Table Of Content'
THE AUSTRALIAN ASC1DIACEA
PART 4, APLOUSOBRANCHFA (3% DIOEMNIDAE
PATRICIA KOTT
koti. P. 20D1 ON 15: I he Australian Ascidiacea pan 4. Apiousohranchia (3), Didemnidae.
Memoirsofthe QueenslandMuseum 47( ] ): 1-407. Brisbane. ISSN 0079-8835.
This fourth part ofa monograph of Ascidiaoea in Australian waters treats the Didemnidae
which contains some of the smallest and most simplified /.ooids, and most e&ten$!vc
coloniesand prolific replication rates known in theClass. The laniih ismore>>peeK>se than
others, largeh as a result ofdiversity in IndoAVesl Pacific (including northern Australian)
tropical waters where, despite a shorl nee-swimming larval lite, species have a wide
geographic range. In Australia, indigenous species generally are found in the more
temperatewatersofthesouthern halfofthecontinent.Noevidenceofpantropica! rangeoroi
Atlantic speciesofDidemnidae exists in the western Pacific oreastern Indian Ocean. The
affinities ofthe famiK with others in the Aplousobranchia are not clear, although a high
vanadium content in Lepfoclinides suggest an early origin from a Diazi>naA\ke artca
Intra-familiai relationships arc equally equivocal- Although there seems to be a trend to
reduced zooid si/e [rom Afn'ohwi and icptocdnides to Poiysvncraton, Dtdemnum and
Trididemnuni. similarities cou\d be the result of convergence rather than evident.
phyloeenetic ,ni i fr, ftjgpn. Liov., LfssoclUntmond QiplosomahavevquaU) equivocal
relationships with one another and with other genera. Ofthe 202 species described, 51
previous!} were known to occur in Australia, J$ were known onl\ rVoiti other parts ofthe
western Pacific and 1 16 are new. CoIoniaI Organisation, spicule si/e. form and distribution.
and larval and zooid morphology of newly and previously recorded material have been
scrutinised for tuv>nomie implications, tight genera, Ah-iolitm. Liplocii'nidc.s.
Pi'lysynerciton, Dtdemnum, Trididcmtnmu Lissoelinttm. Ciiteiht gen. nov. and Dipiosomfl.
aredocumented, (nbothtropicalandtemperatewatersDftfl mnumisthemostspectoscgenus
in the family. Biological data on breeding seasons arc indicated where possible. The new
species include a number Of previously unknown ProchfotvutDldetiwUm symbio.scs.
Crowdedectodermalcolumnarcells projectingfrompartsofthe wholeoftheoutersurfaceoi
adultzooidsandpigmentedsquamousepitheliumincertainspeciesinanumberofgeneraare
reported although phvlogeneTic implications were not detected. Scanning electron
micrographsofcak i-m' spiculesare presented asan identification aid tocomplement the
dichotomous keys to ta\n. Species descriptions arc complemented, where possible, with in
situphotographs- Anannotatedglossary isincluded, Thecharactersol speciesreportedfrom
adjacentareas!eg-thewestern IndianOcean,Indonesia. Malaysiaandother western Pacific
tropical locations to Fiji, as well as New Zealand), but npt >et from Au$tf Ji is waters, are
summarised and compared. O tnda-Weat Pacific Prochhron vymbio&G9\ trap
temperate, columnarepithelium, squamous epithelium,
PatriciaKott, QueenslandMuseum. POBox 33(H). SouthBi 'hath- -1 10i. Ausiralia;
6October2QQ0.
CONTENTS INTRODUCTION
INTRODUCTION . I Speciesofdn-single familyDidemnidae(Class
LISTOETAXA 2 Ascidiacea), one of 14 in the suborder
tAKCtkrxN.ObUWLLKttisDGLMhN l S 5o- Athpeloufislotreranefheiedai,ncgomcpormimsuenaitmiajeosricnomspuobnleiunotraolf
DIDEMNIDAEGiardJX72 6 ]to|lccairliao|nmSoistestpweoG-idalifmyensiniotnraolpigcraolwtwhatpeartsterwnhearned
ANNOTATED Gl OSS \RY S rapid rale ofreplication ensure that they occupy
TAXONOMY .19 muchoftheavailablesubstrate.Theirdi\crsit\ in
LITERATURE CITED. . WW'. S5D Australia far exceeds lhat ni other parts of'the
ScDPtIrCtfUiLEc AATT-rLAaSc («Frigs iI>«7-1r./*&i> #*<1•? wforrolmd«[hpcossxivbclsyterbnecapuascejfioci r.maddiatlihoanroflssopleacliieons
PLATES 3-79 around the southern parts ofthe continent where
INDEX 401 the majority of indigenous species occur. The
5 1 1 1 1 8 5 1
MEMOIRS OF THE QUEENSLAND MUSEUM
—
TABLE 1. ListofTaxa Theformal pagecitations fornewtaxaerected in thiswork are indicated inthis list,
although ataxonmay be informally referredto in precedingpages.
Atriolum Kott, 1983, 19 P. robustumsp.nov., 130 D.straguhimsp.nov.,238
A. bitcimimsp.nov.,21 P, rubitapumsp.nov., 131 D.sitcosumsp.nov.,240
A eversumsp.nov.,22 P. rugosumMonniot, 1993, 132 D. Tabu/atumSluiter. 1909,241
A. liiiumsp.nov.,24 P,scobirtumsp.nov., 134 D. ternerratumsp.nov.,242
A. marinensesp.nov.,25 P.scorteumsp.nov., 135 D. thecasp.nov.,243
AA.. rtoubbiupsotruummKastpt.,no1v9.8,3,2927 PP.stiadsemriasnesnp.senosvp..,n1ov3.6, 137 DD.. tuotunrgoaa(CH.er&dmFa.nM,on1n8i86o)t,,2149387,244
LeptoclinidesBjerkan, 1905,31 P. tegetumsp.nov., 137 D. vahatuioC.&F.Monniot, 1987,246
L. aciculussp.nov.,37 P. tenuicutissp.nov., 139 D. verdantumsp.nov.,247
L.albamacutatussp.nov.,38 DidemnumSavigny, 1816, 140 D. viasp.nov.,248
L. brandisp.nov.,40 D. a/bopunclatum.Sluiter, 1909, 148 D- viride(Herdman, 1906),249
L. caelestissp.nov.,42 £>.aranciumsp.nov., 150 D. vulgaresp.nov.,25
L cardialssp.nov.,43 £).astrumsp. nov., 151 TrididemnumDeliaValle, 1881,252
/_, cavernosassp.nov.,44 £). bicolorsp.nov., 152 T. amiculumsp.nov.,256
L. coeknteratus(Kott, 1962),46 D. bisectatumsp. nov., 154 T. areolatum(Herdman, 1906),259
L.comitassp.nov.,48 £>. caesiumSluiter, 1909, 155 T. caelatumsp.nov.,260
L.compactassp.nov.,49 D, candidumSavigny, 1816, 157 P. clinidesKoXi, 1977,261
L. conftrmatussp.nov.,50 £). chartaceumSluiter, 1909, 160 T. cristatumsp.nov.,262
L.constellatussp.nov.,51 D. clavumsp.nov., 162 7^ crystallinumsp.nov.,263
I. cuspidatus(Sluiter, 1909),52 D. complexumsp.nov., 164 T. cyclopsMichaelsen, 1921,264
L.ductus(Sluiter, 1909),54 D.crescentesp.nov., 166 tdiscrepansSluiter, 1909,267
I.duriissp. nov.,57 D, cucutliferumSluiter, 1909, 167 T.dispersum(Sluiter, 1909),267
L. echinussp.nov.,59 D. cygnuussp.nov., 169 T. lapidosumsp.nov.,270
L. erinaceussp.nov.,61 D.delectumsp.nov., 171 T. miniatumKott, 1977,271
L. exiguussp.nov.,62 £>. effusiumsp.nov., 173 T. nobilesp.nov,,272
L.fungifurmisKott, 1972b,63 £>. ehngatumSluiter, 1909. 173 T.nubi/umKott, 1980,274
L. imperfectus(Kott, 1962),65 D. eftWumKott, 1982a, 175 T.paraciinides Kott, 1982,276
I. kingiMichaelsen, 1930,67 D.flavoviri.deMonniot, 1995, 176 T.paracyclopsKott, 1980,276
Z,. levitatussp.nov.,69 D'fragileSluiter, 1909, 177 Tpigmentationsp.nov.,278
L fe.vw.vHastings, 1931,70 D.fragumsp. nov,, 179 T.pssudodiplosoma(Kott, 1962),278
L.longicollissp. nov.,70 D.'fucatumSluiter, 1909, 182 T. savignii(Herdman, 1886),281
L. macalatussp.nov.,72 D.fuscumSluiter, 1909, 184 T. sibogae(Hartmeyer, 1910),283
L. magnistellussp.nov.,73 D.gramfe(Herdman. 1886), 185 T.spumosumsp.nov.,286
L. multilobatusKott, 1954,74 D.granulatumTokioka, 1954. 188 T. tectumsp.nov.,288
L.placidussp, nov.,75 D.guttatumF.&C.Monniot, 1996, 189 T. tomarahiC.&F.Monniot, 1987,288
L. rigidussp.nov.,77 D. hcrba sp.nov., 190 T, vermiformesp.nov.,289
i. rufus(Sluiter, 1909),79 D. hiopaaC.&F.Monniot, 1987, 191 LissoclinumVerrill, 1871,291
L. semimidvssp.nov.,82 D. iticauum(Herdman, 1899), 191 L. badiumF.&C.Monniot. 1996,296
L. Sulawesi!F.&C.Monniot, 1996,83 D. inveteratumsp.nov., 193 I. bistratum(Sluiter, 1905a),298
L. umbrosussp.nov.,83 D.jedanenseSluiter, 1909, 194 L. caliginosumsp.nov.,300
L variegitussp.nov.,86 D.jucundumsp.nov., 197 L. calycisMonniot, 1992,301
L. volvusKott, 1975,87 D, lacertosurnMonniot, 1995, 199 L concavumsp.nov.,303
PoivsyncralonNott, 1892,89 D. levitassp.nov.,200 L. conchyliumsp.nov.,305
P. arafurensisTokioka, 1952,93 D. linatumsp.nov.,200 L. durabilesp.nov.,306
P. circutumKott, 1962,94 D. lissoclinumsp.nov..202 L- levitumsp.nov.,307
P. dentatumsp.nov.,96 D. macrosiphonicumsp.nov.,203 L. limosumsp.nov.,308
P discoidesKott, 1962,98 D. mantilesp.nov.,203 L, maculatumsp.nov.,31
P. dromidesp.nov.,99 D. membranaceumSluiter, 1909,205 L. multifidmn(Sluiter, 1909),311
P. echinatumsp.nov., 101 D. microthoracicumsp.nov.,207 L ttebuiosumF.&C.Monniot, 1996,31
P.flammeumsp.nov., 103 D. miniscu/uinsp.nov.,207 L- ostreariumMichaelsen, 1930,314
P,glaucumsp.nov., 104 D. mode(Herdman, 1886),208 L.pate/la(Goltschaldt, 1898),31
P infundibulumsp.nov., 106 D. monilesp.now,21 L.punctatumKott, 1977,31
P.///.?o\7/m(Herdman&Riddell, 1913), 106 D. moseleyi(Flerdman, 1886),21 L.reginumsp.nov.,319
P. /otfa'sp.nov., 108 D muliispiralesp.nov.,213 L.roseumsp.nov.,322
P. magnetaeHastings, 1931, 109 D. mutabileC.&F.Monniot, 1987,215 L.sentesp.nov.,323
PP.. mmielaknpdorraetuVamsCs.eu&r,F.19M6o8n,ni1o1t3, 1987, 11 DD.. oobslsiituummsspp..nnoovv..,,221165 LL., staproantgairuamC.sp&.nFo.v.M,on3n2i5ot, 1987,325
P, multiforme$y.nov., 114 D.paranciumsp.nov.,218 L. tasmanense(Kott, 1954),326
P. oceaniumsp.nov., 11 D.patuhim(Herdman, 1899),220 L. timorense(Sluiter, 1909),328
P. orbiculumKott, 1962, 117 O.pectensp.nov.,220 L- triangidum(Sluiter, 1909),330
P. etfuefaeC.&F.Monniot, 1987, 118 D.pel/ucidumsp.nov.,222 L. variabilesp.nov.,331
PP,.ppaalplyirou/sumsps.p.nonvo.v,.,12I018 DD..ppoeercpilleoxmuomrpshpa.Fn.ov&.,C.22M4onniot, 1996,226 CiCi.tenUuatrgiecnu.lanosvp..,no3v3.2,333
PPP...pppeosndetiuomdncoiiradueagtCou.smu&mspFM..onnMonovin.o,nti1,o2t11,99139,871,23122 DDA..pprrosbeaecmromtciaiMtnioucdmhease(pl.Slsuneiontv,e.r,,1291328089,5)2,30229 DiDDp..tflaeissrotrmeuargieaMumamicmdsop(.nMainllodvn.,e,-E138d35w79a,rd3s3,51841),339
P.pulchrumsp.nov., 125 D.scopisp.nov.,233 D. simile(Sluiter, 1909),341
P.pttrowC.&F.Monniot, 1987, 126 D. sordidumsp.nov.,234 D. translucidum(Flartmeyer, 1909),343
P. reguhtmsp.nov., 128 D. spadixsp.nov.,236 D. velatumsp.nov.,345
P. /7casp.nov., 130 D. spongioideSluiter, 1909,237 D. virens(Hartmeyer, 1909),347
;
THE AUSTRALIAN ASCIDIAd
present work is the first comprehensive study of TABLE 2 Measuresofspicule ra\ length.
ihe family m Australian waters, Of the 702
species now recorded 1 1—6 are new and onK 86
Were previously known 51 already recorded s
from Australia and 35 previously known only 3 oc i- E 1c
frTomheothoetrheparrtsApotlothueswoebsrtaenrnchPacfifaimci.lies are _ — _ -uh" —iEn S 3r5 >Hi
discussed in the Australian Asckiiaeea pans 2 <uph
ndenadljsiKwoiltth, tKh>e9(s)uab;olr^d2ear)sanPdhlpearbtohIr(aKnocuh\ia19a8n5d) rrCfseft.navin.fivi11mii tf-Leur - 1 1 . i
SiHntecaoltlueidddionighnrpnaaeinlweshisape.3cioeAfsdtdhaientdAiuosrnteracalolridaisnnfiAnoscrtumhleaiaItciaoexnaa JIK.ciinjiyni.itih>(!I[:t«r.SifyJi n E 3'i/,-7i -l int.si- ' 1 inJ - ! i14i
1
nre discussed in supplements (Kntt,
a1r9e90nbo;wl99k2nboJwnAbtoouotcc6u0r0 isnp»A?uisetsroalPiAasncuwIaitaecresa. scoinmtprlaicftiicoantioofntenanodbsccounrevsergsiegnncifei.canFturt/hoeoird,
Much material in all suborders, including the characters, the form ofcolonial systems often arc
Didemmdac remains to be examined. difficult to detemiine, colony shape and sizx: an
affccicd hy age, environmental factors and
All specimens referred to by a museum preservation and colours are variable and
legislationuumbei were examined in the course affected by oxidation and preservative. These
of this study, Where a sample of a colony Ot factors have been a major constraint to accurate
specimen lot is lodged in a second institution its species definitions and determinations, which
registration member is given m italics following bothdepend toa greatextent,on larval characters
the registration ofthe principal lot. and spicule si/e and form. As in all colonial
Museums holding ascidian material examined aseidians. larvae are viviparous, and inmost ta\a
during (his Mi'dv. with their abbreviations, -ire: have been found being brooded in one or mote
AM. Australian Museum, Sydney; AMXH, colonies. The month m which they occur has
American Museum of Natural History. New been tccorded.
York, U.S.A., BMNH, Natural History Museum,
London. UK; MV, Museum of Victoria, Spicules have inidilionallv be—en dellned by
Melbourne; NTM, Northern Teinlorv Museum their size (maximum diameter) the distance
Darwin; QM Queensland Museum, Brisbane; betweendiepointsofniyson opposite sidesB
SAM, South A3ustralian Museum, Adelaide; TM, sphere, and by the number of rays in optical
Tasmanian Museum, Ilobart; WAM, Western transversesection, bach specieshas spiculesof;i
Australian Museum, Perth; USNM, U.S. characteristic si/e range. Spicules M'maximum
National Museum oi' Natural History, diameteroeeui relatively frequently (mixed With
Smithsonian Institution, Washington DC. USA; othersol lesserdiameter)andarcreadilydetected
SM,SenckenbcrgMuseum, frankiurt.Germany (by light or scanning electron microscop> | [J1
ZMA, Zoological Museum of Amsterdam. preparationsofstripsoflestfromSffijq long. The
University of Amsterdam. The Netherlands; maximumm spicule diameter is used to dcllne
ZMC Zoological Museum, University of species die keys and descriptions that follow.
Copenhagen. Denmark; ZMH. Zoological The significance Of&Ver&g£ or mean values to.
Museum, University of Hamburg, Germany. spicule size is doubtful without an accurate
Photographic collections relating to thismaterial assessment ofstandard deviations, an indication
include the Australian Marine Photographic of(he full range ofsi/cs and some measure ofthe
Index (AMPi, Neville Coleman i, South variations in frequency of different sized
Australian Museum (with prefix PE, K. Gowlett spicules. Interpretation ofspicule form by light
Holmes and others); and the Queensland microscopy has been subjective and is not
Museum. always reliable. Scanning electron microscopy
has allowed more critical interpretationsofthese
Throughout this work a senior synonym is Vdimcnsional. opaquestructures. A moreor
preceded by "-'and ajunior synonym by >' pentagonal arrangement ofeach whorl ofspicIule
Zooids h«.VC relatively tew reliable rays has been demonstrated, making possible
Morphological characters owing to their small iciaiivciy p oi ratecountsofthenumbersofrays
size and overall uniformity - a result of in a so-called optical transverse section. Also
.
MEMOIRS OF THE QUEENSLAND MUSEUM
used in thepresent workto describe the spicules study that colonies in the intertidal rubble zone
and their rays is an assessment of the ray are not as large as some found subtidally, but
length/spicule diameter ratio (Table 2). In the there is no evidence that SCUBA diving is
spicule atlas (Figs 157-178) similar spicules are sampling a different fauna from that sampled by
grouped (rather than arranged in species shore collectingat lowtide. The large numberof
alphabetical order) forease ofcomparison. newspeciestakenfromNewCaledoniaandthose
Therehavebeen fewstudies ontheAscidiacea describedherein apparentlyreflectourignorance
inAustralianwatersand. probablybecauseofthe ofthedidemnidfauna. Itisnotevidenceofeither
problems set out above, even fewer on the isolation, or habitat specialisation. Most ofthe
Didemnidae. Previous attempts to study the tropical species in this family are now known to
family often were unsuccessful because have awide geographic range.
charactersforspeciesdeterminationhadnotbeen These studies have established some
identified, and in many cases similarities in the appreciation of the intraspecific variation that
small simplified, convergent and often can be expected to occur amongst populations
contractedzooids distractedattentionfromother over wide geographic ranges in the Indo-West
characters,frustratedattemptstoseparatespecies Pacific. Proposals ofpantropical species ranges
from one another and resulted in many wrong resultingfromtransportonship'shulls(Rocha&
assignations. Revision of much of the Pacific Monniot, 1993) or any other cause are
material in the Zoologische Museum speculative and the conspecificities on which
(Amsterdam) and the US National Museum these proposals are based are not confirmed by
(WashingtonD.C.)hasshownthatSluiter(1909), the present study.
VanName(1918)andTokioka(1967)hadsimilar In temperate waters the didemnids of the
problems in defining species parameters.
Challenger expedition (Herdman, 1886),
Nevertheless, these works and the associated
providethebasis forstudyofthefamily. Reports
well conserved collections arethebasis formore
on small collections from south-western
recent studies on the didemnid fauna of the Australia (Michaelsen, 1930), New South Wales
tropical western Pacific. Few other authors had (Herdman, 1899; Kott, 1972c), southern
reported on any significant collections of
Australia (Kott, 1972a-b, 1975, 1976) and other
didemnidsinthetropicalwesternPacificuntilthe
general collections (Kott, 1962) did not
past decade. The exceptions areEldredge (1967) appreciably advance understanding of
ontheDidemnidaeofthecentral Pacific;Tokioka
Didemnidae in these waters owing to the same
(1950, 1952, 1955, 1961, 1967, 1970)and Millar
(1975) on collections containing some lack of understanding of the group that beset
studies in otherparts oftheworld.
Didemnidae from the central to western Pacific;
and Kott (1977, 1980, 1981, 1982a) on Few species of the Didemnidae have a
didemnids in symbiotic relationships with continuous range from tropical into temperate
prokaryotic chlorophyll-containing algae which, waters, sucharangeoccuringmoreofteninother
associatedwithanemergingworld interestinthis families of Ascidiacea (see Kott, 1985, 1990a,
symbiosis, were the first systematic works on 1992). As with other taxa, more indigenous
large collections of exclusively didemnid species occur in temperate than tropical waters,
ascidians from the tropical western Pacific. The although Didemnidae are more diverse in
species list of Didemnidae in this part of the tropical waters (Kott, 1982c), reducing diversity
world has increased as a result ofwork in New toward the poles. Two tropical species known
Caledonia (Monniot, 1989, 1991, 1992, 1993, from Australian waters may possibly occur in
1994, 1995), French Polynesia (Monniot & New Zealand, viz. Polysyncraton fuscum {IP
Monniot, 1987) and other locations (Monniot & meandratitm) and P. paradoxum (IP robitstum).
Monniot, 1996; Nishikawa, 1984, 1994). However, although possible Gondwana ascidian
8 sMpoencniiesotof(1P9o9l3y)sywnacsrasturopnrirseecdorthdaetdnfornoemoNfethwe NreeliwctsZehaalvaendbeteenmpreercaotredeldocfartoiomnsA,ustthrearleiaanreannod
Caledonia were known from other locations in records ofdidemnidspecies in this category (see
the SW Pacific. She suggests this is because the Didemnumfragum)
collections were made by SCUBA rather than Kott (1998) documented 59 valid species
dredge or shore collecting (although this would previously recorded from Australia. Didemnum
surely have affected other genera as well as incanum, removedfromsynonymyandvalidated
Polysyncraton). It has been found in the present in the presentwork, shouldbe addedtothetotal.
THE AUSTRALIAN ASC1DIACEA 4
Of these 60 species, D. rottnesti Kott, 1962, coast, theArafura Sea and theGreat BarrierReef
Pofysyncraton victoriemis Kott, 1976 and D. (McCauleyetal., 1993).
fthiemibrrsitaattuums iHseurndcemratna,in.18A99furatwhaeirt6rsepveicsiieosn saanidd maIdaemitgproastseifbulletoforthmeephtootoagpprraepchiear—tsewthheolihvaivneg
to occur here result from misidentification, viz appearance ofmany ofthe species especially
Didemnum augusti: Kott, 1962, D. lambitunr. Neville Coleman (Australian Marine
Kott, 1962; Pofysyncraton mortenseni: Kott, Photographic Index), Karen Gowlett Holmes
1954; Trididenmum cerebr(forme: Kott, 1962 (South Australian Museum), Roger Steene
and T. spiculatum Kott, 1962. (Cairns), Ron and Valerie Taylor (Sydney),
Myriam Preker (Heron I. Research Station) and
ACKNOWLEDGEMENTS members ofthe AIMS Bioactivity Group.
During this study, I have had the support of woIrkacokfnmoywlseudccgeesswiivtehrepsaeratricchulaasrsigsrtaatnitstubdoeththien
colleagues both in Australia and overseas. In
the laboratorv and in the field, John Kennedy
particular, I thank the successive Directors and (1991-3), Susan List (1994-6) and Daniel
Boards of the Queensland Museum for their Schmidt 998-2000).JohnKennedydrewmany
continued support. I also thank Curators and of the bl(a1ck and white figures ofLeptoclinides
Collection Managers in Australian and overseas
museums fortheirvery prompt r—esponses to my maincdrAotgrriaopihusmaonfdtpheriorduscpeicdutlhese.scSaunsnainngLeilsetctarnodn
requests for loan of specimens in Australia Daniel Schmidtdrewtheremainderofthefigures
Penny Berents (Australian Museum), Sue Boyd
and prepared and scanned spicules ofmore than
(Museum ofVictoria), Loisette Marsh and Jane
1000 specimens of Didemnum, Pofysyncraton,
Fromont (Western Australian Museum) and
Trididenmum and Lissoclinum. As well as
Wolfgang Zeidler, Karen Gowlett Holmes and drawing many ofthe figures, Daniel has revised
ThierryLaperousaz(SouthAustralianMuseum);
andupdatedmostoftheothersandhascomposed
and from overseas Joke Bleeker (Zoological
the paste ups and scanned these and the colour
Museum, Amsterdam), Sheila Halsey (the
Natural History Museum, London), Hilke plates. In executing these responsibilities he has
demonstratedan appreciationofthe Didemnidae
Ruhberg (the Zoological Museum, Hamburg)
and Linda Cole (the US National Museum of that has significantly advanced this work.
Natural History, Washington D.C). Also, since 1980, able and enthusiastic
assistance in the field has been provided, at
I have been fortunate in the richness of the various times, by Andrew Rozenfelds, Lucille
collections available to me and the Crevola-Gillespie, Stephen Cook, David Parry
comprehensive sampling ofthe Australian coast and Myriam Preker. Georgia Pass generously
tbhyeySCreUprBeAsendti.viMngu,cyhieolfdtihnigsmcaotlulreec,tiungndhaasmabgeeedn hfieglupreeds.wiJtehnntihfeeirnitMiaalhopnasetye,upsAuodfrmaanTyoppoifntgh,e
colonies. The Western Australian Museum Lynette Dickfos, Katie Laws and Jennifer
(especially Shirley Slacksmith and Loisette Cannonsuccessivelyupdatedthemanuscriptasit
MSaCrUsBhA),toforkommaaltlertihael,websyterdnreAdugsetraalsiawnelcloasast tdheveemlofporedthtehirrocuog-hopietrsatmiaonn,yddirlaiftgse,ncaenadnIdtghoaondk
including the North West Shelf. Jan Watson has humour. I also thank Mr U. Tinggi of the
extensively sampled the Victorian coast. The Scientific Service in the Queensland Health
South Australian Museum (especially Wolfgang Department, for his analysis of a sample of
Zeidler, Karen Gowlett Holmes, Hugh
Atrioium rohustum for vanadium.
Bavenden) and South Australian Fisheries
Department (Scoresby Shepherd and his team) I am grateful to my colleague, Dr Lester
have sampled the GulfSt Vincent, Spencer Gulf Cannon, for sharing his wide knowledge of
and the Great Australian Bight. Karen Gowlett taxonomy and invertebrate structure and
Holmes photographed samples from across the function with me overthe past 20 years.
southern coast from Tasmania to Albany and Since 1980, grants from various agencies have
from the Northern Territory. I have also had supported the field and laboratory programme as
available the collection (now in the Queensland collections were made and examined, data
Museum) made by the Australian Institute of compiled and manuscripts prepared for this
Marine Science (AIMS) Bioactivity Group from Monograph. The agencies are the Australian
allaroundthecontinent, includingtheKimberley Biological Resources Study 1980-2; Marine
MEMOIRS OF THE QUEENSLAND MUSEUM
Sciences and Technology Grants Scheme dissection and manipulation, although they are
1984-86 and the Australian Research Council not always easy to remove from the colony and
1991-3, 1994-6 and 1998-2000. are best observed in situ. In other genera the
structure of small zooids can be adequately
PROCEDURES examined only in stained and cleared permanent
Formalin fixed, and preferably narcotised mounts ofeither the isolated zooids orthe hand-
specimensareessential toadequatelydissect and cut, thin, decalcified sections of the colony.
observe the morphology of specimens of the Larvae also are stained and mounted for light
Ascidiacea. This is particularly true for microscopy.
Didemnidae, whichhaveespeciallysmall zooids Spicules areprepared forSEM by incinerating
in complex systems. Long term preservation a small fragment oftest (to remove all organic
specimens should be transferred to 70% ethanol material)onthetipoffineforceps. They arethen
afterat least 2-3 months in fixative. In all genera putintoadropofabsolutealcoholonthetopofan
ofthis family, following observations on surface adhesive surface on the stub. The spicules
structures, a thin vertical inspection slice or separate from one another in the alcohol and
wedge, through the whole depth of the colony senle fairlyevenlybeforethealcohol evaporates,
from a common cloacal aperture to the outer leaving a suitably clean surface for coating. In
margin, will display the general form of the order to avoid 'drowning' the spicules, it is
cloacal systems, the position ofthe zooids, and essential thatthe—adhesive useddoesnotdissolve
the distribution of bladder cells, spicules and in the alcohol in the present study Avery
otherinclusionsinthetest. Theinspectionsliceis 'Spot-O-Glue' tabs were used.
—always cut parallel to the long axis ofthe zooids In addition to the general subjective accounts
i.e. generally at right angles to the upper ofcolour,many livingspecimenswerecompared
surfaceandthickenoughtoinclude wholezooids (in the field) with colour charts (Ridgway 1866)
but thin enough for light microscopy. Efforts to give a more precise and objective account of
should be made not to excessively mutilate the colour and these are indicated in the text by a
ccoolloonnyy.sNheoiutlhderevdeirdbeemcnuitdhonroirzoanntyaloltyhe(rpaarsaclliedliatno superscript R (e.g., rose red R)
the surface), for this divides the zooids and Permanent slide mounts of most zooids and
obscurestheconfigurationofthecloacalcavities. larvae for light microscopy, as well as
photomicrographs and scanning electron
Zooids and embryos can be observed in situ in microscopy stubs of spicules are in the
these inspection slices, or they can be removed Queensland Museum collection.
formanipulationanddissection. Careneedstobe
taken to avoid tearing off branchial or atrial Analysisforvanadiumcontentofafreezedried
siphons when removing zooids. It usually is not sample of Atriolum robustum was by nitric
possibleto removedidemnid zooids entire. They peroxide wet digestion followed by
invariably break across the oesophageal neck. determination with ICP-AES.
Zooids can be dissected with sharpened needles
or forceps in a drop ofglycerol on a glass slide. Family DIDEMNIDAE Giard, 1872
Sometimes a drop of stain added either to the The family isrelativelyuniform althoughvery
colony itselfor to the slice ofit, or to the zooids speciose. It is characterised by its small zooids
and embryos (after their removal) will help to divided into thorax and abdomen, the former
display their structure. Often zooids are held so consistingofalargepharynxperforatedby 3 or4
tightlyinthetestthattheycannotberemovedand rows of stigmata. Gonads, in the abdomen
itisnecessarytodecalcifythehand-cutsectionof respectively dorsal or posterior to the short,
colony in order to observe the zooid structure. vertical orventrally flexed gut loop, consist ofa
Hand-cut thin sections of colony can be small ovarywithonlyoneeggmaturingatatime,
decalcified by dropping into an excavated block and dome-shaped to spherical or oval testis,
or watch glass with sufficient 3% HCI to cover entire orsubdivided, withthe vas deferens either
the section. Generally decalcification will be straight, or coiled around the testis. The zooids
completed in 1-3 hours, although often it is are arranged in usually extensive cloacal
necessary to renew the acid owing to the systems. With the exception ofDiplosoma and a
buffering effect ofthe calcareous spicules. few species in each of the other genera except
Leptoclinides and Atriolum have large zooids Lepioclinides and Atriolum, the test contains
in which organs can be readily observed by minute (seldom more than 0.1mm diameter and
THE AUSTRALIAN ASCIDIACEA 4
often lessthan halfthatsize), stellate,globularor retains the Leptoelinides-\ike atrial siphon) to
burr-like, calcium carbonate (aragonite) spicules Didemnum. Polysyncraton zooids are not so
synthesised in pairedlateral organsintheparietal small, and they have Leptoclinides-like
thoracicwall. Bodywall musculatureisconfined multiplicity of male follicles, relatively num-
to the thorax, and never occurs inthe abdominal erous stigmata and a coiled vas deferens.
wall. Usually (except in Atriolum and Lepto- Condition of the testes and ofthe vas deferens
clinides and a few species in other genera) a may be indicative ofgeneric relationships, viz. a
retractormuscleprojectsoutintothetestfromthe coiled vas deferens is present in Leptoclinides
ventral surface of the oesophageal neck of the and Polysyncraton (with many 6 follicles), and
zooidand2 or3 vascularprojections,each witha Atriolum, Trididemnum and Didemnum (each
terminal expansion(ampulla)extend intothetest with an undivided testis). The straight vas
fromtheventralsideofthepoleofthegutloop. deferensofLissoclinum^ Clitella andDiplosoma
The Didemnidae have long been regarded as may indicate another group of related species.
the most highly evolved of aplousobraneh The retractor muscle (probably associated with
ascidians.Certainlycolonyorganisation,andzooid reduction in length of the thorax and loss of
size-reduction and simplification, arc more muscles from the abdomen) in 6 ofthe 8 genera
apodsvsainbcleedalsiontthhaitsinftaemgiraltyiotnhoafnthiencootlhoenrys.isIwtelils n(aelclesesxacreipltyAitnrdiicoaltuemaacndomLempotoncloirniigdines.) does not
advanced, a nerve complex havingbeen demon- Romanov (1989) proposed that a straight vas
strated (Mackie & Singla, 1987)rMevertheless, deferens and absence of spicules are primitive
these developments ofcolony and zooid do not features and therefore Diplosoma and related
imply direct linear evolution through the Lissoclinum are primitive. However, there is no
Aplousobranchia. Compelling evidence of an evidence to support a primitive status for these
early origin for the Didemnidae exists in the characters. Diplosoma (the only genus
presence,inLeptoclinides,ofverylargeamounts consistentlylackingspicules)hascomplex larvae
ofvanadium generally found in more primitive with precocious blastozooids forming in the
ascidians such as Ciona (Hawkins et al., 1983). trunk and contains species with prolific repli-
Unless the Didemnidae is polyphyletic, which cation in which primary, secondary and even
seems unlikely, these high concentrations of tertiary buds form before separation from one
vanadium suggest thatLeptoclinides is the more another. Although in Cionidae and Diazonidae
primitive genus, and that the evolution ofother regeneration of the thorax on a conserved
genera has been associated with loss of atrial abdomen probably is an early stage in the
siphons, reduction in zooid size and loss of evolution ofreplication in the Aplousobranchia
vanadium. The related genusAtriolumhas larger (Kott, 1990a), a similar process observed in
zooids than Leptoclinides and, like a fe—w7 Diplosoma by Romanov (1989) is more likely
Leptoclinides spp., has a functional oviduct convergent than primitive.
the ovum passing from the abdomen through the
oviduct to a thoracic brood pouch where it is Larfargue(1983)proposedthe linearevolution
incubated.Thus, somecharactersofAtriolumare of didemnid genera from Cystodytes (Poly-
more primitive than in other Didemnidae. citoridae),throughLissoclinumtoPolysyncraton
However, Atriolum has an undivided testis (like and Didemnum to Trididemnum, while
Didemnum). Further,althoughAtriolumhasbeen Diplosomaisderived fromLissoclinumbylossof
found to contain vanadium it is in lower spicules. Larfargue (1983) has not included
concentrations (350ppm in A. rohustum) than in Leptoclinides in her considerations, being
Leptoclinides spp. (Hawkins et al., 1983: primarily concerned with Didemnidae from the
8,000-10,000ppm) which may indicate a French coast. The present study suggests that a
Leptoclinides ancestor linear relationship ofthe genera is unlikely, and
thatderivationofthefamily(withtheDiazonidae
There are few morphological clues to or Holozoidae) from some common ancestor is
phylogeny in the Didemnidae largely because of more likely than from the Polycitoridae (see
size reduction and simplification which have
discussion onAtriolum, below).
resulted in a preponderance of convergent
characters of doubtful relevance to phylogeny. Didemnid genera are distinguished from one
There is an apparently significant progressive another by the presence or absence ofspicules,
reduction in zooid size from Atriolum to condition ofthe testis (undivided or bisected, or
Leptoclinides to Trididemnum (which often divided into more than 2 follicles), course (and
MEMOIRS OF THE QUEENSLAND MUSEUM
—
length) of the vas deferens (hooked proximally branchial apertures, siphons: Branchial
but otherwise straight, vertical, and relatively apertures always are on cylindrical siphons
short; or a longer duct, its length taken up in its which sometimes, especially in Didemnum, are
spiral course around the testis), presence or particularly long. The siphons are relatively
absence of a retractor muscle, presence or uniform, with 6, usually pointed projections or
absence ofan atrial siphon, and number ofrows lobesaroundtherim oftheapertures, althoughin
of stigmata (3 or 4). Species are distinguished some Leptoclinides the pointed lobes around the
from one another by zooid size (generally aperture are not developed. The test always
directly related to the number of stigmata per projects to line the siphons, very often, with
row), presenceorabsenceofananterioratrial lip spiculeswhich eitherform apluginthesiphonor
(or tongue), orientation and general proportions appear (from the surface) to line the margin ofa
ofthe gut, numbers ofcoils ofthe vas deferens, stellate opening. The shape of the openings
size, shape anddistribution ofthe spicules, form appears to be determined by a stellate cross
ofthe colony and common cloaca! systems and section of the lumen of the siphon, possibly
size and form oflarvae. Position, shape and size caused by longitudinal muscles inserted into the
ofthe lateral organ are affected by contraction of branchial lobes.
the thorax and are generally significant
branchial sac: see stigmata.
characters for species determination only within
colony shape: Convergence in the form of
limits.
colonies is conspicuous, most genera containing
ANNOTATED GLOSSARY representatives ofthe full range ofshapes from
small one-system cushions with a central
The followingentries relate specifically tothe common cloacal aperture to more extensive
Didemnidae.They shouldbeusedinconjunction single or multi-system colonies. The thin
with glossaries on aspects ofall families ofthe sheet-like irregular colonies, containing
Ascidiacea (Kolt, 1985, 1990a, 1992a). randomly distributed common cloacal apertures
—
atrial apertures, siphons: Atrial apertures are probably the most commonly encountered
are on long muscular siphons in Leptoclinides, colony form in most genera exceptAtriolum and
Atriohim and usually in Trididemmtm. In other Leptoclimdes which tend to form more 3-
genera(excepting Didemnumfucatumwhichhas dimensional shapes with terminal common
a small circular sessile opening) the atrial cloacal apertures on elevated parts of lobed or
aperture is a large sessile opening that exposes a irregular fleshy masses. Some species in most
large part ofthe perforatedbranchial sac directly genera except the soft Diplosotna and
to the cloacal cavity. In certain Didemmtm, Lissoclinum have finite and characteristic
occasionally in Lissoclinum and commonly in shapes, e.g. flask-shaped, spherical, stalked or
Polysyncraton, an anterior tongue (sometimes small oval orcircularcushions. Uprightcolonies
called a lip) projects from the anteriorrim ofthe or projecting lobes sometimes are supported by
opening. It is muscular, and in many species in the basal test expanded up into a pillar or solid
which itoccurs its lengthisrelatedtotheposition centralmass, partially separatedfromthesurface
of the zooid relative to the common cloacal zooid-bearing layeroftestby acloacal cavity; or
aperture.Thetipoftheatrialtongue(especiallyin water pressure in a large central cloacal cavity
Polysyncraton)oftenisbifidandsometimeshasa maintainsthe shapeofthe colony. Somemassive
fringe ofsmall papillae along its edge. It can be 3-dimensional colonies in Leptoclinides,
inserted into the test over the common cloacal Didemnum andoften Trididemmtm arebranched
cavity or it may be expanded and increase in or fold over and the surfaces coalesce to form
length to extend throughthe roofofthe common 3-dimensional reticularorsponge-like structures
cloacal cavity intothe rimofthecommoncloacal with external surfaces and spaces as well as
aperture. The zooid then has some capacity to extensivecommoncloacal spacesenclosedinthe
control water pressure in the colony and in the colony (Leptoclinides echinus, Didemnum
pharynx either by closing the common cloacal clavum, D. cotnplexitm, D. ossium, D.
aperture or by pulling the roof ofthe common lissoclinum. D. psammatode, D, spongioide,
cloacal cavity down over the common cloacal Trididemmtm crystallimmu T. lapidosum, T.
canals and overthe atrial apertures. nobile, T. sibogae and T. vermiforme). Many
— species (e.g. Lissoclinum histratum, Didemnum
atrial lip, tongue: see atrial aperture. mode, Diplosotna virens) lobulate and the
blastozooids: see larvae, replication. replicatesmoveapart,spacingthemselvesevenly
THE AUSTRALIAN ASCIDIACEA 4
tnF^
over the substrate (Ryland, 1990). Extensively a
branched tree-like structures (e.g. Didemnum
ossium,D. Hssoclinum, Trididemnumlapidositm)
often have ahard core ofpacked spicules which
servesasasupportingframethroughthecentreof
each branch (see also cloacal systems; common
cloacalapertures;colonysurface;substrates).
colony surface: The colony surface is either
smooth or (less often) has surface ridges (see
Didemnum spongioide) or papillae. Some
species have small spicule-filled papillae on the
whole orpartofthe surface which make itrough
or raspy. A few species in Didemnum (e.g. D.
cucuUiferum) and occasionally Polysyncratari
(P. echinatum) have a hollow spiky papilla
associated with each branchial aperture which
accommodates an enlarged ventral lobe of the
branchial aperture. These papillae appear to
protect the branchial apertures (Didemnum
cucuUiferum). The surface may also be raspy if
spicules are crowded and/or large in the
superficial layer of test, although they are not
always presentthere, the superficial layer oftest
beingcrowdedwithsphericalbladdercells(often
mixed with pigment cells) which can create a
particularly smooth surface. Many colonies,
especially when preserved, have the surface
marked by a mosaic ofcircular to oblong areas
separated from one another by narrow
depressions. These depressions, usually lined on
each side by zooid openings, are formed by the
collapse ofthethin layeroftestformingtheroof
of the primary common cloacal canals that
surroundsolidstandsoftestorclumpsofzooids.
colour: Colours derive from pigment cells inthe
test, bloodcells (which often diffuse intothetest
and symbionts in the test) or in the common
cloacal cavity. All colour appears to change,
probably as a result of oxidation following
collection and fixation, and generally is an
A
unreliable cha—racter for identification.— black
pigmentspot endostylarpigmentcap onthe
anteriorendoftheendostyleoccursinthecyclops
group ofTrididemnum species and others in.the
same genus. Similar spots are in the mid-dorsal
line near the neural ganglion in Diplosoma spp. FIG. 1. Common cloacal systems (diagrammatic). A,
(see also squamous epithelium.) horizontalthoraciccavity;B,thoracicprimarycanals
common cloacal apertures: Common cloacal lined with zooids; C, deep primary canals and
secondarythoracicandposteriorabdominalcavities;
aperturesusuallyareraisedabovethesurfaceofa
D, sheet or cushion-like colonies with sessile
colony where the excurrent water flow is commoncloacalaperturesandatrialsiphonsopening
entrained by passing currents, thus keeping it into posterior abdominal cavities (cf Leptoclinides.
separated from the smaller incurrent streams Trididemumspp.);E,conesorlobeswithcentraltest
enteringeachbranchialaperture(seeKott, 1989). core and terminal common cloacal apertures. F,
Elevatedcommoncloacal apertures are eitheron clumps of zooids in terminal branches of test
chimney like projections ofthe test, or they are connectives (cf. Diphsoma spp.).
MEMOIRS OF THE QUEENSLAND MUSEUM
—
terminal on elevated parts ofthe colony on the embryo remains in an abdominal pouch
upright colonies oronvertical lobes orswellings attachedtotheabdomenofthezooid(Diplosoma
caused by structural thickenings ofthe basal test ferrugeum).
to form an axial core oftest which support the gene flow: Although some apparently
upright colony or elevations or colony lobes. indigenous species have restricted ranges, many
Elevations also are created by pressure of the speciesoftheDidemnidaeintropical aswellasin
excurrentwaterwhichinflatethesurfaceoverthe temperate and polar waters, have a wide
large common cloacal chambers (beneath the geographic range despite being internally
cloacal apertures). In some colonies, however, fertilised and brooding their larvae. In those
sessile common cloacal apertures are not species with known life histories, the free-
conspicuously elevated and there is no obvious swimminglarval life is lessthan20mins (Olson,
separation of incurrent and excurrent water 1983) and occasionally larvae appear to begin
currents except the differences in their relative their metamorphosis before liberation from the
strength(Kott, 1989; Polysyncratonechinatum). parent colony ( L. ditrus). In such cases, larval
common cloacal cavities: Common cloacal dispersal overgreatdistancesseemsunlikelyand
canals or horizontal spaces are either shallow, at gene flow probably occurs through chains of
thoracic and/or oesophageal level; or they are recruitment between adjacent locations.
deeper, extending the length of, and sometimes Nevertheless, larval free-swimming life may be
into posterior abdominal cavities behind, the extended when stimuli to settle are not available
zooids. The small zooids are embedded in test —(e.g. open sea without shadowe—d undersurfaces
aroundorabovecloacal canals andspaces; orthe Berrill, 1955, or night-time Olson, 1983),
cloacal spaces penetratethetestsurrounding the —providing opportunities foralternative strategies
the zooids or penetrate into clumps of zooids one for gene flow, and one for population
separating them from one another so that maintenance (Kott, 1980, 1985). Another
(depending on the depth of the cloacal cavity) possibleagentforgeneflowbetweenpopulations
somepartorthewhole oftheirthorax, supported of widespread species, separated from one
by a narrow ventral strip oftest, is completely anotherby vast expanses ofdeep ocean (such as
surrounded by cloacal space, the thoraces Fiji and other parts ofthe western Pacific, and
stretching between the surface and a thicker Hawaii),maybetransportbydriftwood,theslow
basal layer of test in which abdomina are recruitmentrate likelytobeassociatedwith such
embedded. Especially in Lissoclinum and transport possibly being accommodated by
Diplosoma, whole zooids or clumps of zooids longevity ofthe colonies (Jackson, 1986).
stretch between the surface and basal layers of geographic range: see gene flow.
testwiththeabdominaembeddedseparatelyorin gut, gut loop: The vertical oesophageal tube,
clumps in the test strand (Fig. 1). smooth and almost spherical stomach, and thick
dispersal: see gene flow. cylindrical duodenum (often expanded distally)
ectodermal ampullae: see larvae. form the descending limb of the gut loop. A
endostylarpigment cap: see colour. posterior stomach is in the pole ofthe loop, and
the rectum forms the ascending loop. Usually
epidermis: see projecting columnar cells, thesedivisionsareseparatedfromoneanotherby
squamous epithelium. constrictions, and there are no short lengths of
fertilisation: Fertilisation is internal, the egg mid-intestine between them as in other
generally is fertilised in the abdomen of the aplousobranchs(Kott, 1990a,b).Theoesophagus
zooids,throughthevestigial oviduct(Burighel et andstomacharealwaystotherightoftherectum.
ah, 1986; Martinucci et al., 1988, Ryland & The posterior stomach is more or less oval in
Bishop, 1990, 1993; Bishop & Ryland, 1991; most genera, although in Polysyncraton it is a
Burighel Sc Martinucii, 1994a,b). The embryo roomy organ which expands tojoin the rectum.
passes intothetest directlyfrom the abdomen, is The rectum may form an elbow where the
incubated in the test, and liberated as a posterior stomachjoins it. The proximal part of
free-swimming larva eitherthroughthe common therectumiswideandinmostgeneraisseparated
cloacalcavity,ordirectlythroughthesurfacetest. from a narrower upper distal part by a short
Only in Atriolum Kott, 1983 and some lengthofnarrowgutsurroundedbytubulesofthe
Leptoclinides (e.g. L. brandi) does the ovum gastro-intestinal gland. In Polysyncraton the
move up the oviduct into athoracic pouch where distal part ofthe rectum is a particularly narrow
it is fertilised and incubated. Verv occasionallv cylindricaltube. Separationoftheproximal from
