The Swarming Behavior of the Dioithona oculata: In Situ and Laboratory Studies Author(s): Edward J. Buskey, Jay O. Peterson, Julie W. Ambler Source: Limnology and Oceanography, Vol. 41, No. 3 (May, 1996), pp. 513-521 Published by: American Society of Limnology and Oceanography Stable URL: http://www.jstor.org/stable/2838586 Accessed: 25/10/2010 20:11

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http://www.jstor.org Limnol. Oceanogr.,41(3), 1996, 513-521 ? 1996, by the American Society of Limnologyand Oceanography,Inc. The swarmingbehavior of the copepod Dioithona oculata: In situand laboratorystudies

EdwardJ. Buskeyand Jay0. Peterson Marine Science Institute,750 Channelview Dr., Universityof Texas at Austin,Port Aransas 78373

JulieW. Ambler Department of Biology, MillersvilleUniversity, Millersville, Pennsylvania 17551

Abstract The behaviorof the swarm-formingcopepod Dioithonaoculata was studiedboth in situ and in the laboratoryusing a video-computersystem for motion analysis. In nature,swarms form in lightshafts between theprop roots of redmangroves. Swarms maintain their position within these light shafts despite currents ofup to 2 cm s- 1.In thelaboratory, swimming speeds and turningrates of swarming in stillwater werelower than those observed in thefield. Copepods studied in a flowthroughchamber in thelaboratory had swimmingbehaviors similar to thoseobserved in nature;the stimulation from water movement caused increasesin bothswimming speed and rateof change of direction. Increased current speeds also causedthe swarmsto becomemore tightly packed within the center of a verticallight shaft. Nonswarming copepods wereunable to maintaintheir position in a currentin darkness.In laboratoryexperiments, the presence of activelyfeeding planktivorous fish caused swarmsto temporarilydisperse due to escape responsesof the copepods.However, planktivorous fish were rarely observed feeding on swarmsin nature,perhaps due to thepresence of predatory fish hiding among the prop roots.

Copepods have been frequentlyreported to formdense swarmin theabsence of active swarming behavior (Oku- aggregations,called swarms,in a wide range of habitats, bo 1980). includinglakes (Byron et al. 1983), temperateand sub- Numerousdetailed studies have focusedon theswim- tropical marine bays (Ueda et al. 1983), coral-reefenvi- mingbehavior of captivemarine and freshwatercope- ronments(Emery 1968), and near mangrove cays (Am- pods underlaboratory conditions (e.g. Strickler1975; bler et al. 1991). The cyclopoid copepod Dioithona ocu- Wonget al. 1986; Tiselius 1992), but fewstudies have lata is a swarm-formingcopepod commonlyfound near beendone on theswimming behavior of copepods in their coral reefsand mangrovecays (Hamner and Carlton 1979; naturalenvironment (Schulze et al. 1992).The lackof in Ambleret al. 1991). Swarms ofD. oculata near mangrove situstudies of copepodbehavior is partlybecause cope- cays typicallyform between prop roots in shaftsof sun- podsusually are found at lowdensities in nature,so view- lightthat penetrate the mangrovecanopy. These swarms ingthem on a spatialscale appropriate for detailed studies form at dawn and disperse at dusk and are composed of theirswimming behavior (field of view of a fewmil- primarilyof adults and late-stagecopepodites (Ambleret limeters)is difficult.In addition,copepods usually exist al. 1991). The suggestedadaptive advantages of swarm in mixedspecies assemblages in nature,so preciseiden- formationin planktoniccopepods includeprotection from tificationof speciesfrom videotape records may be dif- predators, enhanced opportunitiesfor mating, and re- ficultwhen images are small enoughto allow extended strictionof dispersal by currents(Hamner and Carlton swimmingbouts to be observed.The copepod swarms 1979; Folt 1987). The formationand maintenanceof these thatform between the mangrove prop roots in Belizeare swarms must include a behavioral component because ideal forstudying copepod behavior in situ;high-density swarms are composed of a single of copepod in copepodswarms of a knownsingle species form in pre- an environmentwhere numerous species are found and dictablelocations and remainin these locationslong because turbulentdiffusion would lead to dispersalof the enoughto allow filmingof theirbehavior. In addition, this swarmingbehavior makes it easy to capturelarge numbersof individualsof the same speciesfor detailed laboratorystudy, and theseswarms can be re-createdeas- Acknowledgments ilyin thelaboratory. This studywas fundedby a grantfrom the National Science Mostlaboratory observations of copepod behavior are Foundation(OCE 92-18516). madein stillwater, even though such conditions are rarely KeithSchmidt and ChrisCollumb provided assistance with observedin nature.Little is knownabout the behavioral data analysis.We thankKlaus Ruetzlerfor allowing us to use thefacilities at CarrieBow Cay and FrankFerrari for assisting responsesof zooplankton to watercurrents, although sev- witharrangements. eral recentstudies have investigatedthe effectsof tur- Universityof Texas Marine ScienceInstitute contribution bulence on copepod feedingand swimmingbehavior 943 andCaribbean Coral Reef Ecosystem Program contribution (Costelloet al. 1990; Saiz 1994; Ki0rboeand Saiz 1995). 463. In situobservations of copepod swarms during our study 513 514 Buskey et al. revealedthat zooplankton experience both directional Experimentsrun during the day werecarried out be- currentsand turbulenceeven when surfaceconditions neaththe laboratory building in a coveredarea thatre- appearcompletely still, and these water movements clear- ceived no directsunlight. Nighttime experiments and lyaffect their behavior. Most previous studies of swarm- daytimelight-intensity studies were carried out in a dark- formingcopepods were field studies describing the dis- enedstorage room that excluded stray light. A blackfabric tribution,densities, and age structuresof swarms formed enclosurefor the experimental containers further exclud- in thefield (e.g. Emery 1968; Hamnerand Carlton1979; ed straylight. Swarming behavior was inducedin the Ueda et al. 1983). In thisstudy, we made detailedmea- laboratorywith a lightshaft produced by a fiber-optic surementsof swimmingbehavior of swarmingcopepods illuminator(Cole Parmer,150-W quartz-halogen lamp) in situ,and, in laboratoryexperiments, we examinedthe witha 5-mm-diameterlight pipe equipped with a focusing effectsof lightintensity, swarm density, water currents, lens.The fiber-opticlight pipe produceda verticalcone- and visual predatorson the swarmingbehavior of D. shaped shaftof light3 cm in diameterat the water's oculata. surfaceand 6 cm in diameteron thebottom to simulate shaftsof naturalsunlight that penetrate the mangrove canopyin thefield. Swimming behaviors of copepods in Materials and methods laboratoryexperiments were videotaped in the vertical planewith the same system used for in situstudies. Image Our studieswere carried out at theNational Museum contrastof the copepodsunder low lightwas enhanced of NaturalHistory's field station at CarrieBow Cay off withillumination produced by a ringof diodesemitting thecoast of Belize. Copepod swarms were collected near infraredlight (peak wavelength, 890 nm)arranged to pro- TwinCays, a mangrove-coveredisland 2 kmnorthwest duce dark-fieldillumination. These long wavelengths of CarrieBow Cay. Copepod swarmswere filmed in situ probablywere not perceivedby the copepods (Steams alongthe Lair Channelof Twin Cays in July1993 and and Forward1984; Buskeyet al. 1989). inTwin Bays in January 1994 and May 1994.The swarms The effectof light intensity on swarmingbehavior was werein shallowwater (< 1 m) betweenprop roots in shafts examinedbetween 1400 and 1600hours in a 20 x 20 x 20- of sunlightthat penetrated the canopyof the red man- cm clear acrylicaquarium filled with seawater filtered grove(). througha 20-Am-meshsieve. Light intensities of between The swarmswere video recordedin situwith a Cohu 10 and 1,280 Amolphotons m-2 s-' wereproduced by 3315 monochromeCCD video cameraequipped with a adjustingthe rheostat on thefiber-optic illuminator and macrolens (Micro-Nikkor55 mm f2.8)and placedin a by.using neutral density filters. Light intensity was mea- waterproofhousing (Video Vault). The cameraand hous- suredwith a LiCormodel 158A photometer with a quan- ingwere mounted on a plastichorizontal adjustment sled tumprobe. Groups of 200 copepodswere added to the attachedto an aluminumtripod. Images were recorded aquariumat thebeginning of each experiment,and they on a SonyFX-7 10 camcorderintegrated into a field-por- quicklyformed a swarmwithin the verticallight shaft. table video system(Furhman DiversifiedFieldcam Copepodswere allowed to adjustto each lightintensity WCMS) thatremained in a smallboat anchorednearby fora periodof 30 minbefore they were videotaped. Swim- and was connectedto thecamera via a waterproofcable. mingbehavior in thecenter of the vertical light shaft was Swarmswere located by snorkelingalong the edge of the thenvideotaped for 10 min. A new groupof copepods mangrovesand investigatingareas that had swarmsand was used in each experiment. wereopen enoughto allow placementof thevideo gear. The effectof copepod density on theswarming behavior Whenwe locateda suitableswarm, we placedthe tripod of D. oculata was examinedby varyingthe numberof on thechannel bottom and the camerawas adjustedto copepodsavailable to forma swarmand measuringden- view the centerof the swarm.With the macrolens, an sityand swimmingbehavior in thecenter of the swarm. area of - 4 cm2(range, 3.3-4.7 cm2)was viewedin the Experimentswere carried out between1400 and 1600 verticalplane at a distancefrom the camerahousing of hoursin a 20 x 20 x 20-cmclear acrylic aquarium. A fiber- 20 cm,allowing us to viewthe swarm without the cam- optic lightpipe thatproduced a 50 ,umolphotons m-2 eradisturbing it. After we recordedeach swarm, we filmed s-I shaftof lightserved as a swarmmarker. Copepods a metricruler underwater to calibratethe spatial scale. wereadded to thechamber and allowedto adapt for30 For laboratorystudies, we collectedD. oculatain the min; theirswimming behavior was thenvideotaped for TwinBays region of Twin Cays by enclosinga swarmin 5 min. a clearplastic bag. This gentlecapture technique yielded Studiesof D. oculata's abilityto maintaina swarm largenumbers of copepodsin excellentcondition. Co- withina watercurrent were carried out in a flowthrough pepodsfrom several swarms were placed in a plasticcool- chambermade ofclear acrylic plastic. Water entered the er filledwith seawater for the boat tripback to Carrie chamberthrough a 1-cm-diameterTygon tube, passed Bow Cay. All experimentswere run within 24 h of col- througha 2.5-cm-thicklayer of 4-mm-diameterglass lectingthe copepods. Examination under a stereomicro- beads held in place by 333-,um-meshNitex screen, and scoperevealed that all thecopepods were D. oculataand thenpassed throughthe 10x 10x 15-cmviewing cham- thatthe swarmswere composed mainly of adults,with ber,which, when filled to a heightof 10 cm,contained a smallnumbers of late copepoditestages. volumeof 1 liter.The waterpassed through another bed Copepodswarming behavior 515

ofglass beads before draining out of the tank. The purpose trueswimming speeds were calculated as follows.Each of the beds of glass beads was to evenlydistribute the segmentof a copepod'sswimming path was treatedas a flowof water throughout the tank. The flowthroughtank vectordefined by the 'sorientation with respect was used in two modes:a single-passmode and a recir- to the current(00 in the same directionas the current, culatingmode. During initialexperiments in January 1800 movingopposite to thecurrent) and its swimming 1994, a continuousflow of waterwas providedto the speedmeasured from the fixed reference point. The cur- tank,requiring inflow and outflowrates to be exactly rentspeed vectorwas added to each pathsegment, and balancedto maintainwater column height in thecham- themagnitude of the resulting vector was used to estimate ber.In May 1994,a submersiblewater pump was placed thetrue swimming speed for the copepod in themoving in a plasticbucket and used to recirculatewater through bodyof water, referred to as thecurrent corrected speed. the chamber.Flow ratesin thechamber were regulated The densityof copepods within the field of view of the by restrictingflow to thetube filling the chamber. Flow videocamera was calculated with Bioscan Optimas image rateswere estimated by measuringthe speed of neutral- analysissoftware. A singlevideo framewas digitizedat densityinert particles flowing through the observation 15- or 30-s intervalsfrom videotaped records, and co- chamberby meansof theExpertvision motion analysis pepod imageswere quantifiedbased on theirsize and systemdescribed below. Measurements were made at cur- imagebrightness. Images of copepodsoutside the depth rentspeeds ranging from 0 to 20 mm s-I between1400 of field(- 1 cm) wereout of focus,and theirimages fell and 1600 hoursfor copepods swarming in a lightshaft outsidethe luminance or size threshold set for quantifying and between2000 and 2200 hoursfor nonswarming co- copepodimages. We analyzeda minimumof 20 frames pepodsin completedarkness. foreach densitydetermination. The effectof fishpredation on D. oculataswarms was examinedby forming a swarm on oneside of a 36 x 18x 24- cm Plexiglasaquarium in whichthree small sergeant ma- Results jors (Abudefdufsaxatilus,-2 cm long)were restrained in a clear plastictube (8-cm diam) for 1 h beforethe ex- We filmed22 swarmsin situ.By observingthe record- perimentbegan. The D. oculataswarm was videotaped ings of swarmsthrough the macrolens, we recognized for5 minbefore releasing the fish; the clear plastic tube thatthese swarms often kept themselves in thesame lo- was thenraised to releasethe fish. The swarmwas then cationdespite persistent tidal currents.These tidalcur- videotapedfor 10 min in the presenceof the fish.This rentsranged from indiscernible to speedsas highas 15 experimentwas repeated10 times,each timewith a new mm s-I (Table 1). For swarmsexperiencing these cur- swarmof copepodsand a differentgroup of fish. rents,the orientation of copepodsin theswarm was not Swimmingbehavior of D. oculatawas quantifiedat the random.Most of thetime, copepods were oriented into Marine Science Institutein Port Aransaswith an Ex- thecurrent, and theirdominant swimming motions were pertvisionCell-Trak motion analysis system. Videotaped directedinto the current;rest periods between move- experimentswere digitized with a video-to-digitalpro- mentsallowed copepods to be carriedalong with the cur- cessor,and outlinesof thecopepods were sent to a per- rent.Even whenwe did not observedirected currents, sonal computerat a rateof 15 framess-', exceptwhere therewas usuallynoticeable water turbulence caused by noted.The digitizedimages were processed to produce surfacewaves or otherunknown sources. These move- pathsthat followed the motion of the copepods over time. mentscaused the copepods to continuallyadjust their These computer-generatedswimming paths are two-di- behaviorto preventthe swarmfrom being dispersed. mensionalrepresentations of three-dimensionalmove- Swarmsdisplaced by sudden, unpredictable water move- ments. mentsquickly reformed in thelight shaft. We minimizedthe depth of fieldof thevideo camera Fromthe in situvideo records,we determinedswarm lens whilerecording behavior to reducethe numberof densityand quantifiedthe swimmingbehavior of the pathsof organisms recorded moving toward or away from copepods.The 1-cmdepth of fieldfor the macro lens at the camera,but our estimatesof swimmingspeed still f2.8 gave us a viewingvolume of -4 cm-3, a mean underestimatetrue swimmingspeeds in threedimen- density(?1 SD) of 34.5?23.8 copepods cm-3, and a sions.Only paths exceeding 15 frames(1-s duration) were rangeof 9-92 copepodscm-3 (Table 1). These density used in analysis,and pathsfor a singlecopepod rarely estimatesare based on our attemptsto filmbehavior in remainedwithin the field of view for> 5 s. Fromthese thecenter of the swarm; the swarms usually drifted slight- records,behavioral parameters, including swimming speed ly duringfilming and therewas no way to confirmthat (mm s-1), rate of change of direction(deg s-1), and net- we werealways viewing the center. We observedlower to-grossdisplacement ratios of the paths, were calculated densitiesof copepodsnear the edges of the swarm. (see Buskey1984). Net-to-grossdisplacement ratio is a Mean swimmingspeeds of copepods in situranged from ratioof the linear distance between the starting and ending 5.18 to 6.85 mm s-I, witha grandmean value (? 1 SD) pointsof a path(net displacement) and thetotal distance of6.08 ? 0.52 forswarms filmed in theabsence of currents coveredby thepath (gross displacement). (Table 1). The mean rateof changeof direction(RCD) Forboth laboratory and in situstudies involving water forcopepod swarms filmed in thefield ranged from 215.9 flowingpast the fixed reference point of the video camera, to 459.1 deg s-I witha grandmean of 367.9?6 1.0. In 516 Buskeyet al.

Table 1. In situswimming behavior of Dioithonaoculata. 10 Eachswarm was videotaped for at least15 min,and a minimum 0 of 10,000measurements ofeach behavioral parameter was made foreach swarm. Density estimates are means based on 20 frames E 8- at 30-sintervals. Speed (mms-') RCDt Density Location* Current Copepods (degs-') (ind. ml-') EU) cn P Jun-Jul93 n4 LC 10.2 11.26: 215.9 79.8 .E 2 0 LC none 5.98 347.1 39.3 05~~ LC 9.5 10.71t 315.6 91.7 ._ Jan94 TB none 6.31 300.2 46.2 450 C TB none 5.32 389.7 64.5 TB 13.8 15.1lt 379.0 21.9 01%400 @0 TB 13.8 15.84: 374.3 17.0 o 350 * TB 5.3 7.30t 407.4 20.3 TB none 5.86 385.5 39.1 .1300300 8 TB 15.2 17.33t 316.8 9.1 O 250 TB none 6.49 417.5 24.7 0 TB none 5.18 244.4 20.8 200- May 94 150* TB none 6.83 321.4 22.3 100- TB none 6.85 358.8 9.8 I - - I -I - I LC none 5.87 429.7 32.4 0 10 20 30 40 50 60 70 80 90 100 TB none 6.51 424.2 9.1 Copepod density(mrl1) 30.1 TB none 5.79 459.1 behaviorof Dioithona oculata as a func- 393.7 81.1 Fig. 1. Swimming TB none 6.16 of densitymeasured in thecenter of theswarm. 12.17: 455.1 39.9 tion copepod TB 11.3 Laboratoryexperiments performed in stillwater during the day TB none 5.36 412.7 30.5 copepodsswarming in a shaftof light-O; swarms recorded 387.3 13.8 with TB none 6.35 in situin the absenceof sustainedcurrents-*. Mean rateof 6.38 360.1 15.5 TB none changeof direction-RCD. * LairChannel on TwinCays-LC; TwinBays of Twin Cays- TB. t Rate ofchange of direction. swimmingbehavior of swarmingcopepods adapted to t Swimmingspeed estimate corrected for water current move- intensities. analysisrevealed no signif- ments. these Regression icantrelationship between light intensity and swimming speedor turning behavior measured as RCD forcopepods exposedto a rangeof intensitiesfrom 10 to 1,280,tmol somecases, we observedcurrents that moved parallel to photonsm-2 s-I in thelaboratory (Fig. 2). Lightintensity theshoreline and perpendicularto theview of the video measuredin copepodswarms in situranged from 50 to camera.Current speeds from 5.3 to 15.2 mm s-' were 660 Amolphotons m-2 s-' (Ambleret al. 1991). calculatedbased on speedsof flocculentdetrital matter D. oculata exhibiteda remarkableability to maintain driftingpast the camera. Current-correctedswimming swarmsin watermoving at speedsof up to 2 cm s- 1.For speedsranged from 7.30 to 17.33 mm s-' (Table 1) in copepodsswarming in a shaftof lightin laboratoryex- situ. perimentsduring the day, current-correctedswimming In daytimelaboratory experiments, variations in the speedincreased with increasing current speed in labora- densityof copepodsin thecenter of the swarm had little toryflowthrough experiments (Fig. 3). RCD also in- effecton theswimming behavior of individual copepods. creasedwith current speed in daytimeswarms. As current Regressionanalysis revealed no significantrelationship speed increased,copepods swam in shorter,more fre- betweencopepod densityin laboratory-formedswarms quentbouts to remainin the lightshaft and frequently and swimmingspeed or rateof changeof direction(Fig. changeddirection. As currentspeed increased in theday- 1). Similarly,no significantrelationships were found be- timelaboratory studies, copepod densities in thecenter tweencopepod density and swimmingspeed or RCD in ofthe swarm also becamehigher (Fig. 4), indicatingthat naturalswarms, but swimmingspeeds and turningrates theswarm was becomingmore tightly packed. weregenerally greater for swarms recorded in situthan For nonswarmingcopepods in the dark, swimming forthose recorded in laboratoryexperiments (Fig. 1). speeds also increasedwith current speed in laboratory The intensityof the lightshaft used as a markerfor flowthroughexperiments (Fig. 3), butcopepods generally swarmformation also seemedto have no effecton the wereunable to orientinto the current and maintaintheir Copepodswarming behavior 517

30-

U) ~~~~~~~0 0) 25 - Oday y-0.82x+ 3.29 r2- 0.96 0 0 E E 3 *night y 3 0.79x + 1.85 r2- 0.96 0 E ~~0 0 E20 0 0IV 15- O- u) CL c 1 E

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150-

100- I l 0 250 500 750 1000 1250 1500 o s 10 15 20 LightIntensity (AM photons mr2s&) CurrentSpeed (mm s.1) Fig. 2. Swimmingbehavior of Dioithona oculata in the lab- Fig. 3. Effectsof current speed on Dioithonaoculata swim- oratoryas a functionof light intensity (,umol photons m-2 S-1) mingbehavior in daytimelaboratory experiments for copepods forcopepods swarming in a beam of lightfrom a fiber-optic swarmingin a lightshaft and forlaboratory experiments run in lightpipe designed to simulateshafts of sunlight in the mangrove thedark.1200 Mean rateof changeof direction-RCD. habitat.Mean rateof changeof direction-RCD. 100-~ swimmingspeed ~ (from ~ ~ 3.09~ to~ 3.24~ mm s-1) and a de- crease in average RCD (from 287 to 266 deg s-1) were position.There was also a trendof decreased turning rate not statisticallysignificant (Student's t-testwith paired withincreased current speed as copepodssurged forward design,ae = 0.05); however,we founda significantincrease in continuousswimming bouts or wereswept along by thecurrent flow, in contrastto thefrequent short bouts O of rapid swimmingexhibited by swarmingcopepods in day experiments 0 nightexperiments currentsduring the day. The densityof copepodsin the fieldof viewalso declinedwith increasing current speed thedr. Mea rat of chng of dieto C.. becausesome copepods moved to thebottom of the con- 10 0 ? tainer,perhaps to avoid thefaster speed flows (Fig. 4). The presenceof planktivorousfish tended to disperse swarmsof D. oculata. Whenthree juvenile sergeant ma- jors werereleased from the clear plastic tube that sepa- o Day- =y 0.46x + 4.53 r2 c 0.69 ratedthem from the swarm,they quickly located the swarmingcopepods and beganfeeding on them.Escape s i g Nighty = -Q.18x + 3.03 r2- 0.70 responsesof individual copepods were clearly visible and theseresponses, in combinationwith the turbulence cre- 02 * atedby the fish swimming through the swarm, caused the swarmto disperse.When the fish pursued copepods into thecorners of thetank, the swarm began to reform,but 0 2 4 6 8 10 12 14 16 18 20 thefish eventually returned to theswarm to pursueother Current Speed (mm s-1) copepods. Fig.4. Changesin copepoddensity in the center of the swarm The averageswimming speed and RCD forcopepods withcurrent speed in daytimelaboratory experiments for co- in the centerof the swarmfor periods before and after pepods swarmingin a lightshaft and in nightlaboratory ex- thefish were released showed little change in mean values. perimentswithout visible light where copepod density was mea- For 10 replicateexperiments, a slight increase in average surednear the middle of theflowthrough chamber. 518 Buskeyet al.

20 ated nets,Van Dom watersamplers, plastic bags, direct measurementsfrom submersibles, and photography (Hamnerand Carlton1979; Alldredge et al. 1984; Ambler 0 Fish Absent * 15D et al. 1991). Hamnerand Carlton(1979) used photographicmeth- ods and estimatedthe densityof D. (Oithona)oculata

CL swarmsnear coral reefsto be 1.6 ml-'; Ambleret al. (1991) usedhand-held plastic bags and estimated the den- ao- o) 10 sityof swarmsin mangroveprop rootsto be 9.1 ml-', CL witha maximumdensity of 23 copepodsml-'. We did notestimate the density of copepods in theentire swarm withour video methods, but instead focused on thecenter ofthe swarm, where we foundan averagedensity of 34.5 copepodsml- I and a rangeof densities from 9 to 92 ml-I (Table 1). Densityprobably was a functionof boththe planktivorousFish Present co15- size of theswarm marker (the shaft of sunlightin which 4, the swarmsform) and the numberof nearbycopepods available to be recruitedinto the swarm.It would be interestingto determinehow densitychanges with dis- CL tance fromthe swarmcenter. Swarming midges show decreasingdensities away from the swarm center but have 4, CL a distinctswarm boundary (Okubo and Chiang1974). One ofour major goals was to comparethe swimming 0I behaviorof swarming D. oculatastudied in situwith that of capturedcopepods studied in the laboratory.Differ- 0 ~5 10 15 2 encesin swimmingbehavior between laboratory and in from SwimmingSpeed (mm s'1) situ studiescould arise a numberof conditions, includingdifferences in physicalvariables, such as photic Fig. 5. Distributionsof swimmingspeeds for swarming environmentor watermovements, and differencesin bi- Dioithonaoculata in laboratoryexperiments before and after ologicalvariables, such as swarmdensity, the stressof planktivorousfish were released. capture,and behavioralresponses to confinement.We wereable to consistentlyproduce swarming behavior in the laboratoryby creatinga lightshaft that simulated in thenet-to-gross displacement ratio (NGDR) (from0.62 shaftsof natural sunlight; light was clearlythe major en- to 0.70) and a significantdecrease in swarmdensity (from vironmentalcue for swarm formation (Buskey et al. 1995). 6.49 to 1.08 copepods mi-') (Student's t-testwith paired However,mean swimmingspeeds and RCDs are higher design, ae = 0.05). The increase in NGDR indicates co- in situ thanunder still water no-flow conditions in the pepods traveledstraighter, less circuitouspaths of mo- laboratory(Table 1, Fig. 1), even when no consistent tion-a behaviorconsistent with the dispersalof cope- currentwas observedin the field.In the absence of a pods fromthe swarm. directionalflow in the laboratory, D. oculataspends 50% The changein distributionof swimmingspeeds for D. of its time swimmingat speeds <2 mm s-', and the oculata swarmsin the presenceof planktivorousfish (Fig. distributionof speedsis highlyskewed (Fig. 6). In con- 5) clearlyindicates the greaterproportion of time spent trast,the distribution of swimmingspeeds for copepods by the copepods in higher speed escape and dispersal filmedin situ in the absence of continualcurrent and behavior. Maximum swimming speeds for D. oculata underslow flowthrough conditions ( 2 mms- ') aremuch duringescape responsesfrom predatory fish were calcu- moresimilar, with copepods spending < 10% oftheirtime lated fromthese experiments. The mean maximumes- at speeds <2 mm s-I and havingsimilarly shaped dis- cape speed(? 1 SD) was 101.3?23.4 mm s-, based on tributionsonly slightly skewed (Fig. 6). 20 randomlyselected escape responsesand calculated Distributionof the proportion of time spent swimming based on motionanalysis at 30 video framess-1. in differentdirections shows that copepods filmed in situ exhibitan evendistribution of swimming directions com- paredto thosefilmed in thelaboratory under still or flow- Discussion throughconditions (Fig. 7). Under stillconditions, co- pepods spend 20% of theirtime slowly sinking, com- This studyillustrates the power of usingin situvideo paredto <5% forin situor flowthroughconditions. For recordingas a tool forstudying the aggregative behavior theflowthrough studies, movements into the current (left) of zooplankton.Videotaped records of swarmscan be and withthe current(right) were more prominent than used to rapidlyand repeatedlymeasure the densityof forthe in situstudy, where persistent currents were not organismsin a swarmby imageanalysis techniques. In measured(Fig. 7). Evenwhen no currentswere observed previousstudies, different techniques were used to esti- in situ,there were always small-scale water movements mate copepod densityin swarms,including diver-oper- inducedby surface waves or otherforces. Our results and Copepodswarming behavior 519

5 12 Swarmfilmed in situ 10 Swarmfilmed in situ 4 8 3 8 4 2 0 0 10 Laboratory:Still Water Stillwater L Laboratory: 0 0

r 4. a. 2,2

10 . Laboratory:Flowthrough

4 0

4nfoLasaminaflwh oratonaeryFlotharcurrntspe Down Left Up Right Down Directionof Travel 0 ~~~~~10 Is Fig. 7. Distributionof time spentswimming in different SwimmingSpeed (mm ') directionsin thevertical plane for swarming Dioithona oculata Fig. 6. Distributionof swimmingspeeds fora swarmof in situin theabsence of persistent currents, for a swarmin still Dioithonaoculata recorded in situ in the absence of persistent water(no flow)in thelaboratory, and fora swarmin a flow- currents,for a swarm in still water (no flow)in the laboratory, throughcontainer at a currentspeed of 2 mms- 1.The direction and fora swarm in a flowthroughcontainer at a currentspeed ofwater flow in thechamber is leftto right. of 2 mm s-i. Swimmingspeeds under flowthroughconditions are currentcorrected.

imum lengthfor D. oculata is 0.8 mm (Ferrariand Bow- previousstudies investigating the effects of turbulence on man 1980), this corresponds to a sustained swimming copepodbehavior (Costello et al. 1990; Saiz 1994; Ki0r- speed of 25 body lengthss-1. The copepods seem to be boe and Saiz 1995) emphasizethe importance of biolog- able to sustainthese swimming speeds for periods of hours. ical-physicalinteractions in planktonic processes and sug- This performanceis impressive for an organism that, gestthat results from laboratory experiments conducted according to the definitionof "planktonic," should be in the absenceof watermovements must be cautiously driftingwith the currents.Under still-waterconditions in interpretedwhen applied to thefield. For D. oculata, it the laboratory,mean swimmingspeeds seldom exceeded seemsthat stimulation from water movement is necessary 4 mm s-1 (5 body lengthss-1). Swimmingspeeds of var- to get behavioralpatterns in the laboratorysimilar to ious freshwaterand marinecopepods measured by sim- thoseobserved in situ. ilartechniques under still-water (no flow)conditions range We observedthat copepod swarms could maintain po- from1.2 to 9.4 mms-I (Buskeyet al. 1987),all ofwhich sitionin currentsof up to 20 mm 51* Becausethe max- correspondto speedsof < 5 bodylengths s- l. Mean swim- 520 Buskey et al.

mingspeeds of 26 speciesof microzooplankton averaged arisingfrom increased competition for food also increase 4.8 bodylengths s-1, butranged from 1.2 to 21 (Buskey (Bertram1978). NonswarmingD. oculata have greater etal. 1993).For comparison,sustained swimming speeds amountsof chlorophylland pheopigmentsin theirguts of fishrange from 2 to 21 body lengthss-I (Beamish whenthey disperse at nightcompared to amountsof these 1978),and burst swimming speeds of larval fish can reach substancesfound in swarmingcopepods during the day up to 60 bodylengths s- 1 (Fuiman1986). Burst swimming (Buskeyand Petersonunpubl.), suggesting that compe- speedsof up to 154 mms5-1 were recorded for D. oculata titionfor food is high.It wouldbe interestingtodetermine escapingfrom predators, which corresponds to 192 body whetherswarm formation of D. oculatais reducedwhen lengthss- 1.The differencebetween a planktonicand nek- riskof starvationis high,as has been demonstratedfor tonicexistence is obviouslybased on size and scalein the B. longispina(Jakobsen and Johnsen1988b). The pattern case of D. oculata-not on therelative swimming capa- of swarmformation during the day, when risk of visual bilitiesof theorganisms. predationis high,and dispersalat nightmay represent a The potentialadaptive value of swarmingbehavior in tradeoffbetween reducing risk of predationand maxi- D. oculatamay includereduced dispersion by currents, mizingfeeding rate. protectionfrom predators, and enhancedopportunities for mating(Hamner and Carlton 1979; Folt 1987). SwarmingD. oculatacan maintainposition between the References mangroveprop rootswith tidal currentsof up to 2 cm ALLDREDGE, A. L., AND OTHERS. 1984. Direct sampling and s-5. Largeschools of small planktivorousfish (Anchoa, in situ observation of a persistentcopepod aggregationin Harengula,Jenkinsia) are foundat theedge of the man- the mesopelagiczone of theSanta Barbara Basin. Mar. Biol. groveprop-root habitat but not betweenthe prop roots 80: 75-81. whereDioithona swarms form. Swarm formation may AMBLER, J. W., F. D. FERRARI, AND J. A. FORNSHELL. 1991. entailthe use ofa visualmarker (light shafts penetrating Population structureand swarmformation of the cyclopoid themangrove canopy) to maintainthe swarm's position copepod Dioithona oculata near mangrovecays. J.Plankton betweenthe prop roots and to preventthe swarmfrom Res. 13: 1257-1272. BEAMISH, F. W. H. 1978. Swimmingcapacity, p. 10 1-187. In dispersingor beingwashed out into dense schools of W. S. Hoar and D. J. Randall [eds.], Fish physiology.V. 7. planktivores.The planktivoresprobably avoid theprop- Academic. roothabitat because of piscivorous fish (mangrove snap- BERTRAM,B. C. R. 1978. Living in groups:Predators and prey, pers,barracudas) found in theseareas. p. 64-96. In J.R. Krebs and N. B. Davies [eds.],Behavioral Swarmsof D. oculatadisperse at duskand reformat ecology. Blackwell. dawn (Ambleret al. 1991), and lightseems to be an BUsKEY, E. J. 1984. Swimmingpattern as an indicatorof the essentialcue forswarm formation and maintenance(Bus- roles ofcopepod sensorysystems in therecognition of food. keyet al. 1995).In thisstudy, copepods seemed incapable Mar. Biol. 79: 165-175. of orientinginto currents in thedark. Currents may dis- , K. S. BAKER, R. C. SMITH, AND E. SwIFr. 1989. Pho- D. tosensitivityof the oceanic copepods Pleuromamma grac- perse oculata into adjacentlagoons and channelsat ilis and Pleuromamma xiphias and its relationshipto light night,where food availability for individual copepods is penetrationand daytimedepth distribution. Mar. Ecol. Prog. certainlygreater than within densely packed swarms dur- Ser. 55: 207-216. ingthe day. The mechanismby which copepods find their , C. COULTER, AND S. STROM. 1993. Locomotory pat- way back to theprop-root habitat at dawn remainsun- ternsof microzooplankton:Potential effects on food selec- knownbut mayinvolve orientation to symmetricalpat- tivityof larval fish.Bull. Mar. Sci. 53: 29-43. ternsof angularlight distribution in a manneropposite , C. G. MANN, AND E. SwIFr. 1987. Photophobic re- to theshore avoidance behavior of some freshwaterco- sponses of calanoid copepods: Possible adaptive value. J. pepods(Siebeck 1980). Plankton Res. 9: 857-870. Clumpingof zooplanktonprey has been shownto be , J. 0. PETERSON, AND J. W. AMBLER. 1995. The role of photoreceptionin the swarmingbehavior of thecopepod an importantprotection against (Milinski 1979; Dioithona oculata. Mar. FreshwaterBehav. Physiol. 26: Folt 1987;Jakobsen and Johnsen1 988a). We foundthat 273-285. once planktivorousfish located the swarmand began BYRON, E. R., P. T. WHITMAN, AND C. R. GOLDMAN. 1983. feeding,the escape responsesof thecopepods tended to Observations of copepod swarms in Lake Tahoe. Limnol. dispersethe swarm. However, the planktivores we used Oceanogr. 28: 378-382. werefree from predators; instances of predation by plank- COSTELLO, J. H., AND OTHERS. 1990. Grazing in a turbulent tivorousfish (or even theirpresence near swarms)was environment:Behavioral response of a calanoid copepod, rarelyobserved in nature.Predators may feed mainly Centropageshamatus. Proc. Natl. Acad. Sci. 87: 1648-1652. aroundthe edges of larger swarms, and escaperesponses EMERY, A. 1968. Preliminaryobservations of coral reefplank- wouldthen involve copepods moving toward the center ton. Limnol. Oceanogr. 13: 293-303. FERRARI, F., AND T. BowMAN. 1980. Pelagic copepods of the ofthe swarm, as does thecladoceran Bosmina longispina familyOithonidae () fromthe east coasts ofCen- (Jakobsenand Johnsen1988a). For smallswarms of D. tral and South America. Smithson. Contrib.Zool. 312. oculata, the main protectionfrom predation may come FOLT, C. L. 1987. An experimentalanalysis of costs and ben- fromthe reduced encounterrates of predatorswith efitsof zooplanktonaggregation, p. 300-314. In W. C. Ker- clumpedprey; however, as thebenefits of reducedpre- foot and A. Sih [eds.], Predation: Direct and indirectim- dationrisk increase with increasing swarm size, the costs pacts on aquatic communities.New England. Copepodswarming behavior 521

FuIMAN,L. F. 1986. Burst-swimmingperformance of larval SCHULZE, P., AND OTHERS. 1992. Video systems for in situ zebra danios and theeffects of diel temperaturefluctuations. studies of zooplankton. Ergeb. Limnol. 36: 1-21. Trans. Am. Fish. Soc. 115: 143-148. SIEBECK,H. 0. 1980. Optical orientationof pelagic HAMNER,W., AND J. CARLTON. 1979. Copepod swarms: At- and its consequence in the pelagic and littoralzones. Am. tributesand role in coral reefecosystems. Limnol. Ocean- Soc. Limnol. Oceanogr. Spec. Symp. 3: 28-38. New En- ogr. 24: 1-14. gland. JAKOBSEN, P. J., AND G. H. JOHNSEN. 1988a. Size-specific STEARNS,D. E., AND R. B. FORWARD,JR. 1984. Photosensi- protectionagainst predation by fishin swarmingwaterfleas, tivityof the calanoid copepod Acartia tonsa. Mar. Biol. 82: Bosmina longispina.Anim. Behav. 36: 986-990. 85-89. , AND . 1988b. The influenceof food limitation STRICKLER,J. R. 1975. Swimmingof planktonicCyclops spe- on swarmingbehavior in the waterfleaBosmina longispina. cies (Copepoda, Crustacea): Patterns,movements and their Anim. Behav. 36: 991-995. control,p. 599-613. In T. Y. T. Wu et al. [eds.], Swimming KI0RBOE, T., AND E. SAIz. 1995. Planktivorous feeding in calm and flyingin nature.Plenum. and turbulentenvironments, with emphasis on copepods. TISELIUS,P. 1992. Behavior of Acartia tonsa in patchy food Mar. Ecol. Prog. Ser. 122: 135-145. environments.Limnol. Oceanogr. 37: 1640-1651. MILINSKI, M. 1979. Can an experiencedpredator overcome UEDA, H., A. KUWAHARA,M. TANAKA, AND M. AZETA. 1983. the confusionof swarmingprey more easily?Anim. Behav. Underwaterobservations on copepod swarmsin temperate 27: 1122-1126. and subtropicalwaters. Mar. Ecol. Prog. Ser. 11: 165-171. OKuBo, A. 1980. Diffusionand ecological problems: Mathe- WONG,C. K., C. W. RAMCHARAN,AND W. G. SPRULES. 1986. matical models. Springer. Behavioral responsesof a herbivorouscalanoid copepod to , AND H. C. CHLANG. 1974. An analysis of the kine- the presenceof otherzooplankton. Can. J. Zool. 64: 1422- matics of swarmingof Anaretepritchardi Kim (Diptera: 1425. Cecidomyiidae). Res. Popul. Ecol. 16: 1-42. SAIz, E. 1994. Observations of the free-swimmingbehavior Submitted:6 March 1995 ofAcartia tonsa: Effects of food concentrationand turbulent Accepted:5 September1995 water motion. Limnol. Oceanogr. 39: 1566-1578. Amended: 16 January1996