Table Of ContentNachrBl.bayer.Ent. 40 (1)
Adaptationmechanisnis in the dorsal ocelli
ofPeriplaneta americana
(Orthopteroidea:Blattaria.Blattidae)
VonH.WUNDERER,P.SEIFERT&G.WEBER
Abstract
Light- and dark-adaptedocelliofthecockroach Periplaneta americana wereinvestigated
usinganultrastructuralandhistochemicalapproach.Thedegradativerouteofphotoreceptive
membraneobservedduringlightadaptationiscomparabletothatininsectCompoundeyes.Ape-
culiarphotoreceptororganeileishistochemicallyshowntobelysosome-related. Duringdark
adaptation,therhabdomsarereorganized;endoplasmiccisternaeassembleaspalisadesaround
therhabdoms.
Introduction
ManyinsectshavethreedorsalocelliattheVertexofthehead;onlytwoocelliina
slightlydifferentpositionarepresentinsomegroupslikemothsandcockroaches(rev.
Goodman1981).Theocellimaybeinvolvedinveryvariablefunctions,e.g.polarotaxis
indesertants(Fent&Wehner 1985),horizondetectioninlocusts(rev.Rowell1988),
flightequilibriumcontrolindragonflies(Stange1981),triggeringofthecircadianac-
tivityinarctiidmoths(Wunderer&deKrämer1989).Thecockroachocellishowawell
organizedretina (Cooter 1975, Weber &Renner 1976) andcomplexnervousconnec-
tions(Cooter1975,Toh&Hara1984,Toh&Sagara1984).Withregardtotheirfunction,
several contradictoryinvestigationsexist(seediscussionbyRivault 1983)butitre-
mainsunclearasyet.Moreover,theseocellishowprominentadaptationmechanisms
whichwillbereportedhere.
Materialsandmethods
1.Animals.MaleadultsorlastmsiarsoiPeriplanetaamericana'L.wereusedfrom
a culture attheZoologicalInstituteofMunich. Theirlight/dark cyclewas 12:12h.
Lightadaptationbyindirectdaylightplusfluorescentlighting(intotalabout800lux)
occuredduringthenormalday,darkadaptationduringthenormalnightperiod.
2. Transmission electron microscopy followed conventional techniques.
After2hadaptation,partsoftheheadbearingtheocelliwerefixatedfor4hat4°C
with5%glutaraldehydeinSörensen'sphosphatebufferwith4%sucrose,pH7.4(cf.
Glauert1975).Afterseveralbufferrinsesandpostfixationwith2%osmiumtetroxide
inthesamebuffer(2hat4°C),thespecimensweredehydratedingradedethanoland
embeddedinDurcupanACM(Fluka/Buchs,Switzerland)viapropyleneoxide.Serial
0.5-1.0ixmsemithinsectionsthroughanocellusalternatedwith60-90/umultrathin
sections. Light microscopical control was done with the semithin sections stained
wuriatnhyalamciexttautreeanofdmleeatdhycilternatee,blaunedaenxdamAiznuerdIwI.itUhltaraZteihsisnEseMct9iAonosrwEerMe1staatin6e0dkwVi.th
3. Histochemistry. ContentsofacidPhosphataseweredemonstratedusingthe
methodofKreutzberg&Hager(1966).TheabovefixationbutwithIMcacodylatebuf-
ferwasapplied.Theincubationmedium(15minat37°C)consistedof0.05Macetate
bufferpH5.0with0.19%sodium-glycerophosphate,0.13%leadnitrate,and0.006%
sucrose,followedbyseveralwashesin0.1Macetatebufferanddehydration.Controls
weretreatedwithi)incubationmediumwithoutsodium-glycerophosphate;ii)com-
pletemediumwithO.OIMNaFaddedasInhibitor.Unstainedultrathinsectionswere
examinedintheelectronmicroscope.
Nachi-Bl.bayer.Ent.40 (1)
ResultsandDiscussion
1. Photoreceptors after light adaptation.
Thestructuralfeaturesofthelight-adaptedocellushavebeendescribedingeneral
byCooTER(1975)andWeber&Renner(1976).Therhabdomconfigurations(Figs. 1,4)
arebuiltbyafusionof2-6rhabdomeresfromneighbouringphotoreceptorcells.Adis-
stinctborderUnebetweentheSinglerhabdomeresistypicallyvisibleinsectionedpro-
filesoflight-adaptedrhabdoms(Figs. 1,2).Thus,therhabdomerescomprisemicro-
villiofequallength(approx. 1 /xm).Attherhabdomericborders(wherethemicrovilli
originale), coatedpitsandmembranewhorlsareadhering.Thesubrhabdomericre-
gionofthelight-adaptedphotoreceptorcellsexhibitssacculiofthesmoothendoplas-
micreticuluminarandomdistribution(Fig.2).Additionalorganellescanbeobserved
inthisregion:numerousGolgiStacks,differenttypesofdensebodies,lipiddroplets
(Fig.3), andmultitubularbodies(Figs.2,3).Themultitubularbodieshavebeende-
scribed by Weber & Renner (1976) as peculiarorganelles of thephotoreceptorcells
withinthePeriplanetaocellus.Theyareonlypresentduringlightadaptation.
Theseorganellescanbefurthercharacterizedbyahistochemicaltestforacidphos-
phatases. Incubation of the ocellar retina with sodium glycerophosphate (see
Methods)revealspositive, fine-granularleadprecipitatesonlywithinmultitubular
(Fig. 3)anddensebodies.Precipitatesareneverfoundinlipiddropletsnearby(Fig. 3),
orinanyothercompartment; theyarecompletelyabsentincontrols.Hence,multi-
tubularanddensebodiesintheocellarphotoreceptorscanbeclassifiedaslysosome-
relatedbodies(cf.Hafneretal.1980;rev.Blest1988).
2. Photoreceptors after dark adaptation.
Several profound changes of the photoreceptor cell structure occurduring dark
adaptation. Incontrasttothelight-adaptedrhabdoms,theclearmiddleborderline
betweenadjacentrhabdomeresdisappears(Fig.4).Partsoftherhabdomeresinterdi-
gitate(Fig. 5);now,itisnolongerpossibletodefinitelyascribethemtotherespective
photoreceptorcells.Anumberofmicrovilliwithlenghtsofupto2.5/Limreachoverthe
wholewidthofsuchrhabdomprofiles (Fig. 5). SeveralmicrovillarrowsshowaU-
shapedappearanceastheybecomecross-connectedattherhabdomborderbymem-
branelayers(Fig.5).Thisfeatureremindsof"membraneloops"inthedevelopmentof
thisocellus(Toh&Yokohari1988),indark-adaptedocelliofwasps(Pabst&Kral1989)
andofarctiidmoths(Grunewald&Wunderer1990).
Afterdark adaptation, voluminous perirhabdomeral palisades areobvious along
theentirerhabdomlength(Fig.4).Similarpalisadeshavealsobeendescribedindark-
adaptedocelliofSc/iistocercagregraria(Goodman1970,1981).Simultaneously,smaller
vesiclesandsacculiofthesmoothendoplasmicreticulumhavedisappearedfromthe
receptorcellcytoplasminthisState.Itmaybeconcluded,therefore,thatthepalisades
havebeenformedbyanaggregationandfusionofvesicularprofilesneartherhabdom
border.Otherorganellesdescribedaboveforthelight-adaptedstatearelessfrequent
orcompletelyabsent,inparticularthemultitubularbodies.
ItfollowsthatobviousstructuraldifferencesoftheocelliinPeriplanetaamericana
arecorrelatedwithlightanddarkadaptation.Atthesametime,thesedifferencesgive
anindicationofthepathwaysformembraneturnover.Thelight-adaptedphotorecep-
torcellsarecharacterizedbycontainingcertaintypesofdegradativeorganelles.The
obsei"vedpinocytoticeventsandvesiclescanbeassumedtomedialetheincorporation
ofmicrovillarmembranesintothereceptorcell,eventswhicharewellknowninother
ivensviecrutleabrrabtoedipehsotaorreefcoerpmtoerdsf(orlelvos.wiWnhgiptieneotcyalt.os1i9s80(,1.Bcl.)eswthi1c98h8)a.reInsetlhdesoemcmastehse,omcuelütai-r
photoreceptors of P.americana. Here, the frequent multitubularbodies mayserve
thisfunction;thisissuggestedbytheirenzymecontent.Thetubuliwithinthesebodies
arestructurallycomparablewiththerhabdomericmicrovilli(Fig. 3).Therefore,these
bodiescouldbedirectlyformedbyaphagocytoticuptakeofrhabdomericpieces,an
alternativeto themostlydescribedformationbyassembliesofpinocytoticvesicles
NachrBl.bayer.Ent.40 (1)
NachrBl.bayer.Ent.40 (1)
(compareBlest1980).Thefurtherwayofdegradingincorporatedmembranesusually
leadstodensebodies,andfinallytolipiddroplets(rev.Blest1988).Boththeseorgan-
ellesarepresentinthelight-adaptedocellarphotoreceptorsofP.americana.
Theformationofperirhabdomeralpalisadesduringdarkadaptationistypicalfor
photoreceptorsintheocelliofP.americana,initsCompoundeyes(Butler1973),and
inthoseofseveralotherinsects(rev.Goldsmith&Bernard1974).Itisdiscussedasan
opticalconsequenceofsuchpalisadesneartherhabdomthattherefractiveindexbe-
tween rhabdomeric microvilli and receptor cytoplasm becomes modified (see the
abovereview).Thisresultsinatotalreflectionoflightattherhabdomborder,hence
abetterguidingoflightwithinthedark-adaptedrhabdoms.Besidethisfunction,the
ampleSystemofcisternaeformedbysuchpalisadescouldserveasaneffectiveand
localcalciumsinkwhichwouldmodifythesensitivityofthereceptorcells(rev.Walz
&Baumann1989).
Inconclusion, ourexaminationhasshownthattheocellusofthecockroachPeri-
planeta americana undergoes adaptational changes in the light and dark which
involveaconsiderableturnoverofphotoreceptivemembranes.
Zusammenfassung
Hell-unddunkeiadaptierteOcellenderSchabePeriplanetaamericanawurdenul-
trastrukturellundhistochemischuntersucht.BeiHelladaptationkanneinAbbaufo-
torezeptiverMembranenübermehrereAbbaustufenfestgestelltwerden,wieervon
Komplexaugen bekannt ist. Ein spezielles Degradations-Organell wird histoche-
mischnachgewiesen.BeiDunkeladaptationkommteszueinerRhabdom-Umbildung
undzurEntstehungvonrhabdomnahenPalisaden.
Referenees
Blest, A.D. 1980; Photoreceptor membrane turnoverin arthropods: comparativestudies of
bofreCoanksdtoawnntpLriogchest.osensVainsduatlhePirrociemspsleisc.at-ionPsl.eInnuWmiPlrleisasm,sN,eT.wPY.o&rkB,a2k1e7r,-2B4.5N..:TheEffects
- — 1988:TheturnoverofphototransductivemembraneinCompoundeyesandocelli.In:Evans,
P.D.&WiGGLESWORTH,V.B.:AdvancesinInsectPhysiologyVol.20. -AcademicPress,
London,1—53.
Butler-,JR..C1o9m73p.:TPhheysainoal.to8m3"y2o3f9t-h2e6C2o.mpoundeyeofPeriplanetaamericanaL.2.Finestructure.
Cooter,R.J.1975:OcellusandocellarnervesofPeriplanetaamericanaL.(Orthoptera:Dictyo-
ptera).-Int.J.InsectMorphol.&Embryol.4,273-288.
Fent,K.&Wehner,R.1985:Ocelli:acelestialcompassinthedesertantCataglyphis.-Science
228,192-194.
Glauert,A.M.1975:Fixation,dehydrationandembeddingofbiologicalspecimens.In:Practical
MethodsinElectronMicroscopyVol.3/1.-North-Holland,Amsterdam.
GoLDSMiTH,T.H.&Bernakd,G.D.1974:Thevisualsystemofinsects.In:Rockstein,M.:ThePhy-
siologyotInsectaII.-AcademicPress,London,165-272.
Goodman,L.J.1970:Thestructureandfunctionoftheinsectdorsalocellus.-Adv.InsectPhy-
siol.7,97-195.
OcellarretinaotPeriplanetaamericana,left:inlightadaptation,right:indarkadaptation.
Fig.1: Rhabdomconfigurations(RH)areformedbyseveralneighbourmgphotoreceptorcells
with nuclei (N). Middle borderlinebetween contributing rhabdomeres indicated by arrows.
Scale:5/um.Fig.2:Multitubularbody(MTB)neighbouring(electron-lucent)sacculiofendoplas-
micreticulumandseveralelectron-denseprotiles.Rhabdom(RH)withdistinctmiddleborder-
lsipnhea.tSacsaelew:it1hßinm.muFlitg.it3u:buEllaecrtbroond-yde(nMsTeB,)doetn-clliokseinpgrelciippiidtadtreosplientdi(cLa)t.iNngotaectsiivmiitlyaroiftaycoifdMPhToB-
Contentswithmicrovilliofrhabdom(RH)nearby.(x16.800).
Figs.4,5: RH: dark-adaptedrhabdoms,N:photoreceptornuclei. Subrhabdomericpalisades
indicatedbysmallarrows.5showsaggi-egationotsmallerperirhabdomeralcisternae(arrows),
Insetin4showslargepalisades.Noteabsenceofmiddleborderlineswithinrhabdoms(RH)(only
partiallyin5).Arrowheadsin5indicateU-shapedmicrovilliandmembraneloops.Scalebars:
5/u,min4,1/um5.
NachrBl.bayer.Ent.40 (1)
- - 1981: Organisation and physiolog>' oftheinsect dorsalocellarSystem. In: Autrum, H.:
HandbookofSensoryPhysiologyVol.VII/6C.-Springer,Berlin,201-286.
Grünewald,B.&Wunderer,H.1990;Theocelliofarctiidmoths:structureofthelight-anddark-
adaptedretina.In:ELSNER,N.&RoTH,G.:Proc. 18thGöttingenNeurobiol.Conf.-Thieme,
Stuttgart,204.
Hafner,G.S.,Hammond-Soltis,G.&Tokarski,T. 1980:Diurnalchangesoflysosome-related
bodiesinthecrayfishphotoreceptorcells.-CellTissueRes.206,319-332.
Kreutzberg,G.W.&Hager,H.1966:ElectronmicroscopicaldemonstrationofacidPhosphatase
Pabst,acMt.ivAi.ty&inKrtahel,ceKn.tr1a9l8n9:erEvfofuesctSsysoftegmr.ee-nHainsdtoUcVhelmiigeht6,an2d54d-a2r5k9n.essontheultrastructure
ofocellarphotoreceptorsinthewaspParavespulagermanica.-Z.mikrosk.anat.Forsch.
103,459-475.
Rivault,C.1983:Roleofphotoreceptorsinthesynchronizationofthecircadianlocomotoracti-
vityrhythmswiththeLDcycleincockroaches{Periplanetaamericana).-J.interdiscipl.
CycleRes.14,21-31.
RowELL,C.H.F.1988:Mechanismsofflightsteeringinlocusts.-Experientia44,389-395.
Stange,G.1981:Theocellarcomponentofflightequilibriumcontrolindragonflies.-J Comp.
Physiol.141,335-347.
ToH,Y.&Sagara,H.1984:DorsalocellarSystemoftheAmericancockroach.1.Structureofthe
ocellusandocellarnerve.-J.Ultrastruct.Res.86,119-134.
ToH,Y.&Hara,S. 1984: DorsalocellarSystemoftheAmericancockroach.2.Structureofthe
ocellartract.-J.Ultrastruct.Res.86,135-148.
ToH,Y.&Yokohari,f.1988:PostembryonicdevelopmentofthedorsalocellusoftheAmerican
cockroach.-J.Comp.Neurol.269,157-167.
Walz,lBo.gi&caBlauamnadnnf,unOc.ti1o9n8a9l:Ccahalrcaicutme-rsiezqauteiosnt.er-ingPrcoelglr.orgHainsetlolecsh:emi.nsiCtyutloocchaelimz.atViooln.,m2o0r/pNhoo2-,
G.Fischer,Stuttgart.
Weber,G.&Renner,M.1976:Theocellusofthecockroach,Periplanetaamericana(Blattariae).
Receptoryarea.-CellTissueRes.168,209-222.
White,R.H.,Gifford,D.&Michaud,N.A.1980:Turnoverofphotoreceptormembraneinthelar-
valmosquitoocellus:rhabdomericcoatedvesiclesandorganellesofthevacuolarSystem.
In: Williams,T.P.&Baker,B.N.:TheEffectsofConstantLightonVisualProcesses. -
PlenumPress,NewYork,271-296.
Wunderer,H.&deKramer.J.J.1989:Dorsalocelliandlight-induceddiurnalactivitypattems
inthearctiidmothCreatonotostransiens.-J.InsectPhysiol.35,87-95.
AnschriftderAutoren:
HansjörgWunderer,Zoolog.Institut/Biol.I,
Universitätsstraße31,D-8400Regensburg,F.R.G.
PeterSeifert,Zoolog.Institut,Luisenstraße14,D-8000München2,F.R.G.
GerhardWeber,PlaneggerStraße24A,D-8000München,F.R.G.
Wie sehenInsektenpolarisiertes Licht?
(Diptera,Syrphidae,Tabanidae)
VonFranziskaPILSTL,AndreasLANGE,PeterSEIFERTundUlrichSMOLA
Abstract
ForthreedipteranspecieshighlyspecializedvisualcellsinthedorsalrimareaoftheCompound
eyearedescribed.Withintheseommatidiatheeightretinulacellsaremorphologicallydifferent
fromthoseofnormalommatidia.TheretinulacellsRl-6havereducedrhabdomeresandcellso-
mata,therhabdomeresofthecentralcellsR7andR8areenlarged.Thesetwocellsformshort
rhabdomeralSegments,whicharealignedoneafteranothersoresemblingtherhabdomsfoundin
some Crustaceans. Judging from their morphology these highly specialized ommatidia are
extremelysensitiveforpolarizedskylight.
ImGegensatzzuunsMenschenbesitzenInsektenverschiedenerOrdnungendiebe-
merkenswerteFähigkeit,linearpolarisiertesLichtwahrnehmenzukönnen.
