Table Of ContentPROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES
Volume52, No. 17,pp. 209-225, 10figs., 1 table. SEP J 200J August21,2001
First Record of a Bioluminescent Soft Coral: Description of a
Disjunct Population ofEleutherobia gmyi (Thomson and Dean,
1921) from the Solomon Islands, with a Review of
Bioluminescence in the Octocorallia
by
GaryC.Williams
DepartmentofInvertebrateZoologyandGeology, CaliforniaAcademyofSciences
Golden GatePark, San Francisco, California 94118
ApopulationofalcyoniidsoftcoralsassignabletothespeciesEleutherobiagrayi(Thomson
andDean, 1931)isdescribedfromtheSolomon Islandsinthesouthwestern PacificOcean,
ataxonpreviouslyknownonlyfromtheIndonesianandRyukyuanArchipelagos.Thespe-
cies isremarkable in thatthe anthocodiaeare strikingly bioluminescent. This represents
thefirstrecordofabioluminescentsoftcoral,otherthanadubiousrecordforAlcyonium.
Other octocorals for which bioluminescence has been verified are restricted to the
gorgonianfamilyIsididaeandthePennatulacea.Atableofalloctocoralliantaxainwhich
bioluminescence has been recorded (along with newly presented data) is also included,
alongwithabriefreviewofbioluminescenceintheOctocorallia.Twoadditionalspeciesof
Eleutherobia, which are presently unidentified and presumably undescribed, one from
Palau,andtheotherfromthePhilippineandMarianaArchipelagos,areherereportedto
also bioluminesce.
Previously, bioluminescence in octocorals has been presumed to be restricted to many, butnot
all, sea pens (Pennatulacea) and two to four species ofgorgonians (Alcyonacea: Isididae) (Harvey
1952; Muzik 1978). The present paper reports the discovery ofbioluminescence in a species ofthe
alcyoniidgenusEleutherobia fromthe Solomon Islands. Thediscoveryrepresentsthefirstrecordof
bioluminescence in a softcoral.
The genus Eleutherobia was last revised by Verseveldt and Bayer (1988). Three species of
Eleutherobiahaverecentlybeendescribed: E. luteaBenayahuandSchleyer, 1995,fromNatal,South
Africa;E.zanahoriaWilliams,2000, fromtheTongaIslands;andE. vinadigitariaWilliamsandLit-
tle, 2001, also fromNatal, South Africa. Seventeendescribed sp—ecies ofthegenus (consideredvalid
taxa)areknownfromsouthernAfricaandtheIndo-WestPacific fourfromsouthernAfricaandthir-
teen from the Indo-West Pacific (Somalia to Japan and Tonga). Bioluminescence has not been re-
ported in anypreviouslydescribed species ofthe genus.
Material collected from a disjunct population ofa soft coral species identified as Eleutherobia
grayi(ThomsonandDean, 1931)isdescribedfromtheSolomonIslands.Thespecimensdonotdiffer
morphologically from the lectotype (redescribedbyVerseveldt and Bayer 1988), whichwasclearly
illustrated with scanning electron micrographs ofsclerites. However, the Solomon Islands material
differsecologicallyinonerespectfromthetypematerialandotherknownspecimens.Thepreviously
known material: type specimens from Indonesia, andarecord from the RyukyuIslands (Verseveldt
andBayer 1988:33),wascollectedfromsandyorrubblybottomsubstrata(sandwithsmallstonesand
shellsorpiecesofdeadcoral),whereasspecimensfromthenewlydiscoveredpopulation intheSolo-
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Volume52, No. 17
monIslandshavebeenobservedonlyonhardsubstrata(floors,wallsandceilingsoflimestonecaves,
alcoves,andoverhangs). Thepopulationsalsodifferbathymetrically. TheIndonesianandRyukyuan
populations are known from 30-73 m, while the Solomon Islands population has been observed at
shallowerdepths, 5-18 m.
Williams(2000:159)hassummarizedrecentdiscoveriespertainingtonaturalproductsbiochem-
istry andthe genus Eleutherobia.
Material and Methods
MaterialforthisstudywascollectedbySCUBAandpreserveddirectlyin70%ethanol. Sclerites
were isolated by disassociating them from the coenenchyme with household bleach (sodium
hypochlorite).UnderwaterphotographsforFigure I weremadewithaNikonis-VcameraandNikonis
SB 103 flashunit.OtherphotographsandmicrographsweremadeusingaNikonCoolpix990digital
cameraandaNikon SMZ-1 dissectingmicroscope. Scanningelectronmicrographsweremadewith
a Leo 1400 series scanning electron microscope. Sclerite drawings were made using an Olympus
CH-2 compound microscope with an attached drawing tube. Digital images and plates ofphoto-
graphs, micrographs, and scanning electron micrographs were made using Adobe Photoshop soft-
ware. An abbreviation used in the text is CAS (California Academy ofSciences, San Francisco).
Systematic Account
Family Alcyoniidae Lamouroux, 1812
Eleutherobia Putter, 1900
Eleutherobia Putter, 1900:449. Verseveldtand Bayer, 1988:27. Williams, 1992:306; 2000:160. Williams and
Little, 2001.
—
Diagnosis. Alcyoniid soft corals, colonies digitiform (finger-like), conical or cylindrical,
rarely lobate to subglobular. Polyps monomorphic with calyces absent, however, retracted polyps
mayform lowroundedorconspicuousandmound-likeprotuberancesofthecoenenchyme. Sclerites
predominantlyderivedfromradiates,withspindles,barrels,tuberculatespheroids,rod-likeforms,or
crossessometimespresent. Anthocodial scleritespresentascrownandpoints,oraseightpointsonly,
oraltogetherabsent.—Colorvariable.
Type Species. Eleutherobiaj—aponica Putter, 1900, by monotypy.
DiversityANDDistribution. SeventeenspeciesintheIndo-WestPacificandSouthAfrica
(eastern and southern Africa to Japan, Saipan, and Tonga) (Fig. lOB).
Eleutherobiagrayi(Thomson and Dean, 1931)
Figs. 1-10
NidaliagrayiThomsonand Dean, 1931:37, pi. 2 fig. 2. Type locality: Indonesia.
Eleutherobiagrayi : Verseveldtand Bayer, 1988:33, figs. 24, 25.
Eleutherobiasp.: Williams, 1996:34 (colorphotographstaken bothatnightandduringtheday).
—
MaterialExamined. CAS 101096, stationnumber35, Solomon Islands, MborokuaIsland
(Murray's Island), 18 mdepth, 9November 1994, collectedbyG. C. Williamswith aid ofSCUBA,
one whole specimen, 22 mm in length. CAS 147475, same data as CAS 101096, one specimen cut
longitudinallyintotwohalves, 29 mm in length. CAS 147476, station number 16, Solomon Islands,
WILLIAMS: BIOLUMINESCENT SOFTCORAL 21
Figure 1.Eleutherobiagraymi.mA-B.Underwaterphotographsoflivingsoftcorals, SolomonIslands. Colonies(excluding
polyps)areapproximately25 inlength.A.Photographtakenatnight.B.Photographtakenduringmidday.C.Lectotype,
approximately33mminlength(fromThomsonandDean 1931,pi. 2fig. 2).
2
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Mborokua Island (Murray's Island), 10 m depth, 12 September 1998, collected by G. C. Williams
with aid ofSCUBA, onewhole specimen, 24 mm in length. CAS 101095, station number20, Solo-
mon Islands, Mborokua Island(Murray's Island), 16 mdepth,4November 1994, collectedbyG. C.
Williams with aid o—fSCUBA, three whole specimens: 22 mm, 24 mm, and 27 mm in length.
Description. Growth form and size. Alcyoniid soft corals in which the colonies are
digitiform(Figs. 1A,2E)orsomewhatlobate(Figs. 1B,2A-D),mostlycylindricalinshape(Fig.2E),
not markedly tapered, distal apex bluntly rounded (Figs. IB, 2B-E), somewhat truncate (Figs. IC,
2A)orsomewhatclavate(Fig.2A,C,D),notpointed.Thestalkisveryshort,asthepolypsaredistrib-
utedoverapproximately95%ofsurfaceofcolony(Figs. 1,2). Thepolypariesofmostcoloniesarise
directly from a broad holdfast (Figs. IC, 2A). Wet-preserved colonies vary in length from 1 1 to
29 mm.
Polyps. The polyps are arranged uniformly over the surface of the colonies. They are
monomorphic and do not have calyces, although the retracted polyps may form low rounded or
mound-likeprotuberancesonthesurfaceofthepolyparyin somepreservedortightlyretractedcolo-
nies(Fig. 1C).Theseprotuberancesareformedfromthecoenenchymeandhencecannotbedefinedas
true calyces. In most cases, the retractedpolyps are often more or less flush with the surface ofthe
polypary (Figs. IB, 2). Polyp sclerites are absent (Figs. 1A, 3, 4).
mm
Thelivingexpandedpolypsarecolorlessandtranslucent,9-12 inlength.Thelengthofphar-
ynxisapproximatelyone-thirdthelengthofthebodyofthepolyp(Figs. 1A,3).Theperistomeisalus-
trous and reflective opaque white, while the glandular uppermost portions of the mesenterial
filaments are pale yellowish orcream-colored (Fig. 1A). The narrow elongate tentacles are mostly
6-8 mm in length, gradually taper to a point, and have two opposite rows ofapproximately 12-16
pinnules. (Figs. 1A, 3, 4). Wet-preserved expanded polyps are opaque white (Fig. 2B).
mm
Sclerites. Sclerites are ofseveral distincttypes varying from 0.05 to 0.15 in length. In the
surface coenenchyme ofthe polypary and holdfast are seven-radiates (Figs. 5C; 6G; 7E, O; 81),
eight-radiates(Figs.5A,C;6C,I;71,K; 8B,F,N),crosses(Figs.7J, 8D),quadriradiateswiththreetu-
berclesinoneplane andonetubercleverticallydisposedinthe center(Fig. 6A), andtriradiates (Fig.
6K). Inthesubsurfacecoenenchymeanddeepinteriorofthecoloniesaretuberculaterodsandirregu-
larly-shaped, somewhat flattened, rod-like forms (Figs. 5B, D; 7G, L, P).
Color. Mostcolonies arebrickred (Fig. 1A), butsome have varyingamounts ofyellowcolor-
ation (Fig. 1B). Scler—ite colorvaries from red to orange, orcolorless.
Distribution. Solomon Islands (5-18 m depth) (present study) plus the type localities:
Ceram Sea,betweenMisool andthewesternendofNewGuinea; Indonesia(32 mdepth)(lectotype,
designated from two syntypesbyVerseveldtandBayer, 1988); and Flores Sea, northwestern end of
Sumbawa, Indonesia (73 m depth) [paralectotype, designated from two syntypes byVerseveldt and
Bayer(1988)]. Theyalsoreportedthespecies fromtheregionofOkinawain theRyukyu Islands,Ja-
pan (30 m depth). I have examineda largenumberofspecimens ofmaterial assignable tothe genus
EleutherobiafromOkinawa.ThesespecimensdifferinseveralrespectsfromEleutherohiagrayi,and
arehereconsideredto representanother(asyetundetermined) speciesofthegenus. I thereforecon-
siderthe occurrence—ofEleutherohiagrayi in the—Ryukyu Archipelago as unverified (Fig. 10).
VARIABILITY. Colony shape is variable digitiform, or bilobate, to somewhat globular.
Coloris also variabledepending on theproportionsofred, orange, andcolorless scleritespresent in
thecoenenchyme. Somecoloniesareauniformbrickred,orredwithyellowishpolypmounds,while
others are very pale pink with cream-colored mounds created by the retracted polyps. These ca-
—
lyx-likemoundsareusuallyuniformlycolored,butmaybebicoloredinsomecolonies yellowwith
eightradiating red stripes—, orred with yellow stripes (Fig. 1).
BlOLUMlNESCENCE. During night dives on three occasions (November 1993, November
1994,andSeptember 1998),avividgreenbioluminescence(brightgreen flash)wasobservedimme-
diatelyupontactilecontactwiththefiillyexpandedpolypsofEleutherohiagrayi.Thislightseemsto
WILLIAMS: BIOLUMINESCENTSOFTCORAL 213
Figure2.Eleutherobiagrayi. A. Wet-preservedspecimen(CAS 101096);22mminlength. B.Wet-preservedspecimen
withexpandedpolyps(CAS 147476);24mminlength.C.Wet-preservedspecimen(CAS 147475),externalview;29mmin
length. D. Wet-preserved specimen (CAS 147475), cut longitudinally to show internal aspects; 29mm in length. E.
Wet-preservedspecimen(CAS 101095);27mminlength. Scalebar= 12mm.
emanatefromtheregionoftheperistome(oraldisc)andthedistal-mostregion ofthepharynx (Figs.
1A, 3,4), althoughthepreciseoriginofluminescenceremainsuncertain. Theperistomeappears lus-
trouswhiteunderthewhite-lightofanunderwatercameraflashunit,andthusdisplaysastrikingcon-
trastto otherpartsofthe softcoral colony (Fig. 1A). Research using epiflourescence microscopyto
determine the location ofphotocytes in this species is in progress.
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Figure3.Eleutherobiagrayi.Asinglepolyp,fullyextended;scalebar=3mm.
WILLIAMS: BIOLUMINESCENT SOFTCORAL 215
Figure4.Eleutherobiagrayi.Mouthandtentaclesshowingoraldiscsurroundingthemouth(peristome),whichisthesus-
pectedregionofbioluminescence;scalebar=5mm.
Since the polyps ofEleutherobia grayi are bioluminescent and devoid ofscleritic armature as
well, itispossiblethattheattributeofbioluminescenceprecludestheneed foranthocodial armature,
andmayberegardedas adefenseagainstpotentialpredatorsofthe softcoral polyps. Onlyoneother
describedspeciesofEleutherobia(£".zanahoriaWilliams,2000)isknowntolackpolyparmature,but
the presence orabsence ofbiolumi—nescence in this taxon is not known.
EcologicalObservations. Muchoftheshallowwater,hardcoralcoveratthetypelocality
was dramatically alteredbetween 1994 and 1998, presumablyby a combination ofwarming events
andaseriesofseverestorms.Physicaldecimationofhermatypicaswellasahermatypicscleractinians
tookplace,togetherwithasubstantialamountofbleaching(predominantlyonthedistal-mostextrem-
ities of the coral colonies). On the exposed reef flats and slopes, replacement of hermatypic
scleractinians by soft corals such as Paralemnalia spp. and various taxa ofcoralline algae, was ob-
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servedduringthisperiod.Inthelimestonecaves,alcoves,andoverhangs(Fig. 9),aphysicalreplace-
mentofTubastraeafaulkneriWells, 1982(whichprovidedthedominantcoverin 1993 and 1994)by
the softcoral Eleutherobiagrayi, was also observed during the same period.
Thepolypsofthesoftcoralareretractedintothebodyofthesoftcoralduringdaylighthours(Fig.
1B), gradually expand atdusk, andremain fully expanded (in feedingmode) forthe duration ofthe
night(Fig. lA).
SeveralcoloniesofEleutherobiagrayiwereobservedtohaveminuteepizoites(mostlytunicates
orbryozoans) gr—owing on the surface ofthe polyparies, between the polyps.
Remarks. Morphologically,material fromtheSolomon Islandspopulationfullyagreeswith
theoriginal descriptionofEleutherobiagrayibyThomson andDean(1931), andthewell-illustrated
redescriptionofthedesignatedlectotypebyVerseveldtandBayer(1988). Severalimportantpointsof
concurrence are listed below.
1. Total lack ofsclerites in the anthocodiae.
2. Redoryellow coloration due to varying amounts ofred andyellow sclerites.
3. Deep interiorofcolonies with many sclerites, almost exclusivelyrod-like forms.
mm mm
4. Sizerangeofsclerites: 0.05-0.15 (presentstudy); 0.03-0.18 (VerseveldtandBayer,
1988).
5. Scleritetypes:Eight-radiates,seven-radiates,triradiates,crosses,quadriradiateswiththreetu-
berclesinoneplaneandonetuberclearisingverticallyfromthecenter,andirregularly-shapedtuber-
culaterods.
DISCUSSION
—
BIOLUMINESCENCEINOCTOCORALS (Table 1). Forthe sake ofthe followingdiscussion, the
various groupsofoctocorals are defined as follows. Stoloniferous octocorals have separatepolyps
connectedattheirbasesbymembranousorribbon-likestolons. Softcoralshavepolypsembeddedin
acommoncoenenchymeandareattachedtohardsubstratabybasal holdfasts,theyhavenoaxial de-
velopment, andonly free sclerites comprise the skeletal elements. Gorgonians, like the soft corals,
havepolypsembeddedinacommoncoenenchymeand areattachedtothesubstratumbybasal hold-
fasts,butunlikesoftcorals,inadditiontofreesclerites,havesomeformofinternalaxialdevelopment
composedofcalciumcarbonate,gorgonin,oracombinationofthetwo. Seapensorpennatulaceans
havethecoralcolonydividedintoaproximalmuscularpedunclethatisanchoredinsoftsubstrata,and
adistalrachisthatcontainsseveralkindsofpolyps.Theymayormaynothaveacalcareousaxialskel-
eton.
Williams (1999:23, 49-50) provided a historical review and comprehensive bibliography per-
taining to pennatulacean bioluminescence. The scientific literature regarding bioluminescence in
octocorals is relatively rich, extending back to the sixteenth century with the works of Gesner,
Boussuet, Imperato, Rondelet, and others. Important modem contributions include: Panceri (1871,
1872a, b); Parker(1920); Harvey (1940, 1952); Nicol (1958); Titschak (1965, 1966); Morin (1974,
1976);Muzik(1978); andHerring(1991). Harvey(1952:168)stated,". . . butamongtheAlcyonaria
are to be found some ofthe most brilliant and striking luminous animals. Ofthe three groups of
Alcyonaria, the Alcyonacea, the Gorgonacea, and the Pennatulacea, only luminescence of the
Pennatulacea has been carefully studied." Pertaining to alcyonaceans, only a few species in the
gorgonian familyIsididaehavebeenknowntoluminesce. Mangold's(1910)recordofLeuckart'slu-
minescentAlcyonium isconsideredbyHarvey(1952:169-170)tobe"verydubious."Nosubsequent
recordsofbioluminescence inthegenusAlcyonium,oranyothersoftcoral taxon forthatmatter, are
known in the previous literature.
The only records ofbioluminescent soft corals are represented by new data presented here of
Eleutherobiagrayifrom the Solomon Islands, aswell as observations made on two otherspecies of
WILLIAMS: BIOLUMINESCENT SOFTCORAL 217
Table 1. Recordsofbioluminescenceinoctocorals.
Taxon
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Figure5.Eleutherobiagrayisp.nov.Sclerites.A.Polyparysurface.B.Polyparyinterior.C.Stalksurface.D.Stalkinterior.
Scalebar=0.1 mm.
