhndrIcal and the other sub-cordate to cordate.

f !The shape of cells might also vary .with age, the older cells having a shape which isfrequently different from that of the young cells.

Cell wall.. As in other members of the Chlorophyceae, the cell wall" .. (F.ig. "III, a-z) is mainly composed of cellulose, but sometimes pectose layers of~lilmuciIage are developed external to the cell membrane proper.

to"i' In the simpler forms of the Chlorococcales, as in the Chlorococcaceae, the~:eUmembrane proper is usually smooth, thin and close-fitting in young cells, frequently'becoming thicker in old ones. However, in the vegetative cells of Chlorochytrium,thejpunetangfa of Phyllobium and the resting cell of Kentr~sphaera,all belonging to the~orochytriaceae, the cell wall is thick and stratified. The lamellation of the cellwan is sometimes seen in other families also. Thus, in the vegetative cells of

~lttunella and E~centrosphaera(Oocystaceae) and the old cells of Burkillia..dissolvensSkuja:(Codastraceaeh the outer wall is thick and layered. CharaciosiPhon(Characiosiphon-~«i:eae)has a firm. lamellated outer wall. In Hydrodictyon indicum Iyengar, the cell~n is not only lamella ted, but has u:.o knob-like projections into the protoplasm.)n Desmatractum(Treubariaceae), the cell wall is in the form of two envelopes, one

'.~~imuiediatelyexterior to the protoplast and close fitting--and the other in two pyramidal~ves, the space betw~en the two being filled Fith mucilage. The pyramidal halves

'Calso joined at the median portion and are provided with longitudinal ridges. In,:iiI/la (Oocystaceae), the longitudinal ridges are spirally twisted. KeriochlamY.f._Pascher

i)in interesting alga in whIch the cell wall is thick with a number of refractive bodies',,~'P.unknownnature embedded in it, giving it an alveolar appearance. .

( Recent studies with the electrone microscope (Moner, 1955; Desikachary, 1957)'.~~veshown that eyen in Pediastrum the apparently simple cell wall is made up~o.~Yers, a continuous internal membran~ and a hexagonally reticulate outer layer:- ,~~, also..Deaso!}'s (1961) detailed study of the structure and composition of the cell_~allof several genera of Chlor~coccalean algae, using stains and employing micro-

~eDlical analys-esj.. . ,.

t. According fo Parker (1964), who investigated tJie structure and chemical compo-:~.iionof three Chlorophycean algae, the cell wall of Pediastrum tetras contains a crystal-~littepolysaccharide composed of D-glucose and D-mannose which forms a non-'p!i9'ofibrilIar net-work of interwoven chains of rings. The cell wall polysaccharide is~.ther a gluco-mannan or aglucan intimately associated with mannan.

.' A large number of Chlorococcales, unicellular as well as colonial, have their cell~ ornamented in different ways. . The simplest form of ornamentation is seen in

.(VERMIFORM); a" Dimo~ph0!J!C.CI{S.fritsch~i (CORDATE); b" Tetrallantos lagerhe~mii(SAUSAGE-SHAPED);c" Kzrchnerzella lunarzs. (SEMI-LUNAR); d" Tetraedronmutzcum(TRIANGULAR); c" T. pusillum (CRUCIATE); f,; Pediastrum duplexvAR. gracillimum(H-SHAPED); g" Schroederia setigera (SIGMOID); h" Ankistrodesmus convolutus(CONVOLUTE); i" A. spiralis (SPIRAL); j" Tetraedron quadratum (Q.UADRATE);k" T.minimum (TETRAHEDRAL);Ir, Pedirzstrum muticum (POLYGONAL).4>

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CHLOROCOCCALES

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FIG. Ill. CELL WALL, ITS LAMELLATIONS, ORNAMENTATIONS, OUT-GROWTHS, -AND MODIFICATIONS

a, Tribouxia humicola (TR~BOUX) WEST ET FRITSCH (P-PYRENOID);b, Te/raedron minimum (A. BR.) HANSG.; c, Muriella magna FRITSCH ET JOHN; d,Hydrodictyon indicum IYENG.; e, Ken/rosphaera facciolae BORZI (RESTING CELL);f, Burki/lia dissolDens SKUJA; g, Ceras/erias irregulare G. M. SMITH; h, Trochisciare/icularis (REINSCH) HANSG.; i-j, Desma/rae/um bipyramida/um (CHOD.) PASCHER;

k, Mycacan/hococcus an/arc/icus WILLE; 1, Te/raedron horridum WEST; m, Trochisciaaspera (REINSCH) HANSG.; 0-0, Sco/ie/la antarctica FRITSCH; p, Pedias/rum araneosumVAR. rugulosum (G. S. WEST) G. M. SMITH; q-r, Gloeo/aenium loitlesbergerianumHANSG. (p-p'-POLAR CAPS); S, Keriochlomys styriaca PASCHER; t, Dictyospliaerium

pulche/lum WOOD (m-MUCILAGE; t, CONNECTING THREAD FORMED FROM MOTHERCELL MEMBRANE); u, Oocystis g/oeocys/iformis BORGE; v, Golenkinia radia/a CHODAT;

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MORPHOLOGY 7

.,

cell walls which are finely punctate, coarsely granulate or verrucose. A number ofspecies and varieties of Tetraedronand Pediastrumthus exhibit cell walls which range frompunctate to coarsely granulate. A similar cell wall may be present in Cerasteriasandsome species of Scenedesmus. In Trochisciaand some species of Pediastrum, the ornamen-tation is in the form of a net-work of ridges. In the latter genus the cell wall may alsobecome undulate to rugulose, especially where it adjoins the wall of another cell. InMycacanth'%coccusHansgirg, the cell wall is verrucose or spinous on the outside. In anumber of other genera, short or long spines or bristles are formed from the exterio~surface and these are usually solid. The spines of Tetraedronand Scenedesmusare usually

, short or long, whereas the spines or setae of Treubaria (incl. Borgea) are very long andsometi~es gelatinous. Bristles, are usually seen in unicellular genera like Golenkinia,Golenkiniopsis,Polyedriopsis,Chodalella, Lagerheimia and Franceia and the colonial generaMicractinium (incl. Errerella Conrad) and Palmellochaete,the number and position of thebristles varying with the genera. In Echinosphaerella,the spines are more or less gela-tinous. These spines anq bristles are usually associated with the' pelagic habit of theforms concern~.

The parent ~~ll membrane sometimes becomes partially gelatinised at the -timeof reproduction -and -forms an envelope for the daughter cells, as in Oocystis. InGloeotaeniumthere is not only an outer mucilaginous envelope, but th~re are also bandsof mucilage betWeen -the cells of colonies with apical and equatorial caps for the cells.

The outermos't layers .of this envelope contain refractive calcit~. .' The.!e are also othergenera like Kirchneriella, Gloeoactinium,Radiococcus,_COetlOCOCCUS,Coeiiochloris,Coenocystis,Dictyosphaeriumand Hofmaniain which there,is an outer colonial mucilaginous envelope,and it may be lamellated as in DictyosPhaeriumpulchellum. In Hofmania,rupturedfrag-ments of the- parent cell membrane as well as the mucilage remain outside the newcolony. These mucilaginous pectose layers d'iliibit all stages from solubility to insolu-

bility in water and formation of the mucilage probably continues throughout the )ifecycle of an alga (Fritsch, 1935). In the Dictyosphaeriaceae, during autospore forma-tion, th~ parent cell membrane gets fragmented. These roll up and become connect-ing tl~reads for the cells of colonies. In g~nera like Coelastrumalso, sometimes multiplecolonies are held together by contact or by bt;.oken b[ts.. of the parent cell wall.

Quite recently, Edelstein and Prescott (t964-) have described. an interestingnew genus Rayssiella, allied to Nephrocytium, ~ith the single species R. hemisphaerica,in which autospores which are polar and hemispherically arranged, have intercon-necting gelatinous: threads, formed by the dis.tion of the mother cell wall.

Protoplast. The protoplast (Fig. IV) fills the cell cavity in young as welt asold cells; or'rarely, it is vacuolate in the centre, as in Chlorococcumvacuolatum.However,

- - I .-+ w, Coe/as/rum 're/icula/um (DANG.) SENN (P-CONNECTING-PROCESSES);S, SPLIT IN

THE REMAINSOF THE CELL WALL THROUGHWHICHDAUGHTERCOLONYHAS BEENLIBERATED); x, Hofmania lau/erbo~nei (SCHMIDLE) BRUNNTH. (G-MUCILAGE;W,REMAINS OF CELL MEMBRANES);y, SceMdesmus arma/us VAR. spinosus FRITSCHETRICH; z, Chodatella ciliata (LAGERH.) LEMM.

(a, VIZ. AFTERCHODAT; b, AFTERG. M. SMITH; C, FROMFRITSCHET JOHN,1942; d, FROM IYENGAR, 1925; e, AFTER BORZI; f, AFTERSKUJA, 1949; g, FROMG. M. SMITH, 1950; h, m, AFTER WEST; i, AFTER PASCHER; j, AFTER KORSHIKOV;k,FROM KOL; I, AFT~R PRINTZ; n-o, AFTERFRITSCH; p, FROM G.M. SMITH 1920;q-r, AFTER STOCKMAYER;S, FROMTHOMPSONIN G. M. SMITH, 1950; t, w, AFTERSE"N; H, AFTER BORGE; x, AFTER OLT/ofANNS; y, AFTER FRITSCH ET RICH, 1930).

8CHLOROCOCCALES

in some adult cells, as in ErtmosPhaera, the cytoplasm is in the form of a peripherallayer with strands radiating towards the centre, where the nucleus is suspended. Theperipheral layer and sometimes the radiating strands contain a number of disc-shapedchloroplasts. In CharaciosiPhonthe protoplasm is restricted to the periphery with cellsap in the central cavity. This genus is also peculiar in that there are a number ofseparate protoplasmic bits one layer thick forming the lining on the inner side of the

cell wall, and these bits are far apart at the basal regoin of the coenocyte, whereas theyare close to each other in the apical region. These discrete protoplasmic units lyingapart are also connected to one another by delicate strands of cytoplasm, not unlikesome species of Volvox (Iyengar, 1936). The increase in number of protoplasts areclearly seen in the germlings (Fjg. IV, i-k).

h

a c

g

a, Trlbouxin SP. ; h, Characium terres/ris KANTH.; c, Bracleacoecus minor

(CHODAT) PETROVA, (a-c, WITH PROTOPLASM FILLING THE CELL; a, UNINUCLEATE;h-c, MULTINUCLEATE); d, Eremosphatrn viridis DE BARY, OPTICAL SEC'lJON SHOWING

CENTRAL NUCLEUS AND RADIATING CYTOPLASMIC STRANDS; e-k, CharaciosiPholl,rivu/aris IYENGAR, e, PROTOPLASTS IN THE UPPER PART OF THALLUS; f, P~OTOPLASTSSHOWING (n) NUCLEUS, (py) PYRENOID, (v) VACUOLE AND (w) CELL WALL; g'-h,PROTOPLASTS IN THE LOWER PART OF THALLUS; h, SURFACE VIEW SHOWING

PROTOPLASMIC CONNECTIONS; g, IN EDGE VIEW; i-k, GERMLINGS SHOWING 4 TONUMEROUS PROTOPLASTS;j, IN OPTICAL SECTION SHOWING 5 OF THE 8 PROTOPLASTSAND THE CENTRAL CAVITY.

(a, c, FROM STARR, 1955; h, FROMKANTHAMMA,1940; d, FROM MOORE;e-k, AFTER{vENGAR, 1936,1954).

'~"'

I-

PY,;.

vii: ·....

f.

FIG. IV. PROTOPLAST

MORPHOLOGY 9

~

Nucleus. Usually there is only a single nucleus (Figs. IV, XIV) in each cell.In young cells of Chlorococcllmit is placed in the region of the notch in the chloroplast.However, in older cells (Fig. VI, h) or during successive division of the protoplast thenumber may increase, each bit of the protoplast receiving a nucleus. This increasein number is probably in preparation for the formation of reproductory units(Fritsch, 1935). Examples are species of Chlorococcum, Tr!bouxia, Chlorochytrium,EremosPhaeraand Chlorella. Sometimes, as in Chlorococcummultinucleatum Starr, themature cells have many nuclei even without accompanying division of the protoplast.The same is tht! case with Ai:tinochlorissphaericaKorsh. and PseudochlorotheciummucigenumKorsh. (Fig. VI, p; VrrI, i).

In ~enera like Tetraedron, Characium,Hydrodictyon,Pediastrum, Sorastrum, Coelastrum. and probably Scenedesmus,the mature cells are multinucleate, and, in these algae,

simultaneous division of the protoplast into a number of bits takes place, each bitreceiving a nucleus. In Characiosiphonthere is a single nucleus in each of the nakedprotoplasmic bits and it is in the strict sense a large coenocyte.

Chloroplast. The chloroplast (Fig. V, a-z) typical of many Chlorococcaleshas been described as 'chlorococcoid' (Fritsch,' 1935). It is.single, parietal a9d inthe form of a hollow sphere with an aperture of varying size on one side,. Chlorococcumhumicolois a typical example. According to Starr (1955), t~ parietal hollow sphere isfundamentally cup-shaped as seen in Chlorococcum echinozygotum, C. hypnosporumandC. minutum. In ~ome of the Dictyosphaeriaceae and in species of Chlorellaand Golenkinia,the chloroplast is typically' cup-shaped. This is almost like that obtaining usually inChldmydomonas. In. Botryosphaera sudetica,. the cup-shaped chloroplast h¥ finger-likelobes at the front c:nd. In' still others, like Characium, Schroederia, Actinastrum -and

NePhrocytium, it is parietal and very' often partially girdling the cell. In Pediastrum,ScenedesmUs,Coe/astrumand a number of other genera, the parietal chloroplast is in theform of a flat band. Sometimes,'as in Characium and Tetraedron, it is parietal inyoung cells, but becomes rather diffuse in old cells.

Though th'e chloroplast in most of the Chlorococcales coi\forms to one of theabove cat~gories,. yet in a number of genera and species it is of different nature : inTre~uxi~, it is axial and massive with the periphery often lobed or wrinkl~; inChlorochytrium,Kentrosphaeraand Phyllobium, though the chloropl~t is usually parietaland cup-shaped in young cells,)t becomes stellate in old cells and in gametangia, withradial branches' expanding to parietal. lobes; ?tctinochloris.Korshikov, Macrf!chlorisKorshikov, Burkillia dissolvens Skuja and CharaciosiPhon Iyengar have also stellatechloroplasts; in Spongiochlorisand Dictyochloris (Starr, 1955), however, it assumes theform of a fine net-work of interlacing strands; and in Hydrodictyonalso, the single chloro-plast is in the form of an elongated parietal reticulum.

. Electron microscopical studies on the chloroplasts of a number of green algae,including Chlorellaand Ankistrodesmus(Albertsson and Leyon, 1951; Desikachary, 1959)have revealed that, unlike the higher plants, where the chloroplasts have a lamellatedstructure with thick grana, the chloroplasts of these algae have a uniform structure,without a trace of the grana, and are made up of parallel lamellae about 70-100Aothick running through their entire length. The lamellae also appear to be bundledin groups of four to eight. Stroma lamellae are absent and the globular stroma

I'litl'

r.

10

0,'"

:L =: .':

...~.. ...:..:

_0":::)0'". . ~.. ':.-;.':-

.: I'.':'~ "'1/,:.:

,"" ~':':~':.

t

CHLOROCOCCALES

e

k

"~,

a-b, ChlorococcumSP; c, .Trlbouxia humicola (TR~BOUX) WEST ET FRITSCH; d, Actino-chloris sphaerica KORSH.; e, Chlorella vulgaris BEIjERINCX; f, Golenkiniopsis minutissima (ivENG.ET BALAKR.) COMB. NOV.; g-h, Burkillia dissolvens SKUjA; i-j, CharaciosiPhon rivularis IYENG.(i. A GERMUNG; j, AN ADULT CELL); k, Scenedesmus denticulaJus LAGERH.; I-ni, Dictyococcu.svarians GERNECK; n, Dictyochloris fragrans VISCHER EXSTARR; 0, ActiJesmium hooken REINSCH;p, Characium sieboldi A. BRAUN; q, C. ornithocephalum A. Br.; r, Oocystis borgei SNOW;s, Hydrodictyon reticulatum (L.) LAGERH.; t-u, Planktosphaeria gelaJinosa G. M. SMITH;v, Botryosphaera sudetica (LEMM.) CHODAT (2 CELLSFROMA COLONY); w, Oocyslis panduriformisWEST; z, Eremosphaera viridis DE BAIlY.

r

FIG. V. CHLOROPLASTS AND PVIlENOmS

v

-+

i

J

. ,

l

~

MORPHOLOGY II

occurs in relatively thin layers between these lamellae or bundles of lamellae. . Anouter membrane, similar to the one seen in the chloroplasts of higher plants, has alsobeen shown to be present in the chloroplasts of the algae, except in the blue greenalgae (Desikachary, t. c.).

The number of chloroplasts in a cell might increase probably in preparationfor cell division (Fritsch, 1935) but in a number of genera the presence of more thanone chloroplast in a cell is a constant feature. Among the unicellular forms, Dictyococ-cus, Trochiscia, Palmellococcus,Eremosphaeraand Oocystaeniumare examples. Dictyococcushas a number of parietal lenticular or polygonal plates bearing a variable numberof centripetally projecting processes(seeStarr, 1955). Trochisciaand Palmellococcusalso have usually several parietal disc-like chromatophores. In Eremosphaerathere ar~numerous discoid chloroplasts in the parietal cytoplasm and in the cytoplasmic strandsextending to the centre of the cells. Oocyslaeniummay have as many as 209 lanceolateto irregular chloroplasts in its cells. In Characium, occasionally there may be severalparietal chloroplasts. In Oocystis, the number varies from one to many and it maybe parietal and laminate (Fig. V, r), stellate, or, when in large numbers, disc-shaped(Fig. V, w). In Planktosphaeria, a colonial planktonic genus, the vegetative cellspossess several separate chloroplasts, each with a pyrenoid. In DictyosPhaerium,thenumber might vary from one to two, and in Cruc:6o,tiafrom one to four. Characiosiphonhas a stellate chloroplast in each of its protoplasmic units.

All the types of chloroplasts mentioned above, except the numerous discoid type,are found irithe single family, the Chlorococcaceae. Ho~ever, there are also forms inwhich the chloroplast or chlorophyll 'is absent altogether. Thus, in RlwdochylriumLagerheim, a parasite living on the leaves ofphanerogamic plants, ther~is no chlorophyll,the frequent red colour of the threads being due to oil drops containing a redpigment. Hyalocharacium Pascher, Prototheca Krueger, Mycoletraedron Hansgirg andHyaloraphidiumPascher et Korshikov are further examples of colourless Chlorococcales.They are colourless parallels of Characium, Chlorella, Tetraedron, and Ankistrodesmus

res,pectivdy. Gloxidium Korshikov, a member o( the Selenastraceae, MyurococcusHansgirg, and Mycacanthococcus,(considered by Printz, (1927) and Bourrelly (1959)as- members of the Tetrasporaceae and by Fritsch as probable members of theChlorellaceae) are also colourless.

In Palmellcoccus variegatus the green colour is lost when the alga is grown onorganic media like agar. Glaucocystisis. a colourless member of the Oocystaceae whichlives symbiotically with a rod-shaped member of the Chroococcaceae (Myxophyceae).The radially arranged chloroplast-;like structure is really the blue green component ofthe symbiont.

The pigments of the Chlorococcales, as in the rest of the Chlorophyceae, areconsidered more or less the same as those in higher plants, viz., chlorophyll-A,

-+ (a,b, d,n, FROMSTARR, 1955(d, ASRadiosphaera dissecla (KORSH.) STARR; V, CONTRACTILEVACUOLE); c, FROM CHODAT; e, FROMGRINTZESCO; f, AFTER IYENGAR and BALAKRlSHNAN,1956 (AS Golenkinia minulissima IVENG. ET BALAKR.); g-h, AFTEIl SKUjA, 1949; i, AFTERIVENGAR, 1954; j, FROM IVENGAR, 1936; k-I-m, FROM GERNECK; 0, FROM MILLER; p-q,FROM A. BRAUN; r, AFTER RICH, 1932; S, AFTER KI.EBS (PVRENOID; N, NUCLEUS); t-u, FROMG. M. SMITH, 1950; v, AFTERKORSHIKOV,1953; W, AFTERWEST; z, AFTER MOORE).

12 CIlLOROGOCGALBSMORPHOLOGY 13

chlorophyll-B, carotin and xanthophyll. One of the reasons why Botryoeoeeushasbeen brought back from the Xanthophyceae to the Chlorophyceae is that it possesseschlorophyll-B, which is absent in the Xanthophyceae. Apart from the carotin presentin the chloroplasts, carotinoid pigments may occur outside the chloroplasts in theform of haematochrome, which is very often dissolved in fat globules (Fritsch, op. c.).Though haematochrome is not very common in the Chlorococcales, ~tmight occasionallyoccur, as in Botryoeoeeus,Chloroehytriumand Phyllobium. In Palmelloeoeeusminiatus val'.porPhyrea, the pigments phycocyanin and phycoerythrin have also bee~ reported inthe chloroplast (Boresch, 1922).

Pyrenoid. In most of the Chlorococcales there is only one pyrenoid in eachchloroplast, rarely more; but in a few forms there is always more than one pyrenoid inthe chloroplast. In some of the forms pyrenoid is indistinct"or absent altogether. Thepyrenoid is usually surrounded by a starch sheath, but sometimes is naked as inBotryoeoeeus.

In Chloroeoeeum,the single pyrenoid (Fig. V, b) is lateral, being phiced oppositethe aperture of the chloroplast. In older and larger cells, it might become several(Fig. VI, h). In Oocystis, usually there are a number of chloroplasts, each with apyrenoid. The same .is the case with Planktosphaeria and Oocystaenium. In Chiorella(Fig. V, e); the single pyrenoid is either distinct or indistinct, or sometimes there is nopyrenoid. In a nl!mber of other genera, like Tetraedron,Ankistrodesmusand Daetylococcusalso, the pyrenoid mayor may not be present. :_

Some of the Chlorococcales possess more than one pyrenoid in the chloroplast:e.g., one to fOlIr per chloroplast in EremosPhaera,and one to two in Desmatraetum.Sehroederiaand CMracium also occasionally show more than one pyienoid in the chloro-plast. EetogeronDangeard is an interesting epiphyte with numerous pyrenoids. Theold cells of Chloroehytriumhave a number of pyrenoids scattered in the chloroplast: Thereticulate chloroplast of Hydrodic.tyo[l(Fig. V, s) has also a number of scattered pyrenoids-.Genera like Dictyoeoeeus,Dictyoehloris, Gloeoaetinium,Pseudoehlorotheeium,Dendrocystis anda few others do 'not have any pyrenoid.

In some of-the Chlorococcales like. Tetraedron,Pediasij-umalld Coelastrumithe singlepyrenoid does not divide at the time of cleavage of the -p.rotoplasm to produce daughtercells, but r~!Ilains in one of the bits. This pyrenoid disappears later and each'daughter c~ll develops a new pyrenoid (Geidel', 1924) whereas in, some, like.Chloroeoeeum, Chloroehytrium, Tribouxia, Chlorella' and Dictyosphae;ium, the pyrenoidsdivide along with successive divisions of the protoplast so that .each daughter cellreceives one.

Compound pyrenoids consisting of two pieces have been reported by Geidel'(1926) in a number of algae, including Dietyosphaeriumpulehellum. I t has been consi-dered that there are as many sheaths in such algae as there are segments of pyrenoids.

, Electron microscopical studies of the pyrenoids of green algae (Leyon, 1954;Desikachary, J959)- have shown that, like chloroplasts, they are also lamellated, thelamellae being three; to four times as thick as the chloroplast lamellae and are .conti-nuous with the latter. However, the pyrenoids of Chlorellapyrenoidosaand some otheralgae fixed in an active state showed only very dense pyrenoids devoid of any internalstructure (Albertsson and Leyon, 1954; Leyon, 1954)..

Vacuoles. Contractile vacuoles, normally associated with the motile cells of theVolvocales and of other flagellate algae, are usually absent in the Chlorococcales. How-ever, ApioeoeeusKorshikov, TrigonidiumPascher, some speciesof Chloroeoeeum(including,Hypnomonas Korsh.), SpongioeoeeumDeason and Bieuspidella Pascher and young cellsof DesmatraetumbiPyramidatumand Troehiseiaaeieuliferaare characterized by the presenceof one to two contractile vacuoles, usually sitUated on one side' of the chloro-plast (Fig. VI). In AetinoehlorissPhatricaKorsh., there are several contractile vacuolesbetween the lobes of the chloroplast in the periphery of the cell. CharaeioehlorisPascher,which resembles a Charaeium, possesses numerous contractile vacuoles scattered in thecytoplasm. Charaeiosiphon,lyengar, another interesting genus, has two to five contractilevacuoles in each protoplasmic unit of a large coenocyte. Korshikov (1953) keptthe coccoid forms with contractile vacuoles under a separate series,. the Vacuolales,under his Protococcineae, whereas others like Bourrelly (1958a, 1958b, 1959) and Fott(1959) included them under a separate order, the Tetrasporales.

Contractile vacuoles also occur in the zoospores of a number of genera belongingto the Chlorococcaceae and Characiaceae, the zoospores of AeanthosPhaera,Polyedriopsisand in the amoeboid zoospores QfGolenkinia and Marthea, the usual number being two.In Chlorococeummulti~ucleatum Starr, though nor!llally there are only two contractile

_ vacuoles in the zoospore, occasionally the zoospore is larger and contains more than twovacuoles. Several contractile vacuoles (2-6) have also been reported in the zoosporesand gametes of CharaeiosiphonIyengar and in the egg of DietyosphaeriumindieumIyengarand Ramanathan. Non-contractile vacuoles may also be found in the protoplast ofsome of the Chlorococcales. Thus, in some species of Chloroeoeeum,.JikeC. vaeuolatum,the centl-al cytoplasm is vacuofate in actively growing cells. In the germlings ofCharadosiphon, there are several vacuoles, but in the adult alga there is only a singlelarge central vacuole filled with sap. The cytoplasm of Eremosphaerais peripheralwith radiating strands towards the centre leaving several large vacuoles in between.Immature cells of Hydrodietyon, developed from zoospores, have innumerable minuteva<;:uolesin the cytoplasm. These gradually increase in size and two or more coalesceto form a single va,cuole. Ultimately there is only a single large vacuole in the centre(Smith G. M., 1950). - -

,Eye-spot or StigDla. Though the adult cells of the Chlorococcales (with t~e ex-ceptio~ of some species of BieusPidella)do not possess eye-spots, the motile reproductorystages very often show them (Fig. VI, b-d, i, 1,0, q,). Thus, the zoospores and gametesof Chloroeoeeumare usually provided with a linear streak-like eye-spot. Normally, itdisappears when the zoospore comes to rest or shortly after a zygote is formed by thefusionof the gametes. Similar eye-spotsare also found in the zoosporesof SpongioehlorisStarr, Tetraedron bitridens Beck-Mannegetta, Dietyosphaerium terrestre Fritsch and Johnand in the antherozoids of. Dictyosphaerium indieum Iyengar and Ramanathan. InFernandinellaalpina val'. semiglobosaFritsch and John, the linear eye-spot of the zoosporeis more prominent and projecting. The zoospores of Desmatraetumbipyramidatum havea prominent disc-like eye-spot and the zoospores and gametes of Charaeiosiphonpossessa fairly large elliptic eye-spot. The amoeboid autospores of Marthea also possessan eye-spot. Chloroeoeeummultinucleatum is an interesting instance in which thelarger zoospores are provided with two eye-spots. Korshikov (1953) has reported

11

a

v

0"

o po '-.' e

r-~.,

s

CHLOROCOCCALES

v

f: fit:... s

p p :.:;::-.:: cb':'.>,

v

n

gy

I

ph

~k

p

t).t Q'..

".~. r

,-

c.Y.

s.t.n

q

FIG. VI. PYRENOIDS, NUCLEUS, CONTRACTILE VACUOLES, STIGMA, AND CIUA

a-b, Chlorococcumchiorococcoides (KORSH.) COMB. NOV.; a, IN OPTICALSECTION; b, SWARMER; c-d, ZOOSPORES OF C. mul/inucleatum STARR; c, A NORMALZOOSPORE WITH ONE STIGMA, ONE PYRENOID AND TWO CONTRACTILEVACUOLES; d, WITH LARGER NUMBER OF THESE; e, ApiocoC&USconsoda/usKORSH.; f, Characium pluricoccum KORSH. (WITH A NUMBER OF P.YRENOIDSAND A SINGLE NUCLEUS; g, Characiochloris characioitfes (KORSH.) PASCHER;h, Chlorococcumhumicolo (NAEG.)RABENHORST, AN OLD CELL WITH SEVERALNUCLEI; i-k, Characiosiphon rivularis lYENG.; i, ZOOSPORE; j-k, GERMLINGS(LARGE NUMBER OF CONTRA~LE VACUOLES IN g, i-k); I, ZOOSPORE OFDictyochloris fragrans VISCHER EX STARR WITH SLIGHTLY UNEQ.UAL CII..IA ANDSTIGMA AT HIND END; m, BicusPitklla roslrum-aquilae PASCHER. WITH 1WO ~

REPRODUCTION 15

)

an eye-spot in the daughter cells of Trochiscia aciculijera, which probably indicatesthe possible formation of zoospores in this species.

Normally, the eye-spots are situated in the anterior half of the cell, but in thezoospores of Bracteacoccusminor (Chodat) Petrova and of Dictyochlorisfragrans Vischerex Starr the small disc-shaped eye-spot is placed in the posterior half of the cell, that ofDictyochlorisbeing right at the hind end. .

Eye-spots are not always present in the motile stages of the Chlorococcales. Thus,.the _zoospores and gametes of Trebouxia do not have an eye-spot, and in Characium itmayor may not be present.

Other cell inclusions. Other cell inclusions .are mostly the same as those inrest of the Chlorophyceae. Food reserves in the form of solid carbohydrates, mostlystarch granules, might sometimes accumulate in the cells. In Chlorochytrium andBotryococcus,frequently oil drops containing a red pigment, probably haematochrome(Fritsch, 1935), are found. It may also be densely packed with starch grains. Thegametangia of Phyllobium are also sometimes coloured red by the presence of haemato-chrome, and oils occur within the cells of Tribouxia (Brunn thaler, 1915), Spongiochlorisand in some species of.Chlorococcum(Starr, 1955). In Dendrocystisthere is a- round fatbody. inside a special vacuole on either side of a central nucleus, and these give the falseappearance of pyrenoids.

REPRODUCTJON

Reproduction is either asexual or sexual. There is hardly any vegetative re-produ~tion, except that in the Dictyosphaeriaceae and Botryococcaceae where frag-mentation of large colonies formed by the successive divisions of the cells into groupsoffour takes place (Fritsch, 1935). The f~ily Chlorosphaeraceae, which some authorsinclude under the Chlorococcales while others treat as a separate order, however,shows vegetative cell division. . .

Asexu~ reproduction. Asexual reprod.uction (Figs. VII-XI) is mainlyeffected by the formation of biflagellate, rarely quadriflagellate, zoospores or by the

. formation of autospores or a~tocolonies-fromeach parent cell. On the basis of thesetwo modes of asexual reproduction, -viz., the zoosporic and azoosporic' ~ethods, theChlor6coccales were formerly classified (Brunnthaler, 1915) into two broad series, the" Zoosporinae " and the" Autosporinae "'. According to Fritsch( op.c.),this ~Iassifica-tion, though convenient, does not reveal the real affinlties of the various families.

Moreover, a few genera (e.g., Desmatractum, Tetraedron)may show both zoospore as wellas autospore formation.

~PYRENOIDS AND ONE STIGMA; n, LIBERATED AUTOSPORE OF Trochiscia aciculifera(LAGERH.) HANSG. SHOWING CONTRACTILE VACUOLE AND STIGMA; 0, ZOOSPOREOF Acanlhosphaera zachariasii LEMM. SHOWING STREAK-LIKE STIGMA AND FOUR CILIA;p-q, AClinochloris sphaerica KORSH.; p, VEGETATIVE CELL WITH SINGLE PYRENOIDAND A NUMBER OF NUCLEI AND CONTRACTILE VACUOLES; q, SWARMERS;r-s, GlaucosPhaera vacuolala KORSH. SHOWING A NUMBER OF VACUOLES;n, NUCLEUS; p, PYRENOID; S, st., STIGMA; V, C. V., CONTRACTILE VACUOLES.

(a-b, AFTER KORSHIKOV, 1926 (AS HyptlOmonas chlorococcoides KORSH.);C, d, I, FROM STARR, 1955; g, AFTER KORSHIKOV (AS Chlamydomonas charadoitksKORSH.); h, AFTER BRISTOL; i-k, AFTER IYENGAR, 1936, 1954; m, FROMPASCHER, 1932A; f, n-o, FROM KORSHIKOV, 1953; p-s, AFTER KORSHIKOV, 1953).

,

16

~;.;..,..;"tV

'::;;tr.;~~e

CltLOROCOCCALES

~<

~p ~. Q,- q

",.c~l.D: ~iJ.!.

$

~. - ~

-

f;:.ii ""

.

,(",;;

Y'-

.

?:.:_ - .::'. - r' -. ':~ - -. .. . ,

u v W )( 'l

FIG. VII. ASEXUAL REPRODUCTION (BY ZOOSPORES AND APLANOSPORES)IN THE CHLOROCOCCACEAE, CHARACIOSIPHONACEAE, CHARACIACEAE,

CHLOROCHYTRIACEAE, AND TREUBARIACEAE

a-b, CLEAVAGE OF PROTOPLAST AND LmERATION OF ZOOSPORESIN Chloro-coccum hypnosporum STARR; c-e, g-i and, t, DIFFERENT TYPES OF ZOOSPORESIN THESPHERICAL CHLOROCOCCACEAE; c, Chlorococcum sP.; d, Spongiochloris spongiosa

STARR; e, Actinochloris sphaerica KORSH.; II ;.TI-ibouxia SP.; h, Spo,ngiochloriseXcentric a STARR; i, Chlorococcum humicolo. (NAEU.) RABEN H.; t, Bracteacoccus

minor (CHOD.) PETROV'A.; f, Chlorococcuminfusionum-(SCHRANK) MENEGHINI,APLANOSPORES; j, Neochloris aquatiea STARR, RELEASE OF ZOOSPORES FROMSPORANGIAL CELL WITHIN A GELATINOUS VESICLE; k, 1 andp, q, u-x, Characium

REPRODUCTiON 17

Zoospore formation in its simplest form is seen in the Chlorococcaceae, forexample, Chlorococcumhumicolo (Naeg.) Rabenh. Here, when ordinary cells reach acertain size, the protoplast divides successively into two, four, eight, or more bits. Thenaked protoplasmic bits, which assume an ovoid or oblong shape, develop two flagellaand are liberated by the rupture of the parent cell membrane. These zoospores mayhave a common vesicle at the time of liberation, but it disappears almost immediately.After moving about for some time the zoospore withdraws its cilia and becomes rounded.A cell membrane is secreted and the alga begins a new vegetative phase. Whenseveral swarmerssettle down side by side, the resulting cells are crowded, very oftenunequal in size' and angular due to mutual pressure. At times the zoospores behaveas gametes.

The naked protoplasmic bits referred to above sometimes do not develop ciliaand behave as aplanospores. These" arrested swarrners" are sometimes formed inlarge numbers and frequently for more than one generation resulting in palmelloidstages, which may ultimately assume the normal vegetative phase or are liberated asswarmers. In the allied genus Dictyococcusalso asexual reproduction takes place bybiciliate zoospores or .by aplanospores. In Trebouxia, the swarmers are formed as inChlorococcum,when it is free living, but when it is associated with a fungus to form a'lichen body only aplanospores are formed. Zoospore formation also takes place inPlanktosphacrJa (Starr, 1954 a; Herndon, 1958 a), which was formerly supposed toreproduce orily by autospores.

_ According to Starr (1955), there are three types .of zoospores in the spheri<;alChlorocoGcaceae: (a) the-Chlamydomonastype in which the zoospore p.as a cell wall and..two equal flagella, (b) the Protosiphontype in which the zoospore is naked, as indicatedby the rounding up of the body on becoming quiescent, and (c) the Bracieacoccustype

. in which the zoospore is naked and with two flagella of slightly unequal length, but ofthe whip type as in other Chlorophyceae.

Zoospore formation is also seen in a number of other families of the Chlorococcales.Thus, in Characiosiphon(Characiosiphonaceae) a large number 01 biciliate zoospores-are formed from each individual and they are liberated by the rupture of the -thallusat the apex (Iyengar, 1936,-1954). _

In Characium(Characiaceae), biciliate zoospores ~re fQrmed by the simultan~~JUsor successive division Qf the protoplast and they are Irberated through a- terminal orlateral aperture. Rarely, as in Characiumterrestrisand in Pseudochlorothecium,the arrestedswarmers develop into aplanospores. In the latter genus these spores are liberated

-+ terrestris KANTH.; k-I, p, q, FORMATION AND LIBERATION OF ZOOSPORES;r, EMPTY CELL AFTER LIBERATION OF ZOOSPORES,u-x, GERMINATION OF ZOOSPORE;m, n, Rhopalosolen. saccatus (FILARS.) FOTT; m, ZOOSPORE; n, LIBERATION OFZOOSPORES; 0, Tribollxia-- parmeliae CHODAT, FORMATION AND LIBERATIONOF ZOOSPORES; S, Kentrosphaera facciolae BORZI, LIBERATION OF SWARMERS;y, Charaeiosiphon rivularis IYENG., ZOO~PORE;z, DesmatraetumbiP;-ramidatum(CHOD.) _PASCHER,LIBERATIONOFSWARMERS(s, STIGMA).

(a-e, g, h, j, t, FROMSTA;R~ 1955 (e, AS Radiosphaera disseeta (KORSH.)STARR; f, FROMBOLD; i, AFTER GRINTZESCO, k-l and p-r, AFTER KANTAMMA,1940; u-x, FROM KANTHAMMA; m-n, AFTER FILARSZKY(AS Charaeium saccatumFIL.); 0, AFTERJAAG; $, AFTERBORZI; y, AFTERIYENGAR, 1954; z, AFTERPASCHER).

-+

18

a

,.

CHLOROCOCCALES ..,...,. ~0... .:. ~. .: "." :.!

. .(S. :.. .:.. :."~" .I."' , .:-. (!-,n-: '.'--:.Q.:'-&-

....FIG. VIII. ASEXUAL REPRODUCTION (BY ZOOSPORES, APLANOSPORES, AND

AUTOSPORES) IN THE CHARACIACEAE, TETRAEDRONOIDEAE, ANDLAGERHEIMIOIDEAE )

a-f, Ankyra ancora (G. M. SMITH) FOTT; a-b, PLANT SHO""ING H-SHAPEDCHLOROPLAST; c, ZOOSPORE FO~MATION; d, TRANSVERSE BREAK OF THE CELLWALL TO LIBERATE ZOOSPORES;. e-f, GERMLINGS; g-h, Bicuspidella rostrum-aquilaePASCHER; g, FORMATION OF ZOOSPORES; h, A ZOOSPORE; i-j and k, Pseudochloro-thecium mucigenum KORSH.; i, VEGETATIVE CELL; j-k, FORMATION OF NUMEROUSAPLA.."IOSPORES; I, Franceia elongata KORSH., SHOWING AUTOSPORES; m, Polyedriopsisspillulosa (SCHMIDLE) SCHMIDLE, SfJOWING REPRODUCTION BY ZOOSPORES; n-q,Hydrianum lageniforme KORSH.; n, VEGETATIVE CELL; 0, LIBERATION OP ONE ZOO-

~

REPRODUCTION 19

.n.1-"

within a mucilaginous vesicle. In the allied genus Ankyra Fott, the zoospores areliberated by a median transverse break of the parent cell wall. Hydrianum Rabenh.is an interesting genus in which only one of the two zoospores formed is liberated throughan apical pore, the other one being retained within the zoosporangium to give rise toa fresh zoosporocyst. Actidesmium reproduces by zoospores but these swarmersfonn colonies at the gelatinized apex of the parent cell as in Ankistrodesmusfalcatus var.stipitatus. Because of this Fritsch (1935) placed it under the Selenastraceae whereasmost other authors c.o.nsider it as a. colonial member of the Characiaceae. Printz(1927Y even suspected this alga to be a member of the Xanthophyceae. "

The number of zoospores formed is usually limited, but in the Characiosiphon-aceae, the Chlorochytriaceae and the Hydrodictyaceae (Subfam. Hydrodictyoideae)quite a large number of zoospores are formed. In Chlorochytriumlemnae 256 zoosporesmay be formed by the successive division of the protoplast. They are enclosed atfirst within a mucilaginous envelop~, but are liberated soon. When not liberated fromthe vesicle immediately, they may behave as gametes. In RhodochyJriumalso, theswarmers behave either as zoospores or gametes. In the colonial Hydrodictyaceaea large number of biciliat~zoospores (several thousands. in the case of Hydrodictyon)are formed by successive division and they ~re liberated into a .vesicle. where theyarrange themselves in an orderly way, withdraw their cilia and develop into a newcolony before liberation from the vesicle. In Euastropsisand probably Sorastrum morethan one such coenobia may be fonned in thiS-way from a parent cell. In the Tetra-

_edronoideae, which is being treated here as a sub-family of the Hydrodictyaceae,zoosp~r.e formation is known only in a. few species like Tetraedronhitridensand Poiyedriopsis-spinulosaand the number of zoospores formed -are also few'.

Acanthosphaera (Micractiniaceae), fonnerly thought to reproduce only byaplanospores, is also zoosporic, the zoospore being 'provided with four cilia and aprominent streak-like eye-spot (Fig. VI-o). Golenkiniareproduces both by zoospores andautospores. The zoospores are without cilia (hemizoospores) and eye-spots but possesscontractile vacuoles, four such. zoospores being formed from a cell (Fott, 1959). Therecord of quadriflagellate zoospores in Golenkinia by Chodat (1894a) has not beenaccepte~by most authors, but according to G: M. 'Smith (1933) the report of zoosporesin the closely related AcanthosPhaeraindicates. that Chodat's report is not incorrect.Incident~lly, ApodochlorisKoma~ek (Characiaceae) also reproduces both by zoosporesand hemizoospores.

Amongst the Treubariaceae, Desmatractumand Octogoniellaare known to reproduceby zoospores. In Desmatractum two to four zoospores, or more commonly two to fourautospores, are formed and are liberated by the transverse breaking of the cell wall.In Octogoniella, z:oospores, or less frequently aplanospores, may be formed: In theDictyosphaeriaceae, zoospore formation is reporte~ only in one species, viz.,DictyosPhaeriumtemstre Fritsch and John. -

Marthea (Scenedesmaceae) is an interesting alga in which the asexual reproduc-tory units do not have cilia, but show amoeboid movements. The parent cell gives

-+ SPORE AND RETENTION OP A SECOND ZOOSPORE; p-q, DEVELOPMENT OF THERETAINED ZOOSPORE INTO ANOTHER ZOOSPOROCYST.

(a-:-f, PR9M FO,." g-h. FROM PASCIIER, i-q FROM KORSHlKov)..

-+

20

l tb -@ ~Q 0 1J::.\~': ,

':

. . ... .'_.

. g' h

f

~~f,

."'"

@)"

i

" ' ,... ~i~~ ',; "fit

~.. ,' .".<, m n

~ .~w~~

CHLOROCOCCALES

d

FIG. IX. ASEXUAL REPRODUCTION BY ZOOSPORES IN THE CHARACIACEAE,CHLOROCHYTRIACEAE, HYDRODICTYACEAE, AND DICTYOSPHAERIACEAE

- a-b, Aclidesmium hookeriREINSCH, FORMATION AND LIBERATION OF DAUGHTER

INDIVIDUALS; c-e and i,H;.drodictyonreliculalum(L). LAGERHEIM; C, A.~D i,SMALLPARTS OF PROTOPLAST SHOWING FISSIONTO FORM ZOOSPORES; d, e,FORMATION OFNEW NETS (h, YOUNG NET; i,INNER LAYER OF WALL; 0, OUTER LAYER OF WALL);f-h, Dictyosphaerium lerreslreFRITSCH ET JOHN; f, FORMATION OF ZOOSPORES;g-h, ZOOSPORES; j-I,Fernandinellaalpina CHOD. VAR. semiglobosa FRIT~CH ET JOHN; j,FORMATION OF ZOOSPORES; k-I, ZOOSPORES; m-n, EuaslTOpsisrichteri(SCHMIDLE)LAGERH.; m, LIBERATION OF SWARMERS; n, FORMATION OF DAUGHTER COENOBIA; o-p,PediaslTumboryanum (TURP.) MENECH.; 0, FORMATION AND LIBERATION OF ZOOSPORES

(b, BLADDER OF MUCJLAGE); p, FORMATiON OF NEW PLATE..! q-t, Soraslrum sPinulosum '

REPRODUCTION 21

h

rise to four daughter cells, which after showing amoeboid movements for some time cometo rest and arrange themselves in the form of a colony before being liberated. Theamoeboid cells of i\1arthea and ,the zoospores of Desmatractum possess a stigma andoften contractile vacuoles. These algae are both interesting since they probably showthe phylogenetic relationship between zoosporic and autosporic forms of Chlorococ-cales (G. M. Smith, 1950). The occurrence of zoospores without cilia and stigmabut with contractile vacuoles in Golenkinia is also equally interesting from this point ofview since this genus also reproduces more commonly by autospores. "

Normally, the zoospores of the Chlorococcales are bi-, and occasionally four-ciliated. In Tetraciella, Pseudocharacium and Fernandinella (Characiaceae) and inChlorochytriumcohnii (Chlorochytriaceae) and AcanthosPhaerazachariasii (Micractiniaceae)the zoospores are quadriciliate. But in Fernandinella (still incompletely known andvariously placed by Chodat, Fritsch, Korshikov and Bourrelly in the Chaetophorales,Coelastraceae, Chlorosphaeraceae and Chlorococcaceae, respectively) autosporeor .autocolony formation also takes place. The zoospores also show vegetative divisioninto two to four after settling.

In contrast, the members of the Oocystaceae, Selenastraceae and the majorityof the Micractiniaceae, Treuuariaceae, and Tetraedronoideae do not reproduce byzoospores but only by non-motile spores called aplanosporc:s or autospores. Thus,in Chlorella, the protoplasLdivides into two, four, eight or 16 bits and each pit developsinto a new individual straightaway within the parent cell, no swarmers being formed:The new individuals are liberat~d by the breaking of the parent cell wall. Sometimes...as in. Trochiscia,Golenkitriaand Franceia (Figs. 22, e-h, X-e, VIII, 1) the daughter cellsbefore liberation even assume the characteristic ornamentation of the parent cell.In Tetraedron (except T. bitridens), reproduction takes place by the successive divisionof the cell contents, resulting in the formation of autospores which assume the shapesof the parent cell. In EremosPhaera,the autospores formed are quite large and few innumber. In Oocystis, they are usually liberated soon after formation, b!1t 'in somespecies, like O. panduriformis and O. lacustris, they remain enclosed within the parentmembrane for shorter or longer periods. In O. gloeocystiformi.$,several successive

generations may remain enclosed within the parent envelope. - -In the S<:lenastraceae,autospore formation is a regular feature, beipg liberated by the gelatinization of theparent cell-membrane or by its rupture. In Ankistrodesmusfalcatus vaI.:.-stipitatus; anattached form, the membrane of the parent cell opens' at one end and the daughtercells become fixed at this aperture in a radiating 'tuft and, when the process is repeated,characteristic dendroid colonies are formed. In Dendrocystis Iyengar (Oocystaceae)the two daughter cells formed within a parent cell by the longitudinal division ofthe protoplast and subsequent formation of individual cell walls are either liberated

-+NAEG.; q-r, DEVELOPMENT OF ZOOSPORES; s-t,YOUNG COENOBIA WITHIN VESJCLE;u-x, Schroederiaspiralis(PRINTZ) KORSH., X, YOUNG CELLS, V, CELL WITH PROTOPLAST

DIVIDING; W, ZOOSPORES, U, A DILATED CELL WJTH two PYRENOIDS; y, Kenlrosphaeraappendicula/a~ORSH., FORMATION OF ZOOSPORES.

(a-b, AFTER MILLER; c-e, AND i,AFTER KLEBS; d, AFTER HARPER; f-h,FROM

FRITSCH& JOHN 1942; m-n, AFTER LAGERHEIM; o-p, AFTER BRAUN; q-t,AFTERGEJTLER; u-y, AFTER KORSJUKOV, 1953).-+

22

~a

i31

n

CHLOROCOCCALES

~b

c

,~G~~

k

~-~'~~~. ..,'.., ~,

C. /~~,..,.n:."::: " -. ,m

~

FIG. X. AUTOSPORES, AUTOCOLONIES, RESTING SPORES OR HYPNOSPORES IN VARIOUSFAMILIES OF THE CHLOROCOCCALES

a, Charaeium teTrestris KANTH. WITH AUTOSPORES; b-c, Chlorella vulgarisBEIjERINCK, FORMATION AND LIBERATION OF AUTOSPORES; d, Chodatella ciliata(LAGERH.) LEMM., LIBERATION OF AUTOSPORES; c, Golenkinia .chlorelloides LUND,LmERATION OF AUTOSPORES; f-g, Tetraedron minimum (A. BR.) HANSG., FORMATIONANDLmERATION OF AUTOSPORES; h-j, Burkillia dissolvens SKUjA, FORMATION OF AUTOSPORES;k, Kirchneriella lunaris (KIRCHN':) MOEB., LmERATION OF AUTOSPORES INTO THE MUCIL-AGINOUS ENVELOPE; I, Coelastrum sPhaericum NAEG., FORMATION OF AUTOCOLONIES;m, SceMdesmus denticulatus LAGERH., LIBERATION OF AUTOCOLomES; n-q, RESTING

p

-+

t

REPRODUCTION

v\):.

~....... ,

. .. .. .. . ".

b . ." c

23

,Ia

"

e

~.:...t1'. .' h.: .:.:. ,: '.' . h

9::::.; \tk":~":

." . . ~. ....00. -" . . .." :,m . j

FIG. XI. ~EXUAL REPRODUCTION BY ZOOSPo"RES AND AUTOSPORES IN Tetraedronhitridens BECK-MANNEGETTA

a, OPTICAL SECTION OF YOUNG VEGETATIVE CELL SHOWING CHROMATO-

.PHORE AND PYRENOID; b, YOUNG CELL; C, OLD CELL; d-g, CELLS SHOWINGINCREASE IN NUCLEI; h, LIBERATION OF AUTOSPORES FROM MOTHER CELL;i, LmERATIONOFZOOSPOREs;j-k, ZOOSPORES; I-n, ZOOSPORES BECOME QUIESCENTAND YOUNG VEGETATIVE CELLS FORMED. NOTE THE EYE-SPOT IN I (FROMSTARR, 1954).

.1

I

as autospores or they move towards the ruptured opening of the parent cell wall andtbecome attached at the top. E\l-ch of these ..daughter cells, when fully de,::,eloped, '

repeat the same process, and, when the process is repeated by daughter ceUs of~everalgenerations a well developed dendroid colony is formed.

/

7"d

Q..,

':..."': n !J:l'j" ,

.:f '.':'1.. :.,'.I.

~(J)~

SPORES ITROCHISCIA STAGES) OF Chlorococcum humicolo (NAEG.) RABENH.; 0, Pedit:-strum duplex MEYE:-I WITH HYPNOSPORES (h); p, Phyllohium sphagnicola G. S. WEST,RESTING CELLS 0:-1 Sphagnum L!,AF; r, Cldorococcum hypnosporum STARR, GROUP OFHYPNOSPORES FOR~(ED FROM GROUP OF APLANOSPORES; S, Rhodochytrium spilanthidisLAGERH., RESTING SPORE; t-y, Oo~ystaellium elegans GONZ. et, MEHRA, SHOWINGAUTOSPORE FORMATION.

. -+

(a, AFTER KANTHAMMA, 1940; b-c, AFTER GRINTZESCO; d & k, AFTERCHODAT (d, AS Lagerheimia ciliata (LAGERH.) CHOD); e, REDRAWNFROM LUND,1954; f-g, AFTERG. M. S~"TH; h-j, AFTER SKUjA, 1949; I, 0, u & p, AFTER WEST;m, FROMWEST & FRITSCH, 1927; n-q, FROM FRITSCH & JOHN, 1942; r, FROMSTARR. 1955; S, AFTER LAGF.RHEIM; t-y, AFTER GONZALVES ~ MEHRA, 1959).