© 2014.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2014)217,3853-3861doi:10.1242/jeb.102947 Received 20February 2014;Accepted3September2014 ‡ contributed*These equally tothiswork authors Biology, IllinoisUniversity, of Northeastern Department Chicago, IL60625,USA. al., 2001;Saunders,2002). clock-controlled physiologicalandbehavioralprocesses(Harmer et output pathway. Together thesecomponentsregulatethe target, one ormoreinterconnectedoscillatoryclockmechanisms,and an of asensoryinputpathway(e.g.photo-ortemperaturereception), changes iscriticalforsurvival.Ingeneral,circadiansystemsconsist The capacitytoanticipateratherthansimplyrespond these factors oftheecosystem,suchaslight,temperatureandhumidity. physiology andbehaviorwithsystematicchangesintheabiotic Circadian systemshaveevolvedtocoordinateananimal’s Prey recognition,Locomotorbehavior KEY WORDS:Mantodea,Prayingmantis,Circadianrhythm,ERG, and behavioroftheprayingmantis circadian rhythmsmodulateseveralaspectsofthevisualphysiology We usedamultilevelexperimentalapproachtoassesswhether onset), butpersistwithperiodsof~24 rhythms thataresynchronizedtoenvironmentalcues(e.g.light Many behaviorsandphysiologicalprocessesoscillatewithcircadian Aaron E.Schirmer* patellifera color, strikingbehaviorandlocomotionoftheprayingmantis Circadian rhythmsaffect electroretinogram, compoundeye RESEARCH ARTICLE the complexitiesofcircadianrhythmsinMantodea. patellifera. Ourresultsrepresentanintriguingfirststepinuncovering operate atthecellular, cellularsystemsandorganismallevelin light cues.Together, thesedataindicatethatcircadianrhythms circadian clocksmodulatingbothwereentrainedtoenvironmental cycles andanticipatedthelight–darktransition,suggestingthat migration andlocomotorbehaviorrespondedstronglytolight:dark around thetransitiontimefromdaytonight.Inaddition,pigment during thesubjectiveday. Locomotoractivitywasstronglyclustered responsiveness washighestduringthesubjectivenightandlowest like stimuliandgrosslocomotoractivity. Inthefirsttwocases, photoreceptor sensitivitytolight,appetitiveresponsivenessprey- under constantconditions,withperiodsof~24 modulate eachofthetargetbehaviors.Strongrhythms,persisting apparatus. Ourresultsindicatethatcircadianclockscontroland/or analyses oflocomotoractivitypatternsonamodifiedtreadmill responsiveness tocomputer-generatedprey-likevisualstimuliand changes (screeningpigmentmigration),behavioralassaysof colorimetric photographicanalysestoassesscompoundeyecolor electroretinograms (ERGs)toassesscompoundeyesensitivity, INTRODUCTION ABSTRACT Author ([email protected]) for correspondence ,‡ , FrederickR.Prete*,EdgarS.Mantes,AndrewF. UrdialesandWil Bogue

h intheabsenceofsuchcues. h wereevidentin . We used H. the photoreceptors synapse(e.g.Starkand Wasserman, 1972; depolarization ofthelaminamonopolar cells(LMCs)ontowhich transient OFF;Fig. Offset. Thefirstwasasharp,corneanegativewaveform (the region b).Thenexttwocomponents wereelicitedbystimulus a moreslowlydecayingwaveform (i.e.thesustainedON;Fig. hyperpolarizing notchonitsrising phase(arrowhead)followedby Fig. sharp depolarizationelicitedbylightonset(i.e.thetransient ON; distinct components.Thefirstwasaphototransduction-induced, elicited byasquarewavelightstimulus,theERGdisplayedseveral 1.When A representativelightadaptedERGisshowninFig. maderae pacemakers controlcuticleformationincockroaches( et al.,2000;Bebas2001).Forexample,independent overarching control(e.g.GiebultowiczandJoy, 1992;Giebultowicz distributed pacemakersoperateindependentlywithoutany environmental cues.However, insomearthropods,multiple or‘central’coordinated bya‘master’, pacemakersynchronizedto modified treadmill. et al.,2013b);and(4)analysesofgrosslocomotoractivity ona to computergeneratedvisualstimuli(e.g.Preteetal.,2013a; Prete behavioral teststoassesschangesintrackingandstrikingresponses color changeswhichresultfromscreeningpigmentmigration;(3) sensitivity; (2)photographic,colorimetricanalysesofcompoundeye electroretinograms (ERGs)toassesschangesincompoundeye Serville 1838.Theexperimentsincluded(1)chronic and behavioralparametersinthemantis and towhatextentcircadianrhythmsmodulateseveralphysiological done usingprayingmantises(:Mantodea). studies (Rossel,1979;Horridgeetal.,1981),noanalyseshavebeen Matsumoto, 2010)].Furthermore,withtheexceptionofjusttwo cockroaches andcrickets(Pandaetal.,2002;Tomioka and analysis havebeendoneinonlyafewspecies[e.g. described inavarietyofinsects,studiesacrossmultiplelevels (Pittendrigh, 1960).Althoughcircadianrhythmshavebeen and bestableacrossphysiologicallyrelevanttemperatures persist underconstantenvironmentalconditions(beself-sustaining) must entraintosomeenvironmentalcue(s),haveaperiodof~24 pacemakers, truecircadianrhythmsmustmeetseveralcriteria:they (Underwood etal.,2010;Tomioka etal.,2012). Samia Cynthia kueniella Electroretinograms RESULTS Some circadiansystemsarehierarchicallyorganized and In thisstudy, weusedamultilevelapproachtodeterminewhether Whether controlledbyonemasterorseveralindependent 1, pointa).Thiswaveformsometimesdisplayed a and and Blaberus Lymantria dispar)andsteroidhormonereleasein , Rhodinus prolixus 1, pointc)understoodto represent the sp.), spermreleaseinmoths( and Hierodula patellifera Galleria mellonella Leucophaea Drosophila, Anagasta 3853

1, h,

The Journal of Experimental Biology 3854 region e(PopkiewiczandPrete,2013)],alsoreferredtoasafter recovering, corneapositivewaveform,thesustainedOFF[Fig. Popkiewicz andPrete,2013).Thefinalcomponentwasaslowly Coombe, 1986;Montell,1999;HardieandRaghu,2001; Fig. RESEARCH ARTICLE on PopkiewiczandPrete(PopkiewiczPrete,2013). the transientOFFandsustainedmaximum.Measurementsbased maximum derivativeofthesustainedOFFmeasuredbetweenrecovery caused bytheefflux ofthecationsadmittedduringdepolarization.(f)The the transientOFF. (e)ThesustainedOFForafterhyperpolarization(AHP) OFF, representinglaminamonopolarcelldepolarization.(d)Theamplitudeof the gradualrectificationofphotoreceptordepolarization.(c)Thetransient notch ontherisingphase.(b)TheslowlydecayingsustainedONindicating light-induced depolarization.Thearrowheadindicatesahyperpolarizing patellifera

Normalized average Stimulus (LED)

0.5 0.6 0.7 0.8 0.9 1.0 .Measurementsusedtoanalyzeatypicalmantis( 1. 0.5 0.6 0.7 0.8 0.9 1.0 0.4 0.5 0.6 0.7 0.8 0.9 1.0 0 0 0 C E AB ) electroretinogram(ERG). Transient ON:max.amp. ○ Transient OFF:amp. Max. amp. 5 mV

Sustained OFF: 24

24 48 24 48 ON OFF a ● 1000 ms Latency tomax.

48 b R 2 =0.6415

f (a) ThetransientON,aninitialrapid c e

72

72 72 Hours 0 0.2 0.4 0.6 0.8 1.0 c 0.5 0.6 0.7 0.8 0.9 1.0 0.4 0.5 0.6 0.7 0.8 0.9 1.0 0.4 0.5 0.6 0.7 0.8 0.9 1.0 d 0 0 0 Hierodula D F Sustained ON:meanderiv. Transient OFF:meanderiv. Sustained OFF:max.deriv.

24 24 24

1,

rectification) oscillatedwithaperiodof22 ON meanderivative(representingtheoverallaveragerateofsignal phototransduction inducedreceptordepolarization),andthesustained amplitude andthetransientOFFmeanderivative;Fig. activity didnotdisplayanyclearrhythmicity(i.e.thetransientOFF However, thetwomeasuresunderstoodtobeassociatedwithLMC the sustainedOFFmaximumamplitude(Fig. sustained onmeanderivative,theOFFandlatencyto rhythms. TheseincludethetransientONmaximumamplitude, associated withphotoreceptoractivitydisplayedclearcircadian were maintained.Ofthesevenparametersmeasured,fourofthose (black) periodsbasedonthelight:darkcycleinwhichmantises in Fig. conditions (N taken every15 (±s.d.) forsevenkeyERGmeasurescalculatedfromrecordings extruding thelight-inducedcationinflux(Jansonius,1990). sustained OFFisunderstoodtobecausedbyanelectrogenicpump et al.,1971;BrownandLisman,1972;Tsukahara etal.,1977).The hyperpolarization (AHP)(BaumannandHadjilazaro,1971;Koike (Fig. photoreceptor current)oscillatedinphasewiththetransientON OFF maximumamplitude(reflectinganoutward,rectifying the subjectivedayandnight,respectively. Likewise,thesustained Fig. antiphase toitsmaximumamplitude(period=20.25 to themaximumamplitudeofsustainedOFFoscillatedin

48 48 48 R R Both thetransientONmaximumamplitude(representing 2 2 h rpsi i.2depicttheaveragednormalizedvalues 2 The graphsinFig. 2A,B). Eachreachedtheirminimumandmaximumvaluesduring =0.3881 =0.4615

2C; period=22.5 2A,B indicatesubjectiveday(gray)andnight

72 72 72 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.102947 =4 ).Theblackandgraybarsbelowthedata

min over72continuoushoursunderconstantlight Amp., amplitude;deriv., derivative. OFF meanderivativedonotdisplayrhythmicoscillations. derivative, thetransientOFFamplitudeand circadian rhythms.(D–F)ThesustainedOFFmaximum the sustainedOFFmaximumamplitudedisplayclear sustained OFFmaximumamplitudeandthelatencyto amplitude, thesustainedONmeanderivative, day, respectively. (A–C)ThetransientONmaximum N under light:lightconditions.Values aremeans(±s.d., measured at15 ERG parametersin Fig. =4). Blackandgraybarsindicatesubjectivenight

.Theaveragednormalizedvaluesfor seven key 2.

h, Qp 89 =233,

min intervalsfor72continuoushours P H. patellifera.ERGswere ≤ 0.003). Incontrast,thelatency

h (Q

2A–C, respectively). 87 >217,

h,

2E,F). Qp P ≤ 80 0.003; =174,

The Journal of Experimental Biology to themaximumamplitudedecreased( F RESEARCH ARTICLE 72 A representativesetof24(out144) photographstakenfromone P over the72 however, thesustainedOFFmaximumderivativeincreasedslightly parameter wastoolowtorevealanyongoingpattern.Overall, (Fig. suggest asmalloscillationduringthefirst24 (Popkiewicz andPrete,2013)butitdidnot.However, thedata also tooscillateinphasewiththesustainedOFFamplitude (PopkiewiczandPrete,2013). seen inbothlight-anddark-adaptedERGsseveralotherspeciesof time andmaximumamplitudeofthesustainedOFFissimilartothat subsequent hyperpolarizationamplitudes,andbetweentheinitialrise P increased slightlyovertime( Prete, 2013).BoththetransientOFFanditsmeanderivative potential amplitudeinotherspeciesofmantis(Popkiewiczand transient OFFinthefaceoflarge fluctuationsinphotoreceptor This isconsistentwithdatademonstratingarelativestabilityofthe or itsmeanderivativeduringtheexperimentalperiod(Fig. Compound eye colorchange (24–48 (48–72 (0–24 ≤ 1,290 ≤ We wouldhaveexpectedthesustainedOFFmaximumderivative There werenooscillationsevidentinthetransientOFFamplitude 0.003); thatis,asthesustainedOFFamplitudeincreased,latency 0.0001). Thiscorrelationbetweenreceptordepolarizationand htgahcsre ssoni i.3A.Eachrowofeight h photographicseriesisshowninFig. LD LL LL ≥ Normalized green color value 2D), anditmaybethatthesignal-to-noiseratioforthis

B A 184, h)

h) h) 0 2 4 0 09:00

h periodofrecording( P ≤ LL (72h) LL (48h) LD (24 h) 0.0001).

12:00 h

15:00 h R R

18:00 h 2 2 =0.461, =0.641, 0.388,respectively,

Time (h) Time 21:00 h R F 2 1,289 =0.449, 12 =248,

h ofrecording

00:00 h P F ≤ 1,285 0.0001).

2E,F). =234,

h 03:00 controlling pigmentmigration,asseeninotherinsects. that ambientlightlevelsinteractwiththecircadianmechanisms under thesubsequentconstantlightconditions(24–72 pigments. However, theabsenceofmeasurableeyecolorchanges suggests alight-independentanticipatorymigrationofscreening their originalcolorjustbeforelightsON.Thisprogressivelightening change (i.e.darkening)coincidentwithlightoffset (Fig. lightened progressivelyoverthenext9.5 reached theirdarkestpoint~2.5 during thedark(versuslight)phase(z=4.10, which isevidencedbythesignificantlyloweroverallgreenvalues continuous lightasindicatedinthelegend. Open symbolsindicatethevaluesforsubsequent48 for thefirst24 in theinsetphotograph.Filledcirclesgraphindicatevalues value (±s.e.m., cycle. Thescatterplotdepictstheaveragenormalizedgreencolor indicates thelight(white)anddark(black)phasesoflight:dark scatterplot inFig. which thethreeweretakenandwithscaleonabscissaof Columns ofphotographsarealignedbothwiththetimedayat photographs represents24 seven mantisesthatweretestedwithcomputer-generated visual 4A,Bdepictstheaveragetrackandstrikerates,respectively, for Fig. Tracking andstrikingbehavior

h Photographs takenduringthefirst24 06:00

h The JournalofExperimentalBiology(2014)doi:10.1242/jeb.102947 24

N h, duringwhichthelightswereturnedonandoff. =5) calculatedwithintherectangularareaindicated

light:dark (LD;0–24 conditions. patellifera Fig. phases oftheLDcycleduringfirst24 images indicatesthelight(white)anddark(black) color valueswerecalculated.Theshadedbarabovethe the scatterplotindicateseyeregionfromwhich are nochangesineyecolor. Theinsetphotographon phase (priortolightonset).UnderLL conditionsthere lightens progressivelyoverthelast9.5 the darkphase(indicatedbyarrow).Eyecolor stable inthelightphasebutdarkensatbeginningof experimental period.UnderLDconditions,eyecoloris N depicts theaveragednormalizedgreencolor(±s.e.m., register withtheabscissaofscatterplot(B),which aligned withthetimesindicatedbelow, andarein conditions. Eachcolumnofthreephotographsis 3B. Thebarabovethetoprowofphotographs =5) valuesofthecompoundeyesover

.Photographicanalysisofchanges inH. 3. h, asindicatedtotheleftofrows. compound eyecolorunderdifferentlight (A) Imageswereobtainedinsuccessive

h afterlightsOFF, andthen h) andlight:light(LL;24–72

h, eventuallyreturningto

h showarobustcolor P≤ 0.0001). Theeyes

h ofthedark

h.

3B, arrow), h), implies

h under

h) 3855

The Journal of Experimental Biology 3856 moving againstthegraybackground( (relatively darker)versusthewhitebrighter)disks struck atsignificantlyhigheroverallratesinresponsetoblack mantis tested(Preteetal.,2013a), sensitive, respectively(cf.Fig. indicated thattheireyeswouldbemaximallyandminimally stimuli atthetimesduringdark:lightcyclewhenERGdata maintained underLL conditionsfor24 rates becomeconsistentlyandsignificantlyhigherthanthedaytimerates.(C)Theday-versus-nightdifferencepersists whenmantisesare instrikerates open symbols,respectively).Asthesizeofblackdisksincreasesbeyond5 condition(A,B,filledversus darker (black)versusbrighter(white)stimuliwhenmovingagainstagraybackgroundinboththedayandnightphasesofLD are higherinresponsetorelatively respectively) andlight:light(LL;C)conditions.Asisthecaseforotherspeciesofprayingmantis,overallbehavioralrates Fig. RESEARCH ARTICLE higher duringthenightphase( strike ratestothe7–11 when stimulienlarged beyond5 size increased.However, thedayandnightresponseratesdiverged overall responseratesfollowedalogisticprogressionasstimulus striking (10.79≤ to 11 between thenightanddayresponserateselicitedbywhitedisks. for trackingandstriking,respectively, andtherewerenodifferences none oftheresponseratestowhitestimuliexceeded0.23or0.36 B A Normalized activity Days Increasing thesizeofblack(butnotwhite)disksfrom2 10 0 1

9 8 7 6 5 4 3 2 1 .Tracking andstrikingbehaviorelicitedfromH.patellifera 4. 0 01 deg hadarobustoveralleffect ontheratesofbothtrackingand Fr≤ 23.43, 0.029≥

deg diskswereconsistentlyandsignificantly 24 Track rate 0.2 0.4 0.6 0.8 1.0 0 0 A z N=8

2). Asisthecaseforallspeciesof =3.77, Disk diameter(deg) 2 4

h, andthenre-testedwiththe11

deg suchthatboththetrackand P H. patellifera ≥ 0.00009). Inbothcases,the P

z Time (h) ≤ 6 ≥ 0.002). 48 3.08,

2 2 8 0

10 P ≤ both trackedand

0.002). Infact, 12

Strike rate 0 2 4 6 8 0 by erraticallymovingdisks. B

deg disk.

Disk diameter(deg) 24 2 4 White day White night Black day Black night

deg, theresponseratesduringdayandnightdiverge,night-time

eeae ytomnie vra1 dayperiodunderlight:dark generated bytwomantisesovera10 5A showstworepresentativedouble-plottedactograms Fig. influences ratherthantodifferences inambientlightlevelsperse. experiment weredue(eitherdirectlyorindirectly)tocircadian suggest thatthedifferences inresponserateseentheprevious during thesubjectiveday(Fig. mantis strikeratesduringthesubjectivenightwerehigherthan would resultfromlongerexposuretoconstantlight.Again,the having toaccountforanybetween-animaldifferences inperiodthat each animaltobeexaminedunderfree-runningconditionswithout under constantlight.Thisstandardcircadianprotocolallowsfor and thenre-testedwiththe11 periods, fiveofthemantiseswereexposedtoconstantlightfor24 effects oftheambientlightdifferences duringthetwo testing night seeninthepreviousexperimentwerenotduesimplyto Locomotor behavior 6 8 To confirmthatthedifferences instrikerateduringthedayversus

10 12 48 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.102947 4 Measurements wererecordedunderlight:dark(LD;A,B, Strike rate phases, respectively. open andshadedsectionsindicatethelightdark phase. Inboththeactogramsandhistogram, diminishing andstabilizingfortheremainderofdark of activitylasting60 transition. Thisgradualincreasewasfollowedbyaburst light phase,presumablyinanticipationofthelight–dark activity graduallyincreasesoverthesecondhalfof of themantisentrainstoLDcycles.Locomotor actograms (B)indicatethattheoveralllocomotoractivity normalized activity(±s.e.m.)calculatedfromthose under alight:dark(LD)cycle(A)andtheaverage different lightconditions. Fig. 0 1 2 3 4 5 C

.LocomotorbehaviorofH.patellifera 5. Night

4C; deg diskinthesameprotocolbut Day

min (three20 z N=5 =3.49, Actograms werecollected P =0.0005). Thesedata

min bins)before under

h

The Journal of Experimental Biology and stabilizedfortheremainderofdarkphase. largest overallactivitybouts;theselasted~1 transition. Thetransitiontothedarkphasewasfollowedby suggesting ananticipatorychangeinactivitypriortothelight–dark level increasedgraduallythroughoutthelaterhalfoflightphase, (z≤2.66, RESEARCH ARTICLE Tomioka et al.,1993;PyzaandMeinertzhagen, 1999). pigment chromophore(Kaiser, 1979;KaiserandSteiner-Kaiser, 1983; channel densityorconductance, oroscillationsinavailablevisual photoreceptor membrane, ion(especiallypotassium) may occurinthephototransduction cascade,thepropertiesof Horridge etal.,1981;PyzaandMeinertzhagen, 1997).Otherchanges migration ofscreeningpigment (FleissnerandFleissner, 1978; diameter (Blest,1980;Whiteetal.,Horridge1981) or and Warrant, 2000;Reisenman etal.,2002),changesinrhabdomere eucone dioptricapparatus(Walcott, 1971;Williams, 1980;Nordström ultrastructural changescanincluderetinomotormovementswithin the Reisenman etal.,2002;Heimonen2012).Mechanical or the transductiongainofphotoreceptorcellsthemselves (e.g. respectively, theamountoflightcapturedbyphotopigmentsand/or attributed tomechanicalandphysiologicalmechanismsthatmodulate, ERG. Fluctuationsinthedepolarizationamplitudehave been sustained OFF, orafter hyperpolarization(AHP)componentofthe depolarization. However, asshownhere,fluctuations alsooccurinthe restricted toamplitudechangesinphototransductioninducedreceptor Menzi, 1987).However, inmostcases,thesemeasurementshavebeen a numberofinsects(Tomioka andChiba,1982;Wills etal.,1986; changes incompoundeyeERGamplitudehavebeendemonstrated Circadian fluctuationsinphotoreceptorsensitivitymeasuredas compound eyecolor, andlocomotoractivity. electroretinogram, behavioralresponsestoprey-likevisualstimuli, influences wasseeninthemacroscopiccharacteristicsof physiology andbehaviorof Our resultssuggestthatcircadianclocksaffect severalaspectsofthe greater thanthe6 levels 6 caused simplybyachangeinlightconditionbecausetheactivity light–dark transition.Thispeakinactivitycouldnothavebeen course ofthelightphaseandreachedapeakimmediatelyafter Overall, theaverageactivitylevelincreasedgraduallyover periods ofactivityweresynchronizedwiththelight–darktransition. that themantiseswereentrainedtoLDcycleandtheirpeak eight (Fig. during thedarkphaseofexperiment.Whenaveragedoverall bursts atoraroundthelight–darktransition,andverylittleactivity over thenychthemeron,thesemantisesdisplayedconsistentactivity dark phases,respectively. eight actograms;openandshadedcolumnsindicatethelight average normalizedactivitylevels(±s.e.m., graphical representationofdailylocomotorpatterns.Fig. right halfrepresentsdays2–11. Thisconventioncreatesaclear results inagraphwhichthelefthalfrepresentsdays1–10and 24–48), eachdayisrepeatedatthebeginningofnextrow. This row ofthegraph,andsoon.Hence,beginningwithday2(hours in thefirstrowofgraph;hours24–72areplottedsecond cycle). Inthisstandardplottingconvention,hours0–48areplotted (LD) conditions(grayshadingrepresentsthedarkphaseofLD Circadian rhythmsinthemantisvisualsystem Circadian DISCUSSION The actogramsindicatethatdespiteasparsescatteringofactivity h beforeandafterthelight–darktransitionweresignificantly P≤0.0078). Itisalsonoteworthythattheaverageactivity

5B), thispatternbecameveryclear, suggesting

h beforeandafterthedark–lighttransition H. patellifera . Evidenceofcircadian

h beforetheydecreased N =8) derivedfromall

5B depicts suggest thatthe risetimeandfinalamplitudeof thesustainedOFF durations andintensities(Popkiewicz andPrete,2013).Thesedata proportional toitsmaximum amplitudeoverbothstimulus depolarization andthelatency toitsmaximumisinversely proportional totheamplitude of thelight-inducedphotoreceptor haveshownthatthe amplitude ofthesustainedOFFis cations (Jansonius,1990).Analyses oftheERGinseveralmantis of anelectrogenicpumpextrudingthelight-inducedinflux of its maximum.ThesustainedOFFisunderstoodtobetheproduct the oscillationsinsustainedOFFamplitudeorlatency to oscillations intheERGONcomponents,theydonotaccount for without affecting oscillators that modulatephotoreceptorsensitivity. masks endogenousoscillatorsthatmodulatepigmentmigration phenomenon isthatcontinuous,brightambientlightdampens or control thelatter. Themostparsimoniousexplanationofthis the mechanismsunderpinningformeraredistinctfromthose that under constantlightconditions).Thissuggeststhatfluctuations in oscillates intheabsenceofchangescompoundeyecolor (i.e. or photoreceptors(e.g.Reisenmanetal.,2002). of moreproximalpigmentgranulesinthesecondarycells migration inthedistalprimarypigmentcellsratherthan eye darkeningin basis ofmantiseyeanatomyandwhatisknownaboutotherinsects, this occursinmantiseshavenotbeendocumented.However, onthe Although thisisprobablytrue,theprecisemechanismsbywhich adjusted sensitivityoftheeyetochangingluminancelevels. enlargement ofthe‘pseudopupil’ reflectedpigmentmigration,which night-time darkeningofthemantiseyeandconcomitant et al.,2002;Greiner, 2006).Rossel(Rossel,1979)assumedthatthe an interactionbetweenthesetwofactors(Menzi,1987;Reisenman influenced byendogenouscircadianrhythms,andthereseemstobe directly bychangesinlightintensity. However, itcanalsobe Heimonen, 2008). radially migratingpigmentgranules(ButlerandHorridge,1973; rhabdoms duringtheday, andtherhabdomsbecomesurroundedby cockroaches andmantises,thevacuolesmoveawayfrom accumulation ofvacuolesisalsoseenincockroaches.Inboth surrounded bya‘palisade’ ofvacuoles.Thisnight-time (to 3–4 μmdiameter)atnight,duringwhichtimetheybecame which weresmallduringtheday(1.7–2.1 μmdiameter)andlarger attributed tochangesinthesizeandconditionofdistalrhabdoms 1981). Thechangeinacceptanceanglesasseen to thedaystatewhenheldinconstantdarkness(Horridgeetal., night andin sp. Inbothspeciestheacceptanceanglesapproximatelydoubleat for instance,inthemantises night-time increaseinommatidiaacceptanceanglesasdocumented, changes reportedhere,therearesupportingdatafortwo.Oneisa sister taxontotheMantodea(Heimonenetal.,2012). (Greiner, 2006),includingtheBlatoddea(cockroaches),whichis number ofcrepuscularandnocturnalinsectshaveappositioneyes dichotomy betweeneyetypeandecologycouldbeoverstated;a photon capturerates(Warrant andMcIntyre,1993).However, this smaller lensesthansuperpositioneyesand,consequently, reduced crepuscular ornocturnal)insectsbecausetheeyestendtohave 1979). Thisarrangementisoftenassociatedwithdiurnal(versus abut theproximalendsofcrystallinecones(HorridgeandDuelli, Whereas themechanismsexplainedabovecouldaccount for More important,however, isourfindingthatERGamplitude In anumberofinsects,onsetpigmentmigrationcanbeelicited Of themechanismsthatcouldaccountforeyesensitivity Mantises haveappositioneyesinwhichthedistalretinulacells The JournalofExperimentalBiology(2014)doi:10.1242/jeb.102947 Orthodera H. patellifera the acceptanceanglesspontaneouslyreturn Tenodera australasiae is mostlikelyduetopigment Orthodera and Orthodera 3857 were

The Journal of Experimental Biology oscillations in lobulamovement-sensitive cellsand/orthe 3858 to prey-likevisualstimuliin et al.,2012).Hence,itmightbe thatelevatednight-timeresponses subject tocircadianoscillations (BultandMastebroek,1993;Gaten optic lobeanddescendingmovement sensitiveinterneuronscanbe (Berger, 1985;Gonkaetal.,1999).Ithas alsobeenshownthatboth occurrence ofpredatorystrikes in themantis of thedescendinginterneuronsistemporallycorrelatedwith the stimuli thatelicitorsuppresspredatorystrikingandtheactivity descending interneuronscanbeelicitedorsuppressedbythe same 1996) wasbasedondatashowingthatactivityinboththelobula and ganglia. Theoriginalarticulationofthishypothesis(Preteet al., contralateral ventralnervecordtomotorneuronsinthethoracic dedicated, descendinginterneuronsthatprojectthrough the interneurons residinginthelobula.Inturn,thesecellssynapse on striking beginswiththeactivityofmovement-sensitiveoptic lobe the sensory-motortransformationofvisualinputintopredatory photoreceptor sensitivityperse. behavioral responseratesareprobablynotduetochangesin (Popkiewicz andPrete,2013).Hence,night-timeincreasesin the second-orderinterneurons(LMCs)remainrelativelystable depolarization amplitudefluctuateswidely, responseamplitudesof central neuralcomponents.Thatis,evenwhenphotoreceptor track andstrikeratesareduetocircadianfluctuationsinmore Prete, 2013). and theLMCsargue againstthisinterpretation(Popkiewiczand activity) andthedifferences betweenthegainsofphotoreceptors of circadianoscillationsinthetransientOFF(i.e.putativeLMC Bullaro andPrete,1999;Gonkaetal.,1999).However, theabsence are presynaptictothoracicmotorneurons(Liskeetal.,1989; ultimately inthedescendingmovement-sensitiveinterneuronsthat both theimmediatelypost-synapticinterneurons(LMCs),and changes inphotoreceptorsensitivityarereflectedtheactivityof changes incompoundeyesensitivity. However, thisimpliesthat elevated night-timeresponseratesareattributabletocircadian night, evenunderconstantlightconditions.Itispossiblethatthe the overallratesatwhich are consistentwiththoseresults.Inaddition,however, wefoundthat 12 moving disksathigherratesastheirdiameterincreasesfrom5to than arebrighterstimuli,andthat darker stimuliarestrongerreleasersofbothtrackingandstriking relative brightness.Previousstudieshaveshownthatrelatively responsiveness tovisualstimulithatvariedinbothsizeand In thisstudy, weassessed the differences indayversusnight that functionsundervaryinglightconditions. 2005). Hence,onewouldexpectmantisestohaveavisualsystem Horridge etal.,1981;MatsuraandInoue,1999;Gemeno or locomotoractivity(RobinsonandRobinson,1979;Rossel, many speciesengageincrepuscularornocturnalcourtship,mating capture preyirrespectiveofambientluminancelevels.Furthermore, food deprivedinthefield(Hurd,1999),andmustbepreparedto intermittent appearanceofprey. Consequently, theyaregenerally and-wait orambushpredatorsthatdependontheunpredictable, the daymakesecologicalsenseinthatmany(ifnotmost)aresit- admitted duringdepolarization. is influencedbytheinfluxrateandfinalconcentrationofcations RESEARCH ARTICLE Responses toprey-like visualstimuli Anatomical, behavioralandelectrophysiologicaldatasuggestthat An alternativeexplanationisthattheday–nightdifferences in The factthatthevisualsensitivityofmantisfluctuatesacross deg ofvisualangle(Preteetal.,2013b).Thedatareportedhere H. patellifera H. patellifera Heirodula responded wereelevatedat lineola sp. striketoerratically reflect circadian Mahaffey, 1993;Prete,1999;Preteetal.,2011). fed adietknowntokeepthemhealthybutslightlyhungry(Preteand (Matsura andInoue,1999),inourexperiments,mantiseswere between hungerlevelandlocomotoractivityinthefield explanation maybeplausibleinthatthereisapositivecorrelation associated withvespertinerelocationofforagingsites.This Alternatively, thelight–dark-associatedburstsofactivitycouldbe the peakinlocomotorbehaviorshownhere(Perez,2005). and theonsetofthisreproductivesignalingbehaviorcorrespondsto (and pheromonerelease)hasalsobeendocumentedin release in consistent withthecallingbehaviorsandpresumedpheromone the timinganddurationofactivityburstsdocumentedhereare first isreproductivesignaling(i.e.pheromonerelease).Forinstance, either oftwowell-documentedmantisbehaviorsinthefield.The clustered aroundthelight–darktransitionmaybeassociatedwith circadian controls. (Harker, 1960;Loher, 1972)andhavebeenattributedto transition. Similaranticipatorybehaviorshavebeenshowninother anticipatory increasesinactivityjustpriortothelight–dark mantis locomotorbehaviorissupportedbytheoccurrenceof and Robinson,1979).Thehypothesisthatcircadianclocksmodulate mantis behavior(e.g.pheromonerelease;Edmunds,1975;Robinson behavioral patternshavebeendocumentedincertainaspectsof (Saunders, 2002)anditisinterestingthatbothofthesecomponent (dawn) andvespertine(dusk)components,arecommonininsects crepuscular activitypatterns,whichcanincludebothmatutinal synchronized tothelight–darktransition.Circadian-clock-controlled conditions displayedstrongvespertinepatternsthatwere overt rhythmsinmantisactivity(Liske,1999). However, untilnow, quantitativestudieshavefailedtomeasureany 1964) andstickinsects(e.g.Godden,1973;Saunders,2002). crickets (e.g.NowosielskiandPatton,1963),beetlesLohmann, recordable insectmodels,includingcockroaches(e.g.Brady, 1967), Locomotor activityhasbeeninvestigatedinseveraleasily compound eyesensitivityperse. descending interneuronsonwhichtheysynapse,ratherthanin (Audinet Serville) thatwerelaboratoryrearedaccording topreviously All experimentsweredoneusing adult,female mantis physiologyandbehavior. first steptowarduncoveringthe mechanismsthatmodulatepraying remains tobediscovered.However, these resultsareanintriguing to beindependentandself-synchronizingorcentrallycontrolled levels inthisspeciesofmantis.Whethertheputativeclocksturn out clocks operatingatthecellular, cellular systems andorganismal data suggestthattherearecomplexinteractionsbetweencircadian operate effectively beyondthe daylighthours.Taken together, our synchrony wouldbetoextendthetimesduringwhichmantis can dark phasesofthelight:darkcycle.A byproductofthisfunctional parameters thatwemeasuredpeakedearlyinthedarkorsubjective praying mantis.Interestingly, whenplacedinregister, allofthe perspective ontheeffects of circadianrhythmsinonespeciesof Here, wehaveusedabroadexperimentalapproachtogain some Circadian rhythms of gross locomotorbehavior gross rhythmsof Circadian Mantises MATERIALS ANDMETHODS andbehavior mantisphysiology of organization Circadian Ultimately, therhythmiclocomotorpatternsthatwefoundtobe In thisstudy, rhythmiclocomotor activitymeasuredunderLD Tarachodes afezelii The JournalofExperimentalBiology(2014)doi:10.1242/jeb.102947 (Edmunds, 1975).Callingbehavior Hierodula patellifera H. patellifera

The Journal of Experimental Biology positioned 10 brightness=8.92 (http://www.circadian.org/periodogram.html). between hours19and27withα square periodogramcalculatorsettoacorresponding15 15 maximum valueforagivenparameter. ERGswererecordedevery expressing themagnitudeofindividualvaluesasproportions maximum (PopkiewiczandPrete,2013). measured betweentherecoveryoftransientOFFandsustained maximum; and,themaximumderivativeofsustainedOFF(arrowatf) maximum voltageofthesustainedOFF(e),andlatencytothat its maximumandminimumvoltages,thelatencytothatminimum; (arrow aboveb);theamplitudeoftransientOFF(d)measuredbetween and thelatenciestothatmaximum;meanderivativeofsustainedON the maximumamplitude(i.e.largest absolutevalue)ofthetransientON source. custom built,light-tightchamber(41×41×38 the distalposteriorlateralcompoundeye.Thearmaturewasplacedina was insertedintotheheadcapsule,andactiveelectrode with theterminal0.50 RESEARCH ARTICLE Each mantiswasbrieflyanesthetizedwithCO Eye colorwasassessedunderbothlight:darkandconstantlightconditions. Each mantiswasanesthetizedbybriefexposuretoCO guidelines. operated inaccordancewithallapplicableethicalandanimalcare experimental animalsweretreatedwiththeappropriateconcerns,andwe an averageofonelivecricket( and 25°Cduringthedaynightperiods,respectively. Mantiseswerefed h.Temperatures weremaintainedat30 light:dark cyclebeginningat08:00 maintained inindividualcontainerswithinanenclosureundera12 used inindividualexperimentsareindicatedtheResults.Mantiseswere described protocols(PreteandMahaffey, 1993).Thenumbersofanimals compound eyesuch thatitwascenteredatthe intersectionoftwo (B) valueswithin a16×17pixelrectanglepositioned overtheright Bethesda, MD,USA)bycalculating theaveragered(R),green(G),andblue photographs weretakenunderconstant light(45 light:dark cycleofthemantishome cage.Duringthesubsequent48 taken under12 continuous hours.Forthefirst24 and thenturnedoff theLED. Thiswasrepeatedevery30 turned onthemicroscopesinglewhiteLED(491 time onanexternalcomputerscreen.Duringtheexperiment,program with MacroScheduler(MJT NetLTD, London,UK),andmonitoredinreal GA, USA). USB microscopecamerafromadistanceof20 as describedabove.Inthebox,mantisfacedadigitalbluemodel QX5 color analysescouldbenormalized.Thearmaturestoodinalight-tight box movements andprovidedawhitebackgroundagainstwhichsubsequent a holeinpieceofwhitecardstock.Thecardstockbothprevented head wrapped mantiswasaffixed to anarmaturewithitsheadprotrudingthrough abdomen remainedunencumberedsoasnottointerferewithrespiration. The against itsprothoraxandthewaswrappedwithplasticfilm.The analyses weredoneinLabScribe2v2.348. LabScribe2 v2.348software(iWorx Systems,Dover, NH,USA).Offline USA), andstoredtodiskviaaniWorx model214DataRecorderand amplified (Differential AmplifierModel3000,A-MSystems,Sequim,WA, indifferent electrodeswereTeflon armature, anditsheadwasstabilizedwithwax.Bothrecording Photographic analysis of compoundeye color of analysis Photographic Electroretinogram All ERGdatawerenormalizedusingthestandardconventionof Optical stimulationwasprovidedbya5 Eye colorwasmeasuredwithImageJ software(NationalInstituteHealth, After thechamberwasclosed,photographicprocedureautomated The measurementsusedtoanalyzetheERGsincluded(referFig. min over72consecutivehours.PeriodanalysesweredoneusingaChi- mm infrontandpointedatthecenterofimplantedeye;

h:12 Wm h light:dark(45 − 2

mm strippedofinsulation.Theindifferent electrode (Popkiewicz andPrete,2013).Recordingswere Acheta domesticus ®

-insulated 0.051 h oftheexperiment,photographs were =0.05 (SokoloveandBushell,1978)

lx:0 lx) conditionssynchronizedtothe

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h, h order separatedbyinter-trail intervals faded backtodark.Duringeachtest,mantisessawall10stimuliinrandom 500 darkened screenbrightenedprogressivelyto105 screen illuminationonadaptationstate,atthebeginningofeachtrial, allowed atleast10mintoacclimate.To minimizetheeffects ofcomputer testing, eachmantiswasplacedinfrontofanunlitcomputerscreenand the lightordarkphasefirst)wasrandomizedacrossmantises.Priorto order oftestingwithina12 mantises reflexivelyheldahollowStyrofoam distance of25 semi-cylindrical arenafacingaDellflatscreencomputermonitorfrom healthy andresponsive. periods, mantiseswerefedtwolivecricketsperweekwhichkeptthemboth allowed morethan24 tether wasaffixed tothedorsalpterothoraxwithstickywax.Eachwas briefly withCO described indetail(e.g.Preteetal.,2012).Eachmantiswasanesthetized All mantisesweretestedaccordingtoestablishedprotocolspreviously diagnostic-dependent measure. green valuesfluctuatedwasthegreatestand,hence,usedas between animalsduringtheexperiment.However, therangeoverwhich three ofthevaluesdisplayedsamepatternchangesbothwithinand proportion oftheminimumvalueformantisduringexperiment.All photograph werenormalizedwithinanimalsbyexpressingeachasthe medial-most tothelateral-mostedgeofcompoundeye. of thecompoundeyeandheadcapsule,otherdrawnfrom hypothetical lines,onedrawnfromthedorsal-toventral-mostjuncture IL, USA).Thetreadmillwasafoam cylinder(6.35 conjunction withClockLabdatacollection software(Actimetrics,Wilmette, Locomotor activitywasassessedusingamodifiedtreadmillapparatus in around visualfieldcenterinan‘erratic’ pathfor10 respectively) ranginginsizefrom2to11 deg.Inturn,eachstimulusmoved series offiveblackandwhitedisks(0or185 of visualangle(deg)atthe25 computer monitor[1024×768pixels;pixelsize=0.75×0.75degrees expectancy (Prete,1999). (e.g. prothoraxmovement,stepping,grooming)nordidtetheringaffect life itself norbeingsuspendedinthearenainterferedwithanynormalbehaviors than themantises)withtheirmeso-andmetathoraciclegs.Neithertether Individuals weretestedatrandomtimeswithinthese3 minimum amplitudes(21:00 the timesinlight:darkcycleatwhichERGsreachedtheirmaximumand randomly selecteddaysoveratotalperiodof36days.Testing wasdoneat a gray(105 rates (±1s.e.m.). Overall responserateswerecalculatedastheaveragesofindividual of strikesdividedbythenumbertrialsperstimulusforeachmantis. performed duringasingletrial.Strikerateswerecalculatedasthenumber trial oritdidnot(max.trackrate=1.0).However, multiplestrikescouldbe considered abinomialevent;themantiseithertrackedstimulusduring a movement oftheraptorialforelegs(PreteandCleal,1996).Tracking was the latterwasdefinedascharacteristic,rapid,forwarddirectedgrasping defined asanyheadorprothoracicmovementsthatfollowedthestimulus; magnets topassa MederProximitySensor(MK11-1A66B-500W; Meder mantis madestepping movements,thecylinderrotated causingtheblock positioned suchthatitstoodinanatural postureonthecylinder. Whenthe cylinder. Duringtesting,atetheredmantis washeldbyanarmatureand (9.525×3.175×1.5875 long) thatrotatedonanaluminium axel.Fourneodymiumblockmagnets Tracking andstrikingbehavior Locomotor behavior During tests,mantiseswereheldbytheirtethersinawhite,11-cm-high To accountforbetween-animalvariability, theRGBvaluesineach Computer-generated visualstimuliwerepresentedonaDellflatscreen Two behaviorswererecorded:trackingandstriking.Theformer was ms, astimulusmovedthroughthespecifiedpathandthenscreen lx) background.Mantisesweretestedtwiceperdayon4–6 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.102947 mm inanotherwisedimlylitroom(62 2 after whichitswingswereremovedandasmallwood mm) wereequallyspacedaround oneendofthe

h recoverytimepriortotesting.Duringtesting

h period(i.e.whetheramantiswastestedduring

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lx (subjectivegray)over h–12:00

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The Journal of Experimental Biology (converted to two-sample comparisonsweredonewiththeWilcoxon paired-sampleTest 3860 Research GranttoF.R.P. andA.E.S. US DepartmentofEducationTitle IIIHSI-STEM(P031C110157) Summer initiative oftheUSDepartmentEducation,CCRAA HSIP031C080027)anda Institute ofFoodandAgriculture,theStudentCenterforScienceEngagement (an through EnvironmentalandAgriculturalResearch)fromtheUSDA National Competitive Grantno.2010-38422-21240(CREAR:CollaborationandRetention This workwassupportedinpartbyanAgricultureandFoodResearchInitiative manuscript preparation. participated substantivelyintheon-goingprocessesofdatainterpretationand the experiments,allaspectsofdatacollectionandtabulation.Allauthors design andcontributedequallytomanagementoftheanimalcolony, executionof A.F.U. andW.B. participatedsubstantively inexperimentaldevelopmentand analyses oftheexperiments,andtoallaspectsmanuscriptpreparation.E.S.M., A.E.S. andF.R.P. contributedequallytotheoveralldevelopment,designand The authorsdeclarenocompetingfinancialinterests. manuscript. referees fortheirthoughtfulcommentsandsuggestions,allofwhichimprovedthe sincerely appreciatethetimeandefforts ofthejournaleditorandanonymous Wellems ofPhenomeTechnologies Inc.forhistechnicalsupportandadvice.We Prete, GregJessicaDominguezandRobertTheis.We alsothankMichael collegial andenthusiastichelpinvariousaspectsofthisongoingproject:Ben We acknowledgethesupport oftheothermembersourresearchteamfortheir www.excelcurvefitting.com) orinDataDesk the appropriateaddedmodules(e.g.www.advancedanalyticsllc.com; exception ofperiodanalysisasdescribedabove)weredoneinExcelwith ( experimental questions;multiplecomparisonswereBonferronicorrected hoc repeated-measures datawereanalyzedwithanANOVA. were analyzedusingtheFriedmanTest (Friedman,1940).Parametric All datawerecheckedfornormalcy. Non-parametricrepeated-measuresdata cabinet illuminatedwithgreenLEDs(peak Clocklab system. Electronics, West Wareham, MA,USA).Eachpasswasrecordedbythe RESEARCH ARTICLE amn,F n ajlzr,B. Hadjilazaro, and F. Baumann, J.G. Audinet Serville, ea,P,Cmoosi .adGeutwc,J.M. Giebultowicz, and B. Cymborowski, P., Bebas, ls,A.D. Blest, NY, USA). References Funding Author contributions Competing interests Acknowledgements Statistics illumination withnight-visiongoggles. Feeding duringthedarkportionofcyclewasdoneunderinfraredlight were hand-fedtwoadultcricketsperweekatrandomtimesduringtheday. synchronized totheirhomecagecycle.Duringtheexperiments,mantises 14 Technologies, Chicago,IL,USA).Locomotoractivitywasmeasuredfor (±1 s.e.m.)within20 the maximumaveragebinactivitylevelwithinmantises.Overallaverages 20 activity plotswereconstructedbyaveragingindividualwithin egr F. A. Berger, α Vision Res. studies ofbreakdown processesandtheirimplications.In Criquets, Sauterelles) sperm releaseinmalesofthecottonleafworm, Universität Düsseldorf,Deutschland. den OptischenGanglienderGottesanbeterin MantisReligiosa vitro studies. =0.05; individualprobabilitiesarereportedinthetext).Statistics(with The treadmillstoodina97.79×53.975×46.99 Actograms wereproducedusingClocklabsoftware.Normalized24 min binsoverdays2–14.Thesedatawerenormalizedasproportionsof days (N tests wereappliedconservativelyandonlytoanswerspecific =8) ina12 (1980). Photoreceptor membraneturnoverinarthropods: comparative 11 (1985). J. InsectPhysiol. z , 1198. scores; non-parametricdata)or Morphologie undPhysiologieEinigerVisueller Interneuronenin . Paris:Roret.

(1838). min binswerecalculatedacrossmantises.

h:12 Histoire NaturelledesInsectes.Orthoptères(Grillons, 47, 859-866. (1971). Afterpotentialsinretinulacellsof thedrone. h light:darkcycle(76 Spodoptera littoralis t ® -tests (parametricdata).

cm custom-built,light-tight (Data Description,Ithaca, (2001). Circadianrhythmof λ 55nm;Phenome =515 The EffectsofConstant

Post hoc lx:0 lx) thatwas : invivoand . Dissertation, and other Post

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