Response of Night-Migrating Songbirds in Cloud to Colored And

Responseofnight-migrating songbirds incloud to coloredand flashing light

WILLIAMR. EVANS ß OLDBIRD, INC. ß 605WEST STATE STREET ß ITHACA, NEW YORK 14850 ß (CORRESPONDINGAUTHOR; E-MAIL: WREVANS@CLARITYCONNECT. COM) YUKIOAKASNI ß LIGHTINGRESEARCH CENTER ß RENSSELAERPOLYTECHNIC INSTITUTE ß 21 UNIONSTREET ß TROY,NEW YORK 12180 NAOMI S. ALTMAN ß DEPARTMENTOF STATISTICS PENN STATEUNIVERSITY UNIVERSITYPARK, PENNSYLVANIA 16802-2111 ALBERTM. MANVILLE,II ß UNITEDSTATES FISH & WILDLIFESERVICE ß 4401 NORTHFAIRFAX DRIVE, MBSP 4107 ß ARLINGTON,VIRGINIA 22203

Figure1.1500W halogen test lights with blue and red filters used to study the impact of light upon migrating birds.

Abstract tion on clear nights (Sauer 1957, Emlen causebird aggregationbehavior by Cochran Night-migratingbirds often accumulate near 1967),and on cloudynights they can orient andGraber (1958) and in a subsequentstudy bright man-madelight on nightswith low by sensingthe axial inclination of the earth's by Averyet al. (1976). The towersin these cloud cover or rain. Massavian mortality magneticfield through a light-dependent studieshad multiple tiers of slowflashing red eventsassociated with thisphenomenon have mechanism,probably residing in their eye beacons,each alternating with a tier of non- beendocumented for more than 150 years. (Wiltschko et al. 1993, Ritz et al. 2000, Ritz et flashingred beacons in accordancewith Unit- Understandingthe mechanismthat induces al. 2004, Mouritscnct al. 2004, MOllcr et al. ed States Federal Aviation Administration the aggregationof migrantsin lightedair- 2004. Thalau et al. 2005). (FAA)regulations. By the 1970s,bird kills at spacecould lead to a reductionin suchmor- The groundswellof artificiallighting asso- such towers were widespreadin eastern tality.Toward this end, we subjectednight- ciated wzth modern human habitation has North America (Weir 1976, Avery et al. migratingbirds flying in densecloud cover to greatlyaltered the earth's nocturnal photic en- lq80), with annualmortality of more than alternatingshort periods of differentartificial vironment. Little is known about ho• this 2000 birdsper year at sometowers (Banks light characteristics.Bird aggregationoc- light affectsmigrants on clear nights,but 1979).One long-term study found more than curredduring periods of white, blue, and birdshave long been observed to aggregatein 120,000 bird carcassesunder a 300-m TV greenlight but not in red lightor flashing flight around isolatedbright light sources towerfroin 1957-1995(Kemper 1996). This whitelight. We discussthese results with re- duringnights with low cloudceiling or with included24 individualnights when more spectto visualand magnetoreception-basedlight to moderaterain. The phenomenonwas than 1000 birds were documented killed in aggregationtheories and the phenomenonof widelyrecognized at coastallighthouses zn the tower'svicinity (Kemper,pers. comm.). light-inducedbird mortality at tall television westernEurope and eastern North America in Suchlarge nocturnal tower kills appear to be towers in North America. the nineteenthcentury. By themid-twentieth exclusivelyassociated with low cloudcover century,artificial lighting was known to be a or rain; under such conditions,a tower'savia- Introduction principalagent for causinglarge bird killsat tionobstruction lights clearly induce aggrega- The nocturnalmigration of birds evolved airportceilo•ncters, tall television(TV) tow- tionsof migratingbirds (primarily species in with only starlightand moonlightas consis- ers,smokestacks, and tall buildingsin inland the order Passcriformes)Most of the kills are tent photonsources. It is known that some easternNorth America (for a recent review, believed to result when birds collide with a speciesutilize this subtle light for navigation- see Gauthrcaux and Belscr 2006). towergsupporting guy wires, the tower itself, al aid.They use point sources of lightin stel- In North America, aviation obstruction or frommid-air collisions with otherfi)4ng lar arraysaround the NorthStar for orienta- lightingon tallTV towerswas documented to birds.

476 NORTH AMERICAN BIRDS RESPONSEOFNIGHT-MIGRATING SONGBIRDSINCLOUD TO COLORED ANDFLASHING LIGH1]

Morethan 30 yearsago, Avery et al. (1976) 0.25 called for field studies on the reactions of night-migratingbirds to lightsof variousin- tensities,wavelengths, and flashrates as a meansfor increasingour understandingof 0.20 81750W waFI bird aggregationat tall lightedtowers. We re- A1750W wRF I port hereon the firstdirect investigation of • 0.15 •A1 750WwGFI O •j-•A1750WnoFL theseartificial light variables for causingbird aggregation. -- 0.10 In October2005, on fivenights with steady bird migrationand a cloudlayer at ground level,we alternatedperiods of skyward-facing ,-, 0.05 bright light of knownspectrum and irradi- ancewith periodsof no light.Acoustic moni- 0.00 toringof avianflight-calls was used to indicatethe presenceor absenceof flyingbirds 350 400 450 500 550 600 650 700 duringall light and dark periods.Visual ob- Wavelength (nm) servationsof birdsflying in the lightedspace weremade to verifybird aggregationduring Figure2. Spectralpower distributions ofradiation with and without filters used in this study. Meast•ements arefor a singlehalogen nonflashing light periods. lamp(750W; with UV filter). Filter codes: noF: nofilter, wBF = bluefilter, wRF: red filter, and wGF = greenfilter. We concludedthat a specificlight type inducedbird aggregation if periods of thatlight rate,quantification of flyingbirds involved in curatelybetween birds, bats, and largein- correspondedwith strongacoustic and visual actualaggregation events was not reported. sects,but operationis impededby cloudand evidencefor the presenceof birdsin at least Because these studies were all carried out at rain conditionsthat oftenaccompany aggre- four consecutivealternating cycles with a pe- tall TV towers,the lightsinvolved in altering gationevents. Similar to verticalbeam radar, riodof a differentlight type and/or a periodof avianflight behavior were well aboveground targetcounts during artificial light aggrega- no light in which bird presencewas not level.The birdsstudied were generally well tionevents can only be activity indicators due stronglydocumented. Good correspondence above ground level but under a low cloud to individualbirds flying in andout of theim- betweenthe acousticand visualdata during ceiling,not flyingwithin cloud. agingzone. nonflashinglight periodsgave us confidence Our investigationaimed to studybird ag- Acousticmonitoring is notablefor being in relyingon the acousticdata [or evaluating gregationat a ground-basedlight sourcein capableof discerningstrictly birds--and in flashinglight testswhen we couldnot verily densecloud. This scenariopresents unique manycases the species of birds--innocturnal thepresence or absenceof birdsvisually. challengesfor tryingto monitorsystematical- flight (Evansand O'Brien2002), and this We firstdocumented that white light could ly the quantityof birdsin the airspacenear methodis not impededsignificantly by fog be usedto inducemigrant bird aggregation. the light. Many nocturnalmigration studies andlight rain.But birds that do not call,and We then experimentedwith flashingwhite have used marine radar in the surveillance variablecalling rates among individuals and light,three different colors, and a combination modeto attemptto quantifya passagerate for species,confound quantitative estimates. Re- o[ red incandescentbeacons commonly used targetsproceeding directionally in migration. centstudies indicate that there is at leastgross [ormarking aviation hazard on tall TV towers. But this techniquecan haveproblems with correlation between acoustic data from vocal echoesfrom ground clutter and in detecting birdsand the densityof targetsin someloca- Materialsand methods very low-flyingbirds. Quantifying masses of tions at sometimes (Larkin et al_2002; Evans, Rationalefor studymethod birds in aggregationaround artificial lights in prep).Iwo previousbird aggregationstud- Todocument whether bird aggregation is oc- would be difficult with marine radar in the ies at IV towersfound correspondence be- curringin a givenairspace subject to artificial surveillancemode, and there is a potential tweenflight-calling and the grossnumber of lightalterations, one needs some means to as- problemof validatingthat the targetsare birdsin the vicinityof a tower.Avery et al. sessthe quantit),of birdsflying in that air- birds.The use of flightspeed as a criterionfor (1976)used a cellometer(spotlight) to count space.Since the visuallybased studies by distinguishingbirds from insects may not be birdsvisually in aggregationaround a tall IV Cochranand Graber(1958) and Averyet al. reliableduring aggregation events. towerin North Dakota.When skiesbegan to (1976), fourstudies of bird flightbehavior in When marine radar is used in the vertical clear,they noted that the number of birds the vicinityof TV towerswith aviationob- mode,ground clutter can be eliminated,and seenand hearddecreased sharply. In an all- strucuonlighting have been reported,each low-flyingbirds can be detected.But in cases nightstudy of a towerkill phenomenonon 28 employinga differentmethod. Larkin and wherebirds are milling around in lightedair- September1960, Ogdenand Munro noted Frase(1988) usedtracking radar. Gauthreaux space,quantitative resolution is greatlydi- grosscorrelation between flight-calling and used a thermal imagingdevice, and Gau- minisheddue to theinability to trackindivid- birdsdropping to the ground(Ogden 1960). threauxand Belserused an imageintensifier ual birdsthat may repeatedlypass through Ihey notedthat periods when there was rela- (Gauthreaux and Bclser 2006). Johnson the radarbeam. Counts are reducedto being tivelylow or no flight-callingcorresponded (2005) usedmarine radar. The primary focus merelytarget activit) indicators. with no birdslalling to the ground,whereas of thesestudies was on the flightbehavior of Thermalimaging, image intensifier, and vi- periodsof highcalling rate corresponded with birds, and whether it was linear, curved, or sual(in conjunctionwith a lightsource) tech- a steadyrain of birdsfalling to the ground hovering.Though some documented passage niquesmav allow one to distinguishmore ac- (Ogden1960) Simplystated, calling indi-

VOLUME 60 (2007) ß NUMBER 4 477 RESPONSEOFNIGHT-MIGRATING SONGBIRDS INCLOUD TOCOLORED ANDFLASHING LIGHT

1.00 advancedslowly eastwardduring the first week of October and stalled as a weak frontal

Red-filtered A1 boundaryalong the AtlanticCoastal region 0.80 duringour study period. This weather pattern L864 slowedbird migration in eastern-central L810 North Americain the first week of October, 0.60 with no northerlywinds to facfiitatemigra- tion.After the slowly moving front passed our studysite in centralNew YorkState during 0.40 theday on October8th, winds became steady from the north to northeast and favorable for migration. For a detailed accountof the 0.20 weatherand associated bird migration during our study period, see Dinsmore and Farnsworth(2006) and a subsequentcorri- 0.00 , gendum(Brinkley 2006). 400 450 500 550 600 650 700 Accompanyingthese favorable migration winds was a broad area of low-altitude,solid Wavelength (nm) (100ø6) cloud cover associated with the weatherfront and low pressureon the At- Figure3. Relativespectral power of a red-filteredhalogen luminaire, the large red flashing aviation beacon (L-864), and small red lantic coast. Cloud cover observations were beacon(L-810). madeat our studysite. and regionalweather data, includinghourly cloud cover,cloud caresthe presence of birds;no callingmay or Appalachian/AlleghenyPlateau. The terrain ceilingheight, and wind directionwere ob- maynot indicatethe absence of birds.In cas- to the northand northwestwas generallyat tainedfrom the hhacaairport, 16 km to the eswhere the speciescomposition of a flight lower elevation for more than 200 km. Ter- northof ourstudy site. These data concurred involvesmany that are known to giveregular rainto thenortheast was roughly the same al- with our visual observations that 100% cloud vocalizationsin nightflight, then the lackof titudefor 100 km exceptfor severalnorth- coverwith a cloudceiling at or belowour callingvery likely correspondsto a lack of south runningvalleys. These specificgeo- studysite elevationcoincided with mostof birds given consistentenvironmental vari- graphiccharacteristics are noted because, our studyperiods. In the five nightsof our ables.In caseswhere the species composition with the low cloudceiling, they couldhave study,artificial light experimentation was car- is primarilyof speciesthat are not knownto causedchanneling of migrationas south- riedout in 29 hourlyperiods. Twenty-five of giveregular vocalizations in nightflight, then bound migrantsin the lower atmospheric these29 hourly periodshad cloud height thelack of callingobviously would not corre- stratum encountered an increase in terrain measurementsat the Ithaca airport correspondwith a lackof birds. elevation(Evans, unpubl. data). spondingto a cloudceiling height of between There is no demonstratedway to count Lightfrom three 60W incandescentlamps 45 and 135m belowour studysite. This sug- with accuracybirds flying in cloudor light within the residence emanated from the resi- geststhat birds during most of ourstudy were rain duringground-based aggregation events dence windows to make a constant, weak flyingwell within the cloud layer. in artificiallight. All the currentlypractical lightsource throughout the study. Within a 5- The moonphase ranged from one day be- methodsare activityindicators, which pro- km radiusof thestudy site, there were sever- forefirst quarter (half moon) to threedays af- videonly an indexof abundance. al dozen rural residences with various inter- terfirst quarter. kight from the moon was not In this study,we usedacoustic and visual nal lightingemanating from residencewin- visibleto us during our studydue to the methodsas coarse activity indicators because dowsand some with outdoorlights typical of densecloud layer. Ambient light at ground of theirability to detectbi•ds down to ground residences.There were no brightlight sources levelwhere the studylights were stationed level.It was knownfrom previousacoustic associatedwith businesses,athletic fields,etc. wasless than the measurementcapability of monitoringin the regionthat many species within 5 km. Our study lights were the our light meter(<0.01 lux) in all directions. movingthrough our site during our study brightestsource of skywardfacing light with- This measurementincluded light emanating timewould be vocalduring nocturnal migra- in thisradius. There was extensive brighter fromthe incandescentlamps within the resi- tion (Evans and O'Brien 2002; Bull 1998). In lightingassociated with thecity of Ithaca,10 dence,the nearestof whichwas 20 m away addition, both the acousticand visual moni- km to thenorth of ourstudy site. from the site. toringmethods are inexpensive, which facili- Our studysite was roughly 5 km westof tatesduplication and wider experimentation Studyperiod, weather. moon phase, and mag- the centerof a 180-km,NNW-SSE running with thisstudy technique. netic environment transectof totalmagnetic field strength meas- Thestudy was carried out on fivemghts from urementsmade by kednor(1982). Total mag- Studysite October8 throughOctober 14, 2005_This netic field strengthin the regionis around Our studysite was a lawnoutside a ruralres- time periodcorresponded with an "omega- 56.0 microTesla with variations 9 km to the idence 10 km south of Ithaca, Tompkins blocking"pattern in the jet streamacross northand south of 50-300nT. No majormag- County,New York (42.335ø N, 76.499ø W). easternNorth America. Such patternsare netic anomalies are known from the hhaca The site elevation was 503 m above sea level characterizedby slow-movingfrontal systems area(C. Walcott,pers. comm.). The K-index in hilly terrainnear the northernedge of the at the surface. In this case, a cold front had to fluctuationin theearth's magnetic field for

478 NORTH AMERICAN BIRDS RESPONSEOFNIGHT-MIGRATING SONGBIRDSINCLOUD TO COLORED ANDFLASHING LIGHTl

16 16 -e- Blue B 14 14 -A- Red 12 Red l 12 -•- Off • lo E 8

• 6 • 6

4 4 2

0 O•5 5 1 2 3 4 .5 6 7 8 9 1011 12 13 14 15 16 17 2 :3 4 5 6 7 8 9 10 II 12 1:3 14 15 16 17 Time Period Time Period

16 16

14 14 -•- White D' -e- Off -e- Off 12 -m-White flashing 12 -•- L-864 lO _•_ L-864/L-810

• 6

4 4

2 0 _-,',_,•,_ ,• ..... _-...... •,_' .... 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 1 2 3 4 5 6 7 8 9 101112131415161718 Time Period Time Period

Figure4. Acousticandvisual data from consecutive timeperiods onthe five nights of the light study.Points connected bylines indicate the arian calling rate per minute ineach time period. Thenumbers within the graphs indicate the maximum number ofindividual birds visually de- 3 • -•-White E tectedin a $+ minuteperiod of observation within nonflashing light periods (see Methods). (A)1500W halogen light with red or green filter. All periods were 10 minutes induration. (B) 1SOOWhalogen light with red or blue filter. Ughts-on periods ranged from 10-15 minutes; lights-offperiods ranged from 4-$ minutes.(C) Rashing and nonflashing periods of1500W halogenlight. All periods were 10 minutes induration. (D)1 $00W halogen light or one or more redaviation obstruction beacon lights. Lights-on periods ranged from 15-35 minutes. Lights- offperiods ranged from $-12 minutes. L-864 isthe 1260W red incandescent aviation obstruc- tionbeacon flashing 34 times per minute. L-810 is the 116W nonflashing redaviation ob- structionbeacon. (E) 1500W halogen with red, blue, or no color filter. The first dark period was 44minutes. The first red period was 19 minutes. All other periods were between 10-13 minutesin duration. All the light and dark periods during the alternating white sequence were 10 -4-Off minutesin duration. 8 9 10 11 12 13 14 15 16 17 18 19 Time Period theperiod October 8-14 (asmeasured in Ot- to the northeastof our studysite. Ritz el a[. ended tubular halogenlamps (250W and tawa, Canada, 300 km to the north of our (2000) and Thalau et al. (2005) allude to the 500W), a reflector,a metal housing,and a studysite) was relatively quiet except for Oc- potentialimportance of documentingsuch glasspane that filtered out UV light.The pair tober8•the first nightof our light study-- mid-frequencyradio wave parameters in noc- of luminaires combined to form a 1500W when it reached a value of 5 (k. Newitt, Ot- turnalmigration studies. light source.We usedtwo differentpairs of tawa MagneticObservatory, pers. comm.). luminairesduring the study(Figure 1). One The artificialelectromagnetic environment of Studylights and light measurement of the two pairswas used in the flashingand our study site includedmost notably the Artificiallight in thisstudy was created using nonflashingwhite light tesls and with redfil- WHCU (870 kHz) AM radio station, which one pair of work-lightluminaires, commer- tersfor thered light tests. The otherpair was wasbroadcasting at a powerof 1.0 kW in dz- czallyavailable in the Urnted States Each usedwith blueand greenfilters for the blue rectline of sightfrom a seriesof towers5 km workluminaire was composed of twodouble- and greenlight testsWe usedRoscolux gel

VOLUME 60 (2007) NUMBER 4 479 IRESPONSEOFNIGHT-MIGRATING SONGBIRDSINCLOUD TO COLORED ANDFLASHING LIGHT

custom-built flash rate controller was used to 1.0 flasha 1500Whalogen luminaire pair with no -I- Laurel Mtn. colorfilter at 24 timesper minute.Ihe on- timeper flashwas 0.2 second,and the time to 0.8 Alfred,NY peakoutput appeared nearly instantaneous. * LaurelMtn.- LS Additionallight periodswere carriedout --&--Alfred,NY - LS usinga slow-flashingred beacon (FAA type L- 0.6 864;IWR Lighting,Houston, IX, USA)by itselfor in combinationwith a nonflashingred beacon(FAg. type 1.810; GalaxyLitebeams, 0.4 Burbank, California). Ihe 1-864 consistedof two 620W incandescentlamps inside a red Fresnellens, which focused the hghton the 0.2 horizontalplane to producea peakintensity of about 2000 candela. Ihis beacon was set to produce34 one-secondflashes per minute. 0.0 Eachflash increased in intensity[or the first I 2 3 4 5 6 7 8 9 10 half-secondand decreased in intensityfor the latter half second. Ihe 1.810 contained a sin- Minutes gle 116Wincandescent lamp inside a redFres- nel lensthat whenmounted upright focused Figure5A. thelight on thehorizontal plane to producea peakintensity of about32 candela. 12 Eachpair of halogenluminaires was mounted approximately1.5 m aboveground level on • LS - gr/bl/whlight a tripod.Ihe lampswere angled 20 degrees 10 • LS - dark from the zenith toward the northeast to direct • LS - red lightaway from the residence structure and as- • 8 sociated trees so as to maximize the transmis- sionof lightinto the atmosphere.Each lamp pair radiatedmost light upwardwithin ap- proximatelya 75-degreecone (Figure 1). lhe red aviation obstruction beacons were laid on theirsides and angledapproxi]nately 20 degreesfrom the zenithtoward the northeast.Ihis facihtatedd]recnng the max]mum lightintensity from these beacons into theat- mosphere. Spectralpower distributions with andwith- 0 out filterswere measured at a rangeof wave- I 2 3 4 5 6 7 8 9 10 11 lengthbetween 350 nm and 830 nm at 2-nm intervals. Ihese measurements were made us- Minutes ing an integratingsphere system, which con- Figure5B. sistedof a spherewith a diameterof 1.65m, a computerizeddouble monochromator (Op- Figure5. This graphic shows the average calling rate for the first, second, third, etc minute respectively formultiple ten-mioute seg- tronic Laboratories, Model 750-M-D, Orlan- mentsat the two reference acoustic stations and in spedtic light conditions that were precisely tenminutes induration. •] Showssuch do, Florida), and an enhancedsilicone detec- datafor all nights from September 1 through October 15at the control acoustic stations inNfred, New York, and Laurel Mountain, tor (OpttonicLaboratories, Model DSM-1D, Pennsylvania,withmore than 50 calls detected innine hours. Each night was broken up into consecutive ten-minute periods. The yel- Orlando, Florida). Each of the four luminaires lowline (Alfred) and the red line (Laurel Mountain) represent respective minute calling rates for 1080 and 1404 ten-minute periods. Thegreen and blue lines represent respective minute calling rates for 36 ten-minute periods from Alfred and 180 ten-minute periods was first measuredwith bothhalogen lamps fromLaurel Mountain that occurred during our light study on nights that had more than SO calls detected innine hours. (13) Shows re- on (250W+500W=750W). Iable 1 summa- spectiveminute calling rates for each minute in ten-minute periods during spedtic light periods inour light study (LS). The rising blue rizes the resultsof radiantpower measure- lineindicates the calling rate detected for each respective minute during the 16 ten-minute periods ofaggregation ingreen, blue, and mcnts for the four luminaires derived from the whitelight shown inFigure 4A-D. The eleventh minute of the blue line indicates the calling rate in the first minute of lights-off after spectralpower distributionmeasurements. eachof these 16 light periods. The red line indicates the calling rate per respective minute inthe 13 ten-minute red light periods duringthe green and blue light tests (Figure 4A-B). The black line shows the calling rate per respective minute in 16 ten-minute periods of Ihese radiantpower values were obtamed by lights-offduring the green and white flashing light tests. integratingmeasured spectral radiant power overa wavelengthrange visible to birdsfrom filters(Rosco Laboratories, gel filters #19, 69, implementedusing a singleluminaire with 400 nm to 680 nm (Palacios and Goldsmith 389, Stamford,Connecticut). onlythe 250W,500W, or bothtubular lamps 1993; Goldsmith and Butler 2005). Stnce Variablewattage whtte light periodswere in operation.In theflashing white light test, a thesemeasurements identified consistency in

480 NORTH AMERICAN BIRDS RESPONSEOFNIGHT-MIGRATING SONGBIRDSINCLOUD TO COLORED ANDFLASHING LIGHT1

Table1. Results ofhalogen luminaire TaMe2. Estimated peak irradiances ofwhite and filtered lights ata wavelength possibleto determinebecause individuals typ- radiantpower measurements. Each rangebetween 400 nm and 680 nm. Column 2shows radiant power ofour icallypassed in andout of thevisibly lighted luminairehasan input power of7.50W. whiteand filtered lights (2halogen luminaires; 1500W) over the 400-680 nm space.All visualcounts represent the maxi- Luminaire Radiantpower (W) rangeasmeasured withan integrating sphere Column 3indicates thecalcu- mum number of birds that could be seen in A1 26.9 latedirradiance ofour flitwed lights at50 m (values donot account forattenu- thesame field of view.The only exception is Pair1 ationof irradiance fromcloud). See Figure 2for spedral energy distribution. A2 26.4 whenan individualthat had not beenprevi- B1 26.6 Color Radiantpower (400-680 rim) Peakirradiance at50m ouslynoted was recognized by itsprofile. This Pair2 occurred on several occasions when a thrush B2 25.7 Blue 7.7W < 2.5mW/• specieswas seenduring the count period Mean 26.4 Green 13.6W < 4.3mW/m • whenonly smaller warbler- and sparrow-sized radiantpower between two lu- Red 24.0W < 7.6mW/• passerineshad been previously tallied. Visual minairesin eachpair, only one White 53.9W < 17.1mW/m 2 observationsbegan at leasttwo minutesinto luminairefrom eachpair was the light periodand lastedat leastfive min- used for further color-filtered luminaire meas- This microphonewas positioned 5 m from utes. Once a visual count reachedfive birds, urements.Figure 2 showsthe resultsof spec- the lightsource and aimed20 degreesfrom the observationperiod was consideredsuffi- tral power distributionmeasurements with the zenith toward the northeast. The sensitiv- cientto indicatethe presence of birdsand was and without the colored filters. ity pattern of this microphonewas hemi- usuallydiscontinued. Spectralpower distributions of thered avi- spherical,with a regionof enhancedsensitiv- All visuallyobserved flying bxrds were esti- ation beacons were similar to the red-filtered ity expandingskyward in roughlya 60-degree matedto be withinabout 50 m of the study halogenluminaire (Figure 3). Peakirradiance cone.The audiosignal was digitally recorded lights.Any gross variability in thebird obser- of the red beacons was determined based on forthe duration of thestudy periods. The ver- vationcapability by a humanobserver over the manufacturerspecification for those ticalrange of thissystem for detectingarian this rangeduring the differentcolored-light lights.Peak irradiance of thered flashing bea- flight-callshas been estimated to be greater periodswas roughlyassessed by whethera con (L-864) was about one-third that of the than 200 m for mostsmall passerine (e.g., treeline approximately 50 m to theeast of the red-filteredhalogen luminaire. Parulidaeand Emberizidae)flight-calls and studysite was visible. Since it wasvisible in Mostbirds in thisstudy were estimated to beyond500 m formid-sized passerines in the boththe short and the long wavelength light be 50 m or morefrom the light source. In or- familyTurdidae. The preciserange is not crit- periods,no grossdifferences in the rangeof der to determinethe highestirradiance birds icalfor thisstudy except to notethat it cov- humanvision were evident during our short might haveencountered at this distance,we ereda muchlarger volume of spacethan that and long wavelengthlight periods.In addi- measuredpeak illuminance at 5 m fromone coveredby the visualobservations. tion, severalspecies of mothsin the family of the luminaires (Luminaire A1 in Table 1) in W Evanslistened to the audiorecordings Noctuidaewere active and seendearly at a a photomerrylaboratory at RensselaerPoly- usingheadphones, and calls heard were man- distance in the red as well as other nonflash- technicInstitute. The peakilluminance was uallylogged by the timesof theiroccurrence. ing lightperiods. No batswere seen during approximately250 Ix. At 50 m, thiswould be The temporalcalling record was then associ- our October2005 studyperiod, but a repeat 2.5 Ix. Usingour previous measurement of lu- atedwith thetiming of thelight experiments, of this study during two cloud-grounded minousflux of 7880 lm for this luminaire,we andcall totals were assessed for each light and nightsin September2006 found that bats calculatedthat in orderto getan irradiance of darkperiod. For anothermode of evaluation, weredistinctly visible in thered light periods. 2.5 lx at 50 m, thesolid angle of thebeam-- respectiveminute totals were summed for all Given that the visual observations in both or the areaprojected on the 1-m diameter ten-minuteperiods during specific light tests 2005and 2006 took place in doseproximity sphere--shouldbe 1.26sr, assuming uniform andat tworeference acoustic stations on sig- to the 1500Wbright light source, it is likely light distribution.This beamdistribution is nificantmigration nights. The callingrate in that human cone cells were involved in the vi- equivalentto a 78.6-degreeconical beam. the first, second,third, etc. minuteswere av- sual observations and that the lower sensitiv- From this, we estimatedirradiance of the col- eragedfor all ten-minuteperiods, and any ity of humanrod cells to redlight versus blue oredlight at 50 m, basedon theirpreviously trendsin callingrate were assessed. or greenwas not a factorin assessingbird measuredspectral power distributions. Table Spectrographicanalysis was carried out on presencethrough visual observation. 2 indicates estimated irradiance of the white callsthat were loud enough to producea co- and filteredlights for two luminaires.These herentspectrogram. The flight-callreference Lightregimens estimated 50-m irradiance values do not ac- guideby Evansand O'Brien (2002) wasused Oneof thefollowing light sequences was re- count for attenuationfrom water droplets for speciesclassification. A minimum number peatedat leastfour times on oneof the (cloud;light rain) in the air and,therefore, of individualspresent during each light peri- fivestudy nights: theactual irradiances during our study would od wasdetermined by assessingthe number havebeen substantially lower than those indi- of speciespresent through spectrographic White - Lightsoff cated in Table 2. analysis. White- Lightsoff- Whiteflashing - Lights off Acousticmonitoring and flight-call detection Visual observations Red- Lightsoff- Green- Lightsoff An acoustictransducer (EK-3029cx, Knowles To corroborate the acoustic data's indication of Red- Lightsoff- Blue- Lightsoff Inc., Chicago,Illinois) was mounted to form whetheror not bird aggregationwas occur- FAAbeacon(s) - Lightsoff- White- Lights a directionalmicrophone with goodsensitivi- ring,visual observations of birds flying in the off- FAAbeacon(s) - Lightsoff ty between3-8 kHz (for microphonedesign, lightedspace were made during nonfLashing see ). lightperiods. Precise bird numberswere im- Weseparated all experimentallight periods

VOLUME 60 (2007) NUMBER 4 481 jRESPONSE OFNIGHT-MIGRATING SONGBIRDSINCLOUD TO COLORED ANDFLASHING LIGHT

•n this studyby a periodof no light before Determinationofaggregation tivelight cycles indicating that green and blue startinganother light period.The purpose Callingrate data were not relied upon to indi- light repeatedlyinduced bird aggregation, w•th thiswas to givethe birds that had been catethe densitylevels of migrants.We used whereasthe red lightdid not. The red light exposedto a periodof artificiallight time to acousticmonitoring only as an indicator for a had threetimes greater irradiance than the moveon duringthe darkperiod and poten- strongor weakpresence of birds.Similarly, blueand nearly two timesgreater irradiance nallyallow new birds to bein thevicinity be- data from visual observations were not ex- thanthe green (Table 2). Theeight green and forethe next lightperiod was imposed. The pectedto indicatethe numberof birdspres- blueperiods in Figure4 (A andB) had a mean longerthe dark period,the morelikely this ent. We usedvisual observation data only as of 7.2 callsper minute (s.e. 1.7), whereas the would be the case. However, this had to be an indicatorof whetheror not flyingbirds eightred periodshad a meanof only 0.45 balancedwith thefact that as more time pass- werepresent in thelighted space. callsper minute(s.e. 0.23) and the 18 dark es,weather conditions or thepassage rate of To ruleout thepossibility of misinterpret- periodshad a meanof 0.48 callsper minute m•grants necessaryto cause aggregation ingdiscontinuities in the density of nocturnal (s.e. 0.35). couldchange. By using conservative estimates birdpassage aslight-induced bird aggregation, Birdswere inducedto aggregatewith all forflight speeds (20 km/hr),birds could have we repeatedthe varyinglight regimens and energylevels of whitelight, the lowest tested beenas far as 1400 m fromour study site in 4 notedconsistency in bird presence or absence beinga 250W halogenlamp (in a reflector minutesif theyflew straight. Since we could duringspecific light conditions.We deter- housing)with a peakirradiance at 50 m of not confirm what birds did, and becausewe minedthat a specificartificial light condition less than 2.7 mW/m 2. However, when a verifiedthat some birds landed in thevicinity inducedaggregation if that light condition 1500W white halogenluminaire pair was of ourlights, we couldnot assume independ- showedstrong acoustic and visualevidence flashed(24 flashesper minute;0.2 sec on- ence betweenlight periods.Analysis of for the presenceof birdsduring at leastfour time per flash),no acousticaggregation be- speciesdata within andbetween nights was consecutivecycles with a differentlight type haviorwas documented (Figure 4C). ouronly evidence for different individuals be- and/ora darkperiod in whichbird presence Over the five nightsof studyduring se- cominginvolved in theaggregation events. wasnot strongly documented. To further sub- quenceswhen bird aggregationwas docu- Due to the experimentalnature of this stantiateour light-inducedcalling patterns, mented,the mean calling rate during dark pe- study,the lengthof the darkperiods we used we considerednatural calling patterns from riodsfor any specificnight neverexceeded wassomewhat arbitrary. Light and dark peri- tworeference acoustic stations in theregion. 0.6 callsper minute (s.e. of 0.14).The calling odswere typically 10-15 minutesin duration. Good correspondence between the rateduring the flashingred beacon (L-864), The alternatingred and blue light testhad acousticand visual data gave us confidence in theflashing red beacon (k-864) with thecon- 10-15 minutered and blue light periods but relyingsolely on theacoustic data for evaluat- stant-onred beacon (k-810), and the flashing only 4-5 minutedark periods,in orderto ingthe aggregation tendency of flashinglight whitelight periods was similar to thedark pe- maximizethe numberof lightstudy periods testswhen we couldnot verify the presence of riods.Figure 4D showsa sequenceof fourad- onthat night. Some light periods with the red birdsvisually. jacentlight cyclesin whichthe flashingred flashingbeacon were 15-35 minutes in dura- In thehypothetical case in whichno birds beacondid not induce aggregation by itselfor uon, so as to seewhether aggregation with wouldbe present, both the acoustic and visu- in combinationwith a low intensity,non• that light systemmight be inducedover a al indiceswould produceno detections. flashing,red beacon. The white light periods longertime period. We carriedout thecom- Whena seriesOf repeated light cycles that had in thisalternating light cycle had visual con- parisonof callingrates between periods of beenassociated with aggregationceased in- firmationof flyingbirds and recorded flight- differentduration by presentingdata in a ducingacoustic and/or visual indication of callingan orderof magnitudegreater than calls/minute format. aggregation,we interpretedthis to meanthat boththe dark and red beacon periods. movementsof migratorybirds had dimin- The proximatecalling rate variations Control sites ishedor ceasedin the vicinityof the study shownin Figure4 areunprecedented based Tworeference acoustic stations were in oper- site,or that the weatherconditions causing on 19fall seasons of monitoringnatural avian auonduring this light study Both were locat- theaggregation phenomenon had changed. flight-caflingrates from morethan 10 sites edin ruralareas with minorresidential light- withoutsubstantial artificial light in central •ngin theirvicinity One stationwas located Results New York(W. Evans,unpubl. data). Similar nearAlfred, New York, 107 km to the westof Aggregationappeared to be an on-offphe- patternsof callingrate variationwere not thelight study site. The other station was nomenonassociated with particularlight foundin adjacentten-minute periods for our cared107 km to the southwest,28 km north characteristics.Periods of white, blue, and controlacoustic stations at Alfred,New York, of Williamsport,Pennsylvania. While the greenlight had calling rates an orderof mag- and LaurelHill, Pennsylvania.We lookedat same microphonedesign and recording nitudehigher than dark period calling rates nightswith 50 or moreflight-calls recorded equipmentwere used at theselocations, the andcorresponded with multiplebirds seen in from Septemberthrough mid-October (at ratesof callingbetween sites were anticipated the lightedspace. No visualobservation of least9 hoursrecording per night). The largest to be differentbecause of potentiallyvariable birdsoccurred in the red lightperiods, and callingrate variation in 1404adjacent ten- m•grationpatterns and environmentalnoise thiscorresponded with very low overall call- minuteperiods at LaurelHill, Pennsylvama at thedifferent sites. The purpose of assessinging rateduring red light. These "no aggrega- was 160øœ,with a mean of 42%. At Alfred, datafrom these acoustic stations was to pro- tion" red periodsoccurred repeatedly be- NewYork, the largest variation between 1080 v•dea referencefor natural variation of flight- tweenalternating periods of greenor blue adjacentten-minute periods was 290%, with a callingin theregion, at siteswithout varying light,in whichstrong acoustic and visual evi- mean of 53%. This contrastswith the data •n artificiallight patterns. dencefor aggregationwas detected. Figure 4, Figure4, whichshow eight consecutive van- A and B, showsa sequenceof four consecu- ationsof 1000%or more in adjacentten-

482 NORTH AMERICAN BIRDS RESPONSEOF NIGHT-MIGRATING SONGBIRDS IN CLOUDTO COLORED AND FLASHINGLIGHT

Table3. Species composition ofcalling during each of the four periods ofcongregation inthe flashing white light test, green light test, and blue light test (see Figure 4A-C). Numbers offlight calls ofspecies orspecies' complexes withdistinctive flight calls are iodicated. Many calls ineach period could not be classified because they were too weak to identify orcould notbe placed ina distinctivecategory. Allclassification isbased on Evans and O'Brien (2002). SPECIES/ White Green Blue SPECIESCOMPLEX I 2 3 4 I 2 3 4 I 2 3 4 Gray-cheekedThrush 6 0 0 0 3 1 0 0 0 0 0 0 Catharusrainlinus

SwainsoffsThrush 5 6 7 3 3 1 0 2 0 0 0 1 Catharusustulatus

NorthernParula 9 9 0 1 2 0 0 1 3 0 0 1 Parulaamericana

Chestnut-sidedWarbler 0 0 0 2 0 0 0 0 0 0 0 0 DeMroicopensylvanica Black-throatedBlue Warbler* 29 40 36 2 30 20 36 20 6 2 16 0 Dendroicacaerulescens Yellow-rumpedWarbler 0 1 0 3 0 1 1 2 5 3 29 0 Dendroicacoranora

Palm Warbler 0 8 0 12 0 0 2 9 2 2 1 1 Dendroicopalmarum Rmerican Redstart 0 0 0 0 0 0 0 10 0 0 0 0 Seraphagoruticilla CommonYellowthroat 0 12 19 4 2 4 8 18 3 4 0 1 6eothlypistrichos ScarletTanager 0 0 2 0 0 0 0 0 0 0 0 0 Pirangaolivaceous SavannahSparrow 0 1 11 6 0 0 12 8 4 13 9 1 Passerculussandwichensis Swamp/Lincoln'sSpanow 0 0 0 0 0 0 0 1 0 0 0 0 Melospizageorgiana/lincolnii White-throatedSpanow 0 0 0 0 0 0 0 3 6 12 5 6 Zonotrichiaalbicollis IndigoBunting 0 3 0 0 0 0 0 3 0 0 0 0 Passe#hacyanea Zeepcomplex** 0 2 6 4 5 4 3 29 1 2 0 0 Speciesdetected acoustically 3 9 6 9 6 6 6 12 8 7 5 6 *Note:An iodwidual Black-throated BlueWarbler often gives two calls in succession, about a half-secondapart. In our analysis, wecounted such occurrences astwo calls. '•ln thiscase, most likely Blackpoll Warbler orConnecticut Warbler; see Evans and O'Brien (2002) for other possibilitie• minuteperiods on fivedifferent nights. thoughwith greatervariance due to a smaller beddedwithin the blueand greenlight tests As wouldbe expected,the averagecalling samplesize, was documented at the two ref- (Figure5B). rate in the first, second,third, etc. minuteso[ erencestations during the periodof thelight At ourlight study site, visual observations all ten-minuteperiods on significantmigra- study(Figure 5A) andin 16 ten-minutedark indicatedbirds were flying in all directions. tion nightsat the two referencestations re- periodsin thegreen light and flashingwhite Someflew past within a [ewmeters of ground vealedconsistent calling rates per minute light tests(Figure 5B). level, and somelanded nearby. Most birds (Figure5A). In otherwords, in any random But in 16 ten-minutelight periodswhen wereseen passing overhead through the light- ten-minuteperiod during a recordingperiod, aggregauonoccurred during the blue,green, ed space,or were heard callingabove the onewould not expectany specific m•nute to and flashingwhite light tests(nonflashing rangeof our visionin the doud and/ordriz- consistentlyhave more calling than another, whitelight periods), increased calling o[ birds zle. The numberof speciesdetected acousti- andthere would be no expectedtrend o[ call- typicallyoccurred within the first few min- callyin mostaggregation events was greater ing increaseor decreaseover multiple minutes,and the calling rate tended to increaseas than the maximum number of birds docu- utes.Data were considered during nights with a light periodprogressed. Calling terminated mentedvisually (Table 3; Figure 4). Most at least50 flight-callsper night from Septem- abruptlywhen lights were turned of[ (Figure birdsheard in aggregationevents were esti- ber to mid-October(Figure 5A). Sucha uni- 5B). No trendo[ increasingcalling occurred matedto be greaterthan 50 m fromthe light form minute-to-minute calling pattern, within 13 ten-minutered light periodsem- source.Most birds that were seen d•d not ap-

VOLUME 60 (2007) ß NUMBER 4 483 IRESPONSE OFNIGHT-MIGRATING SONGBIRDSINCLOUD TO COLORED ANDFLASHING LIGHT

pear to give vocalizationswhile in sight. ternsacross broad geographic regions (Evans ancelevels than red light. Our studyis the Speciescompositiofis of the aggregation and Mellinger1999; Evansand Rosenberg firstto systematicallycompare avian aggrega- eventswere typical nocturnal migrant passer- 2000). It is indicatedby radarstudies that tion tendencyin artificiallight of different •nes for the region.Table 3 presentsthe show target passagerate correlationwith wavelengths. acousticallydetermined species composition acousticdata (Larkin et al 2002; Evans,in for the aggregationperiods shown in Figure prep.),as well as by otherobservations that Mechanism(s)ofAggregation 4A-C. Two additionalspecies, not knownto showgross correspondence between the pres- Theoriesfor why birdsaggregate in artificial gweregular nocturnal flight calls, were visu- enceof migrantbirds and the flight-calling lighthave evolved with the paradigmof how ally identifiedwhen individual birds landed phenomenon(Odgen 1960; Avery et al. 1976). birdsnavigate during nocturnal migration, as •n thevicinity of thelight: Gray Catbird (Du- Figure5B indicatesunambiguously that, well aswith progressin understandingavian matellacarolinensis) and the Red-eyedVireo under certain weather conditions, acoustic sensorymechanisms. Current ideas can gen- (V•reoolivaceus). monitoringcan be an indicationof whether erallybe grouped into two categories. One in- Figure4E showsthe resultsof the white birdsare responding to artificiallight. The fact volyesthe avian light-dependent geomagnenc hghttest night. A fewblue and red light peri- thatour visualobservations of bird aggrega- sense,with artificiallight causing aggregation odswere alsotested on this night. The se- tion correspondwith the extremesin flight eitherdue to magnetoreceptiondisruption or quenceof light testsshown here illustrates callingduring the nonflashinglight periods becauseit providesa magnetoreceptionre- whatwas likely a declinein migrationpassage revealsthat acoustic monitoring was a reliable source.The other involvesavian vision, with rate duringthe courseof the night.Toward indexby itself for aggregation phenomenon in artificiallight causing aggregation by disrupt- the endof the night,a periodof whiteand a thoselight conditions. The weight of the evi- inga priorvision resource or by enablinga vt- periodof bluelight did not indicateeither vi- dencestrongly suggests that the lack of the be- sualrefuge. We discussour study results with sualor acousticactivity Careful inspection of havioralresponse of increasedflight calling respectto thesebasic ideas and the phenome- the darkperiod ca]ling rates indicates a drop duringthe flashingwhite light periodsindi- nonof birdaggregation around tail towers m callingrate during this time. catesa lack of bird aggregation.However, with aviationobstruction lighting. there is no substitute for an additional inde- Discussion pendentmeans of validatingany single-source Magnetoreception disruption theory Av•anflight-calling during aggregation peri- pattern.Certainly future work with thisstudy After the reportedconfirmation of light-de- odsceased nearly instantly when lights were methodwould benefit by theintegration of an pendentmagnetoreception in captive birds by turned off. This indicatesthat the lights independentmeans for continuouslyassess- Wiltschkoet al. (1993), the theoryemerged playeda directrole in causingflight-calling ingbird density during artificial lighting alter- thatbird aggregationin artificiallight might duringour aggregationphenomena. It also ations.The challengesof employingsuch an be causedby a "disruption"in the light-de- means that there were numbers of birds in the independentmeans are consideredabove, in pendentmagnetoreception mechanism that nearvicinity of our lightstudy site that were the Methods section. birdsuse for orientation(e.g., Gauthreaux not callingwhen the lightin theaggregation and Belser2006). The Wiltschkoeral. (1993) periodswas first turned off. In thisrespect, the Unexpectedresponse to nonflashing red light studyfound that after being kept in thedark, correspondencebetween calling rate and den- Severalstudies have reportedpronounced captivebirds could not orientin theseasonal- sayof flying birds is shown by our study to be avianflight-calling in associationwith appar- ly appropriatedirection when exposed solely h•ghlyvariable, making call rate potentially entbird aggregation at TV towerswith red avi- to red light, whereasbirds could orient well unreliableas an indicatorof bird density.But ation obstructionlighting (Cochran and when exposedto constantwhite, green,or therewas strong correspondence between the Graber1958; Ogden 1960; Taylor and Ander- bluelight. callingrate and visualobservations of flying son'1973; Avery et al. 1976).Ihere aremany Furthercaptive bird studieshave revealed b•rdsin nonflashingaggregation periods (Fig- suchunpublished accounts, and we havealso the complexityof the mechanismof light-in- ureA-E). This was not just thecase in theno- experiencedthis phenomenon (W. Evans,un- ducedmagnetoreception. Tests using higher aggregationperiods of red light and during the publ.data). We knowwithout doubt that red intensity levels of blue and green light aggregationperiods in blue,green, and white lightscan induce aggregation and that birds showedunique, often seasonally inappropri- hght(Figure 4A-E); it wasalso true in theno- maycall duringsuch aggregation events. Yet ate,"fixed-direction" responses (Wiltschko et aggregationperiods of blue and white light theirradiance level and spectrum of ourlights al. 2000; Wiltschko and Wiltschko 2001, during a time when it appearedthat active were very carefullymeasured, and the data Wiltschkoet al. 2003).Higher intensity levels b•rdmigration had ceased (Figure 4E). fromour study clearly indicate aggregation in of red andyellow light did not producethe Theavian flight-calling rate is influencedby blue,green, and white light--but not in red. fixed-directionresponses but caused what ap- theconjunction of theenvironmental variables Thepossible reasons for thisfinding are com- pearedto be the samelack of orientationas of cloudcover and artificial lighting, but it ap- plex and dependenton unknown mecha- lowerintensity levels of thesecolored lights parentlyhas elementsof consistencywhen nism(s)for aggregation,which are discussed (Wiltschkoand Wiltschko2001; Wiltschko et these variables remain constant. This is in moredetail in thefollowing sections. al. 2004b). demonstratedbythe shared pattern of increas- Our findingappears contrary to somepre- An additionalstudy has shown that comb•- ing ca]lingrate within periods of blue,green, vailingbeliefs that bird kills at tall towers nationsof monochromaticshort and long andwhite light in fourdifferent nights of our with red aviationobstruction lighting are wavelengthlight at the lowerintensity levels study(Figure 5B). It is shownby theconsis- specificallyinduced by thered nature of the used in the earlier studies also elicit the fixed- tent patternsof callingrate variationin our light.But our results may simply indicate that directionresponse (Wiltschko et al. 2004a) two controlstations (see Results) and by other for birdsmigrating in cloud,blue, green, or Thisis interestingbecause white light, which studiesthat revealconsistency in callingpat- whitelight cause aggregation at lowerirradi- hasa broadspectrum of shortand long wave-

484 NORTH AMERICAN BIRDS RESPONSEOFNIGHT-MIGRATING SONGBIRDSINCLOUD TO COLORED ANDFLASHING LIGHT1

lengths,enables functional orientation at the vironmentof the captivestudies. There are theirway because of weatherand "madefor low andhigh intensity levels (Wiltschko and alsovectorial, spectral, and quantitative differ- the lightsin absenceof any otherdirect •m- Wiltschko 1972; M611eret al. 2001). It has encesthat may be important variables as well pulse."However Clarke's personal view, based been theorized,therefore, that the unnatural asdifferences in motivationand behavior pri- on observationsof bird aggregationat two conditionof monochromaticlight may cause or to lightexposure (e.g., flying or not). lighthouses,was that migrants were actually an imbalancein themagnetoreception mech- "decoyedfrom or arrestedon theircourse by anismand a dysfunctionin the orientation Magnetoreception-seekingtheory theinfluence of thelight itself." system(Wiltschko et al. 2005). A moreconsistent explanation for our results In theUSA during the 1960s,vision-based All the evidencefrom captivebird studies with respectto the findingsof captivebird theoriesarose out of speculationabout the now suggeststhat naturalmagnetoreception studies arises if we assumethat natural light causeof massbird mortality events at TV tow- •s dependentnot only on shortwavelength levelsduring. our study were too low to enable ers and other lighted structures.Kemper hghtin theblue to greenrange but also on the magnetoreception.The lower thresholdof (1964) conveyedthe theorythat birdsthat intensityof thosewavelengths and the com- lightlevels necessary for magnetoreception in had lost their stellar reference due to cloud positionof otherwavelengths that arepres- birdsis unknown.While moonlight was covermight be attractedfrom afar by tower ent. Threetypes of responsesto light have tentiallya factorduring our study period, nat- lightsin somemisguided mechanism related been demonstratedwith captivebirds: sea- ural light levelswould have been very low to their stellarnavigation system. Herbert sonallyappropriate orientation, fixed-direc- nearground level due to a persistentlythick (1970)implied that bird aggregation could be nonresponses, and no orientation.The latter cloudlayer. Aggregation in our white,green, due to spatialdisorientation caused when ar- twoare generally grouped. as disorientation or andblue light periods might have occurred tificiallight obliterates any previous reference a disruptionin normalmagnetic orientation. becausebirds found the opportunity for reac- birds have for the horizon. Graber (1968) Thereare still many questions about light-in- tivatinglight-dependent magnetoreception proposed that birds are not attracted from afar ducedmagnetoreception, and this presents a and thentended to remainin, or returnto, the by thelights. Instead, bird aggregation events challengefor determining whether disruption lightedarea to continuegeomagnetic engage- arecomposed of birdswhose trajectories hap- of magnetoreceptionis responsible for bird ment.Since captive bird studiesindicate that pento intersectwith thelighted space, which aggregationin light and, if so,what the spe- redlight does not readilyenable orientation, is createdby therefraction of thetower lights cific mechanism is. thissuggests it does not readilyenable mag- offsmall water droplets of cloudor lightdriz- With strictrespect to the resultsof captive netoreceptionand would explain the lackof zle. Several later studies concurred w•th b•rdstudies, our datado not supportthe the- aggregationin thered light periods. Graber'sidea (Averyet al. 1976;Larkin and orythat the cause of aggregationin our study The utility of magnetoreceptionfor orien- Frase 1988). wasdisorientation from a light-induceddis- tationmay be instantly available to birdsonce While theremay be mechanismsof aggre- ruptionof magnetoreception.If so, we would activatedby light, but therecould be a de- gationthat involvebird attractionto distant nothave expected aggregation to occurin the layedutilization if birdshad been previously lightsources or fromloss of ,horizon,our ex- low lightlevels of our blueand green light, using anothercue such as wind direction. perimentswere not gearedto study such whichcaptive bird studies suggest would en- Anydelay during the process of cuetransfer mechanisms.The aggregationmechanism in- able orientation (Wiltschko et al. 1993; couldbe a factorcontributing to aggregation.volved in our studycould not haveinvolved Wiltschkoand Wiltschko 1999, 2001). How- If suchmagnetoreception-seeking behavior bird attractionfrom afar to point sourcesof ever,we wouldhave expected disorientation- is thecause for bird aggregation around lights lightnor could it havebeen due to spatial basedaggregation with ourred light, because in cloudyconditions, then the questionre- orientationcaused by lossof horizon.Due to red lighthas not beenshown to enablecap- mainswhy birds congregate around tall com- thegrounded cloud conditions and very hm- uvebirds to orientwithout a periodfor adapt- munications towers with red aviation ob- ited visibility,birds would not havehad any mg(Wiltschko et al. 1993,2004b). structionlighting? The red light results from visualreference to thelandscape at ourstudy Similarly,we wouldrule out thepossibility our studydo not correspondwith the evi- site.Whatever aggregation mechanism was at that aggregationin our greenand blue light dencefrom previousfield studiesin which workinvolved dark-adapted birds encounter- wasdue to disorientation caused by the fixed- redaviation obstruction lighting induced bird ing an anisotropicallyilluminated area. &rectionresponse. If thishad been the case, aggregation(Cochran and Graber1958; Av- Why,then, did birdstend to remainin the thenwe would not have expected aggregation eryet al. 1976;Gauthreaux and Belser 2006). vicinityof ourwhite, green, and blue lighted w•th our whitelight, because in captivebird A possibleexplanation is that disorienta- spacebut not thered? One possibility for the studieswhite light has not been shown to in- tion in red light occursonly if birdsare ac- lack of aggregationin the red light is that duceeither the fixed-directionresponse or tivelyusing magnetoreception and the red birds'night (scotopic) vision, relying on rod the "no orientation" mode of disorientation lightcreates an imbalancein the magnetore- cells, is much less sensitive to red wave- (Wiltschkoand Wiltschko 1972; M611er et al. ception mechanism as suggested by lengthsas compared to blueor green.The red 2001). Wiltschkoet al. (2005).The red lights in our lightwe testedhad three times the peak irra- A caveatin comparingour data with captive studymight not have triggered this imbalance dianceof the blue light and two timesthe b•rdstudies on light-inducedmagnetorecep- if, in fact,the birdswere not activelyusing peakirradiance of the greenlight. However, uon is that there are inherent environmental magnetoreception. when convolvedwith a spectralsensitivity and contextual differences between field stud- curvefor rhodopsin,arian sco•opic sensiuv•- •esand captivestudies. These differences in- Vision-inducedaggregation ty in the red wavelengthrange of our test cludeunknowns associated with ambient light Asnoted by Clarke (1912), the general idea in lightswas roughlysix timesless sensitive m the field studies and the fact that there was the early1900s was that bird aggregation at than the blue and 15 times less sensitive than no ambientlight in the controlledphotic en- lightswas due to migrantbirds that had lost thegreen light. Therefore, the red light levels

VOLUME 60 (2007) ß NUMBER 4 485 [RESPONSEOFNIGHT-MIGRATING SONGBIRDSINCLOUD TO COLORED ANDFLASHING LIGHT

m ourstudy could simply have been an insuf- tributeto visualperformance. Since the peak flashingobstruction lighting for aviationand ficient visual stimulus or resource for induc- sensitivityof rodsis at shorterwavelengths boating. For obvious reasons, migratory land- ing aggregationbehavior. thanthat of cones,it is expectedthat the peak birdresponse to artificiallights may be differ- Thisfinding does not concur with the well- sensitivityunder such mesopic light condi- ent at seathan over land, and any behavioral documentedphenomenon of birdaggregation tionswould be shiftedto longerwavelengths responseto lightsat seahas potentially im- at tall towers with red aviation obstruction as light levelsincrease. So as dark-adapted portantconservation implications for •the hghts.The peakirradiance of our red work migrantsencounter artificial light, at some speciesinvolved. hghtwas at leastthree times greater than that levelof increasingirradiance they would the- of themedium intensity red beacons typically oreticallybecome more sensitive to redlight. Conclusion usedfor markingtall towersin NorthAmeri- The aggregationphenomenon may involve Our studyshows that the colorof lightand ca A differencein ourred study light versus thephysiological subtleties of thisshift from whetherit is steady-burningor flashing suchred aviation obstruction lighting on tall rod-based to cone-based vision. To further in- makesa significantdifference in whether towers is that there are more sources of red vestigatevision-induced aggregation mecha- night-migratingbirds exhibit aggregation be- light on towers.But theseindividual light nisms,it will be importantto identifyhow havior.We find no evidencethat bird aggre- sourcesare separated in spaceas they mark avianmesopic vision works as a functionof gationoccurs because a light is red.While red sequentialtiers of a tower.The multiple lights lightlevels. lighthas been blamed for bird mortality at tall createa larger field of irradiancebut not TV towers,our study indicates that for birds greaterirradiance. If thereason birds did not No aggregationinfiashing light migratingwithin cloud cover, blue, green, or aggregatein our redlight was solely due to We found that when flashed,a continuous whitelight wouldbe morelikely to induce lower scotopicsensitivity, then morelights light sourcethat hadjust prior beeninduc- birdaggregation and associated mortality. should not make a difference. ing acousticaggregation behavior now The acousticdata provide strong circum- Theonly way for birds to encountergreater ceasedto do so. Night-migratingbirds may stantialevidence that flashing white light does irradiance from red aviation obstruction bea- needa continuoussource of light to achieve not inducebird aggregation.Our resultsin consthan from our red study light is if they functionalmagnetoreception or to use the thisregard correspond with thecircumstantial fly closerto suchtower lights. This is a likely light asa visualresource. However, the Gau- evidencethat no largekills havebeen docu- scenario because aviation obstruction bea- threauxand Belser(2006) study indicates mented at tall broadcast towers with white consare mounted well aboveground level on thatwhite strobes may have some affect on strobelighting at night (and with no other towers,they project their peak intensity hori- flight behaviorof night-migratingbirds. brightsources of lightingin theirvicinity). zontally,and some migrant birds would un- Theirstudy showed that birds flying in the Whileour study showed neither white nor doubtedlybe on a directcourse toward the vicinityof towers with multiple tiers of white redflashing light to inducebird aggregation, peakintensity vectors of thelights. That such strobelighting had significantly more non- the factthat our nonflashing red also .did not birdswould be the onesinduced to aggregate linearflight than birds flying at nearbycon- induceaggregation suggests that, with equal is consistentwith the theoryof aggregation trol sites without towers. But since the con- irradiance,flash on-time, and flash rate, a proposedby Graber(1968) and the radar ob- trol sitesin their studydid not havetower flashingred light would be lessof a stimulus servationsof Larkin and Frase (1988). structures,it is not clearin the datapresent- to migrantbirds than a flashingwhite light. The horizontal orientation of red obstruc- edin theirstudy whether the more nonlinear With regardto understanding,themecha- tionlights on towers versus the perpendicular flight was due to the white strobelights or nismof bird aggregationin artificiallight, in- orientationwith our studylights brings up fromsome birds altering their flight path to terpretationofour study results is challenging anotherpotential vision aggregation mecha- avoid collision with the tower structure. In because we lack information on what orienta- msm involvingvectorial differences (direc- thisregard, it is noteworthythat their study tion cuesbirds were using prior to intercept- tion and angulargradient) of light sources foundthat the ratesof passagedid not vary ing the influenceof our studylight. There •s discussedby Verheijen(1978, 1985).Vector significantlybetween the controlsites and also a lack of information on the threshold directionhas been demonstrated to be impor- white-strobed tower sites. sensitivityfor avianvision and for light-in- tant for seaturtle and amphibian orientation, Our study0nly involved one light source ducedmagnetoreception, anda lackof infor- and it has beenshown to be importantfor that flashed24 timesper minute, with a mationon the quantalflux of our lightas it birdsin horizonglow studies. But the extent longeron-time per flash(0.2 sec)than the dispersedthrough cloud. We do not know the to whichit impactsbirds migrating in cloudis typicalwhite strobe light used for aviation ob- lightlevels birds had available before encoun- unknown. structionmarking. We do not knowwhether teringour light. We donot know the light lev- Historically,birds migrating in themiddle ourlight had any affect of bird flight behavior. elsbirds first encountered that triggered their of thenight have been accustomed to a dorsal All we know is that it did not lead to an aggregationbehavior, and we do not know lightsource. The degree to whichthey can de- acousticindication of bird aggregation.Ex- howthe light level changed for birds as they tectsuch natural anisotropic light conditions perimentationisneeded with faster flash rates flewrepeatedly through the light field. in cloudis unknown,and this would proba- andlonger duration of individualflashes to Becauseof theseunknowns, our studyde- blydepend on cloudlayer thickness. We can- see if bird aggregationbehavior can be in- signand resulting behavioral data do not allow not rule out that bird aggregationmay have ducedwith otherparameters of flashinglight. usto distinguishbetween a visual or magneto- beencaused by theventral nature and/or the Thisis especiallyimportant with regard to the basedcause of aggregation.With respectto unnaturalangular gradient of our ground- pelagicmigration of landbirds.Proposals for captivebird studies, our data suggest that mag- basedlight sources. thousandsof offshorewind energyturbines netoreceptiondisruption was not the aggrega- At intermediate(mesopic) light levels, are in preparationfor U.S. coastalwaters. tion mechanismin our studyHowever, this both cones and rods in the avian retina con- These structures will have a combination of couldsimply be because birds were not relying

486 NORTH AMERICAN BIRDS RESPONSEOFNIGHT-MIGRATING SONGBIRDSINCLOUD TO COLORED ANDFLASHING LIGHT1

on magnetoreceptionin our study conditions. mentand many useful suggestions, andf'or Evans,W. R., andD. K. Mellinger.1999. Mon- It is likely thatno matterto whatextent the rhodopsinspectral sensitivity function. itoringGrassland Birds in NocturnalMigra- birdswere using magnetoreception or visual We extendspecial thanks to RobertBeason, tion.Studies in AvianBiology 19:219-229 resources,both these light-dependent sensory Ronald Larkin, JenniferJohnson, Louis R. Evans,W. R., and M. O'Brien.2002. Flight- systemswould be impactedby our artificial Bevier,Alvaro Jaramillo, and four anony- callsof MigratoryBirds--Eastern North hghtsources--at least in theblue, green, and mous reviewers for valuable comments on AmericanLandbirds. Ithaca, New York: Old white light periods.Aggregation behavior earlierversions of themanuscript. For edito- Bird, Inc. couldbe due to adaptationsto thenew stim- rial assistancewe thank Miranda Strichartz, Evans,W. R., and K. V..Rosenberg.2000 uli in bothsensory •ystems. Anne Klingensmith,and RobertKulik. An- AcousticMonitoring of Night-migrating Sortingbut the mechanism(s)of bird ag- drewBierman and Martin Overingtonfrom Birds:A ProgressReport. In: Strategiesfor gregationat artificiallight sources will require the Lighting ResearchCenter, Rensselaer bird conservation:The Partnersin Fhght additionallaboratory and field studies. While PolytechnicInstitute, made a valuablecon- planningprocess: Proceedings ofthe 3rd Part- themechanism of inducingaggregation isstill tribution to the light measurements.We nersin FlightWorkshop; 1995 October 1-5, not known, field studiessuch as ourscould would alsolike to thankGalaxy Litebeams CapeMay, NJ. (eds. R. Bonney,D. N. Pash- leadto practicalguidelines to reducethe bird for loan of the L-810 beacon and flash-rate ley,R.J. Cooper, and L. Niles),pp.151-159 impactof manyartificial lighting applica- controlbox. Finally,we wouldlike to thank ProceedingsRMRS-P-16. Ogden, UT: U S tions. William Cochran and Richard Graber for Departmentof Agriculture,Forest Service, With regardto aviationobstruction light- theirseminal research toward understanding RockyMountain Research Station. 281 p lng,two major variables appear to beinvolved the mechanismof bird aggregationaround Gauthreaux,S. A.,Jr., andC. G. Belser.2006 with bird aggregationat suchlights in dense towerswith aviationobstruction lighting. Effectsof artificialnight lighting on mi- cloudconditions: whether such light is flash- Our studywas supported by theSouth Flori- gratingbirds. In: EcologicalConsequences of lng or not andlight color. Our resultssuggest da WaterManagement District and through ArtificialNight Lighting. (eds. C. Richand thatany flashing parameters would cause less a grant administeredby the United States T. Longcore),pp. 67-93. Covelo,Califor- bird aggregationthan continuous lighting. It Fish& WildlifeService (NMBCA grant #NY- nia: Island Press. is likdy thatthe longer the dark duration be- N3R1). Goldsmith,T. H., andB. K. Butler.2005. Col- tween flashes and the shorter the on-time of a or visionof thebudgerigar (Melopsittacus flash,the less impact there would be onnight Literature cited undulatus):hue matches,tetrachromacy, migratingbirds. With regardto color,night Avery,M. L., P. E Springer,and J. E Cassel. and intensitydiscrimination. Journal of migratingbirds migrating in doud appearto 1976. The effects of a tall tower on noctur- ComparativePhysiology A 191:933-951 be lessresponsive to the red spectrumcur- nal bird migration--aportable cellometer Graber,R. R. 1968.Nocturnal migration in rentlyspecified for useby the FAAin L-864 study,Auk 93: 281-291. Illinois--Differentpoints of view. Wilson mediumintensity obstruction lighting than Avery,M. L., P.E Springer,and N. S. Dailey. Bulletin 80: 36-71. lightconsisting of, or containing,substantial 1980. AvianMortality at Man-madeStruc- Herbert,A.D. 1970.Spatial disorientation m amountsof shorterwavelength light (e.g., tures:an annotatedbibliography (revised). birds. Wilson Bulletin 82: 400-419. whitestrobe lighting). U.S. Fish & Wildlife Service,Biological Johnson,J. E. 2005. Marineradar study of Two typesof red flashinglights are cur- ServicesProgram, National Power Plant nocturnalmigrants near TV towersin rentlyin widespreadoperation for aviation Team,FWS/OBS-80/54. Washington, DC: Phfiadelphia,PA, USA. Report to theMeet- obstructionmarking: the L-864/865 incan- U.S.Government printing office. ing of the ResearchSubcommittee, Com- descent and xenon flashtube varieties. In two Banks,R. C. 1979.Human-related Mortality of munications Tower Working Group suchlights we testedthat were purchased Birds in the United States. United States De- PatuxentWildlife Refuge. April 21, 2005 from TWR Lighting(Houston, Texas), each partmentof theInterior, Special Scientific Kemper,C. 1964.A towerfor TV, 30,000 dead had a one-second flash on-time. This con- Report--WildlifeNo. 215. Washington, birds.Audubon Magazine 66: 86-90. trastswith the moreinstantaneous type flash DC:U.S. Government printing office. --. 1996. A studyof bird mortalityat a of theFAA-approved white strobes. Our study Brinkley,E. S. 2006.Editors' Notebook. North west-central Wisconsin TV tower from suggeststhat the red flashinglights have a American Birds 60: 194. 1957-1995.Passenger Pigeon 58:219-235 safercolor for birds but a potentiallyless safe Bull,J. L. 1998.Bullk Birds of New York State. Larkin, R. P, and B. A. Frase.1988. Circular (longer) on-time per cycle.White strobe Ithaca,New York: Cornell University Press. pathsof birdsflying near a broadcasting hghting,on theother hand, has a lesssafe col- Clarke,W. E. 1912.Studies in'Bird Migration. towerin cloud.Journal of Comparative Psy- or for birdsbut a potentiallysafer (shorter) VolumesI, II. London:Gurney & Jackson. chology102: 90-93. flashon-time per cycle. Determining the rela- Cochran,W. W., and R. R. Graber. 1958. At- Larkin, R. P, V• R. Evans,and R. H. Diehl tiveimportance of thesevariables for causing tractionof nocturnalmigrants by lightson 2002. Nocturnalflight calls of Dickcissels birdaggregation will requireadditional study. a television tower. Wilson Bulletin 70: 378- andDoppler radar echoes Over south Texas We look forward to further research into the 380. in spring.Journal of FieldOrnithology 73 parametersof wavelengthand flashrate of Dinsmore,S.J., and A. Farnsworth.2006. The 2-8. lightstoward reducing impact to night-mi- ChangingSeasons: Weatherbirds. North Lednor,A.J. 1982.Magnetic navigation in pi- gratingbirds. American Birds 60: 14-26. geons:Possibilities and Programs. In: Awan Emlen,S. T. 1967.Migratory orientation in Navigation.(eds. E Papiand H. G. Wall- Acknowledgments the indigobunting, Passeriha cyanea. Part raft),pp. 109-119.Berlin: Springer-Verlag We arein debtto TimothyGoldsmith for re- I: Evidence for use of celestial cues.Auk 84: M611er,A., M. Gesson,C. Noll,J. B. Phillips, viewingour results,providing encourage- 309-342. R. Wiltschko, and W. Wiltschko. 2001

VOLUME 60 (2007) NUMBER 4 487 IRESPONSE OFNIGHT-MIGRATING SONGBIRDSINCLOUD TO COLORED ANDFLASHING LIGHT

Light-dependentmagnetoreception in mi- Sauer,E.G. E 1957. Die Sternenorientierung hal of ComparativePhysiology A 184:295- gratorybirds: previousexposure to red nachtlich-ziehenderGrasmucken, Sylvia 299. lightalters response of redlight. In: Orien- atricapilla,brain and currca Zcitschrift ]fir .2001. Light-dependentmagnetorecep- tationand Navigation:Birds, Humans and Tierpsychologic14: 20-70. tion in birds:the behaviourof European otherAnimals, pp. 61-66. Oxford: Royal In- Taylor,W. K., andB. H. Anderson.1973. Noc- robins, Erithacus rubecula, under mono- stituteof Navigation. turnalmigrants killed at a centralFlorida chromaticlight of variouswavelengths and Moller,A., S. Sagasset,W. Wihschkoand B. TV tower; autumns 1969-197 I. WilsonBul- intensities.Journal of ExperimentalBiology Schierwater.2004. Retinal cryptochrome in letin 85: 42-51. 204: 3295-3302. a migratorypassefine bird: a possibletrans- Thalau,P, T. Ritz, K. btapput,R. Wiltschko, Wiltschko, W., U. Munro, H. Ford, and R. ducer for the avian magneticcompass. and W. Wihschko.2005. Magneticcom- Wihschko.1993. Red light disruptsmag- Naturwissenschaften91: 585-588. passorientation of migratorybirds in the neticorientation of migratorybirds Nature Mouritsen,H., U. Janssen-Bienhold,M. Lied- presenceof a 1.315 MHz oscillatingfield. 364: 525-527. vogel,G. Feenders,J. Stalleicken,E Dirks, Naturwissenschaften92: 86-90. Wihschko, W., R. Wiltschko, and U. Munro. and R. Weiler.200't. Cryptochromesand Verheijen.F J. 1985.Photopollution: artificial 2000. Light-dependentmagnetoreception neurona[-activit)markers coloca[ize in the light opticspatial control systems fail to in birds:the effectof intensityof 565-nm retinaof migratorybirds during magnetic copewith. Incidents,causations, remedies. greenlight. Naturwissenschaften87: 366- orientation.Proceedings of the National ExperimentalBiology 44: 1-18. 369 AcadenLvof SciencesU.S.A. I01: 1'1294- Weir, R. D. 1976. AnnotatedBibliography oJ Wihschko, W., U. Munro, H. Ford, and R. 14299. BirdKills at Man-madeObstacles: a review oJ Wihschko.2003. Magnetic orientation in Ogden,J. 1960.Observations at a T.V.tower thestate oJ thc art andsolutions. Department birds: non-compassresponses under duringa bird fall.Migrant 31:65-67 of Fisheries and the Environment, Envi- monochromaticlight of increasedintensity. Palacios,A.G., and 32 H. Goldsmith. 1993. ronmentalManagement Service, Canadian Proceedingsof the Royal Society of London Photocurrentsin retinal rods of pigeons Wildlife Service,Ontario Region,Ottawa. 270: 2133-2140. (Columba/ivia):kinetics and spectral sensi- Wiltschko,R., T. Ritz, K. Stapput,P Thalau, Wihschko,W., M. Gesson,K. Stapput,and R. tivity.Journal of Physiology(London) 471: and W. Wihschko_ 2005. Two different Wihschko.2004a_ Light-dependent mag- 817-829. typesof light-dependentresponses to magnetoreceptionin birds: interactionof at Ritz, T., S. Adem, and K. Schuhen.2000. A netic fieldsin birds.Current Biology 15: least two differentreceptors. Naturwis- modelfor photoreceptor-basedmagnetore- 1518-1523. senschaften91: 130-134. ceptionin birds.Biophysical Journal 78: Wihschko,W., andR. Wiltschko.1972. Mag- Wihschko, W., A. M611er,M. Gesson,C. Noll, 707-718. neticcompass of Europeanrobins. Science and R. Wihschko.2004b. Light-dependent Ritz,T., P Thalau,J. B. Phillips,R. Wihschko, 176: 62-64. magnetoreceptionin birds: analysis of the and W. Wihschko. 2004. Resonance effects . 1999. The effectof yellowand blue behaviourunder red light after pre-expo- indicatea radical-pairmechanism for avian light on magneticcompass orientation in sureto redlight. Journal of Experimental Bi- magneticcompass. Nature 429: 177-180. Europeanrobins, Erithacus rubecula. Jour- ology207:1193-1202. •

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488 NORTH AMERICAN BIRDS