First record of a bioluminescent soft coral: description of a disjunct population of Eleutherobia grayi (Thomson and Dean, 1921) from the Solomon Islands, with a review of bioluminescence in the Octocorallia PDF
Preview First record of a bioluminescent soft coral: description of a disjunct population of Eleutherobia grayi (Thomson and Dean, 1921) from the Solomon Islands, with a review of bioluminescence in the Octocorallia
PROCEEDINGS 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- 209 PROCEEDINGSOFTHECALIFORNIA ACADEMY OF SCIENCES 2 1 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 21 PROCEEDINGSOFTHECALIFORNIA ACADEMYOF SCIENCES Volume 52, No. 17 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. PROCEEDINGS OFTHECALIFORNIA ACADEMYOF SCIENCES 214 Volume52, No. 17 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- 216 PROCEEDINGSOFTHECALIFORNIA ACADEMYOF SCIENCES Volume 52, No. 17 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 218 PROCEEDINGSOFTHECALIFORNIA ACADEMY OF SCIENCES Volume52, No. 17 Figure5.Eleutherobiagrayisp.nov.Sclerites.A.Polyparysurface.B.Polyparyinterior.C.Stalksurface.D.Stalkinterior. Scalebar=0.1 mm.
The list of books you might like
