The Display Behavior of the Gull-Billed Tern

j. Vield Ornithol., 52(3):191-209

THE DISPLAY BEHAVIOR OF THE GULL-BILLED TERN

By HAROLD F. SEARS

The displaybehavior of the Gull-billedTern (Gelochelidonnilotica) has not been describedin detail, although Lind (1963) discussesmany of the displaysof a Danish population. In this paper, I discussthe form, variation, function, and taxonomicimplications of displaysobserved during the breedingseason.

STUDY AREA AND METHODS This studywas done from March to July, 1971 to 1973, on an un- named island 0.5 km S of the port at Morehead City, Carteret Co., North Carolina(34.7øN lat., 76.7øWlong.). The siteis describedfurther in Sears (1978). I made observationsfrom exposed positionsearly each seasonand from blinds after colonyestablishment. Periodically I photographedbe- haviorswith a Braun-Nizo S-80 camera and super-8 film at 18 frames per sec,and recordedvocalizations with an Uher 4000 Report L tape recorderand M514 microphoneat a tape speedof 19 cm per sec.A few recordingswere made at a distancewith a Dan GibsonElectronic Par- abolicMicrophone. All recordingswere spectrographicallyanalyzed on a Kay Elemetrics Corporation Sona-Graph, model 7029A, using the wide band filter. To obtain data unbiasedwith respectto temporal parameters,I tape- recordeddescriptions of socialinteractions at severalsites for predeter- mined periodsof time (Sears1976). I tentativelydefined as independent those sequencesof behavior separatedfrom each other by over 15 sec of non-display(cf. Nelson1964, Rades•iter1975), and I workedwithin these sequencesto determine the minimum period of time between independentbehaviors. I measuredthe interval from the termination of the initial behavior in each sequenceto the initiation of each subse- quent behaviorof that sequence.Each resultingdatum consistedof a "precedingbehavior" (the initial behaviorof eachsequence), a "following behavior,"and the interveninginterval. For each interval class(10, 15, 20, 25, 30, 35, 40, 45 sec), the associateddata are independent, drawn from independentsequences, and eachof thesedata subsetscan thereforebe analyzedby chi-squarefor statisticalindependence between the variables,preceding and following behavior (analysesperformed using IBM 360 computerand programsfrom Nie et al. 1970). I found behaviorsseparated by 10 secto be clearlystatistically dependent upon eachother, but there wasno indicationof dependencewhere the interval was greater; thus, adjacentbehaviors are statisticallyassociated and a seriesof suchbehaviors both preceededand followedby over 15 sec of rest posturecan be referred to as an independentsequence. To identify associationswithin theseindependent sequences, I tallied eachtransition according to its precedingand followingbehaviors (Fig.

191 192] H.F. Sears J.Field Ornithol. Summer 1981

1). I then compared, using chi-squareanalysis, the relative occurrence of each followingbehavior in the presenceof each precedingbehavior with its relative occurrencein the absenceof that precedingbehavior (Table 1). Finally, the data are too few to permit the study of many transitions,therefore I repeatedthis analysisusing more generalcate- goriesof behaviors(Fig. 2, Table 2). The entire sequenceanalysis and the resultingpicture of the temporal organizationof Gull-billedTern displaybehavior is unbiasedonly to the degree that the data are independent of one another. To test the un- biasednature of this sequenceanalysis, I repeated it using an independent subsetof the data, consistingof the first transition of each independent sequence(n = 428). This revealed only 2 differences that cannotbe explainedby the smallsize of the independentsubset or by the early positionin the sequenceoccupied by all membersof the independent subset(Table 1).

AERIAL DISPLAY The terns that first arrive in the colony area do not appear to be paired, they avoid contactwith one another and with the future colony sites,and the first interactionsseen are aerial interactions.First, groups of up to 6 or 8 terns fly about the colony area. The leader seemsto vocalize more than the followers and sometimes carries food in its bill. Over the courseof a few days,these group flightsgive way to paired flights,and finally, pairsposture more and more on the groundand on colonysites. The followingpatterns are thoseI've observedin the air. V-flying.--The tern flies slowly at a relatively low altitude, its wings moving from about 45ø abovehorizontal to horizontal. Aerial bent.--The tern glideswith its wingsheld stationaryin a v-position over its back, each 45o-60 ø above horizontal, and its head bent downward so that the head and bill form an angle as great as 90ø with respectto the body. Aerialstraight.--The tern glides,wings motionless, with the body and head in line or slightlybowed, head and tail slightlylower than the center of the back, and the wingsas much as 30ø below horizontal. Swaying.--The tern precedesits partner and flies back and forth acrossthe relativelysmooth course of the secondtern. The aerial bent, aerial straight,and swayingall occur in the contextof paired flight. Hairpin course.--Twoor 3 terns flying togetherfrequently fly a hairpin-shapedcourse 100-200 m long. They fly straight, turn 180ø, and continue in this manner back and forth, the same individual leading throughout the flight. Simplepass.--The followingtern overtakesthe leader and flies past, either above, below, or to one side of the leader. The performance of a simplepass almost always results in the former leader initiatinga turn and again precedingthe other along the other sideof a hairpin course (21/23 observations).In addition to theserelatively stereotyped interactions, many brief encountersoccurred in which a tern flew along and a Vol. 52, No. 3 Gull-billedTern Display [193

HERD LANDING BENT ß

ß ß

MOUNT '",, UP W/TURN ...... •FORWARD W/TURN

MQUNTED (MALE) DOWN' •-FOR VyAR D f '.. \•, ? /' \

I '"'".. \\'"', .-"'"' / \\ • % \,, ..' / x. COPULATEDISMOUNT \ ',..-" • ...,,,F•._Y

..." . \', 1..- HEADTOSS-'""'Z-'""-.;,REST•. LAND

B•Et•T / / ",,' I! ',", HUNCHED / " I ß I / ,' I ', I // " I " • • ,,' I ',,

SCRAPEß ,," OBLIQUE• ...... ;.ATTACK ß ß

NEST FIOUREl. Sequential associationswithin the behavior of the Gull-billed Tern. Short dashesindicate that ! 0-I 9 transitionsbetween the behaviorswere tallied. Long dashes indicate 20-29 transitions. A solid line indicates 30 or more transitions. (n = !296). secondtern swoopedpast. Usually, the secondtern made a few passes, the first did not react,and the 2 ternsthen separated. Complexpass.--The followingtern overtakesthe leader and glidespast in the aerial straight;the tern beingpassed performs the aerialbent. At the point of closestpassage, the wings reach the highestin the aerial bent and the lowestin the aerial straight. Arc soar.--Both terns assumethe aerial straight posture and glide togetherin a wide levelarc, usuallyat a high altitude.One is positioned above,to the side,and within a few body widthsof the other. Most aerial interactionsare relativelysimple, involving paired flight and sometimesthe simple passor hairpin course (104/128). I saw the 194] H. F. Sears J. F•eld Ornithol. Summer 1981

LANDING BENT I I I MAPLECOP'•...... •?•R iT ,.FE M'A •E COP

BE NT•.---

I I / S•CRAPE•// AGGRESSIVE

FIGURE2. Sequentialassociations among broad categoriesof behavior.See Fig. 1 for key. morecomplex patterns only a few times.I sawv-flying and swayingonly once.

TERRESTRIAL DISPLAY Oblique.--Thecharacteristic structural features of this postureare abduction of the wings,extension of the neck, and direction of the bill toward an intruder. The degree of abductionand of extensionvaries little, but the orientationof the neck rangesfrom almostvertically upward ("high" oblique) to horizontal ("low" oblique).The oblique is almostalways accompanied by the ackor rattle callor by the gape(below), and it (especiallythe low oblique)is associatedwith approachand with attack(Figs. 1, 2). The Gull-billedTern attackswith its bill and feet. Crouch.--Thebody is horizontal,and the head is withdrawn closeto the shoulders.The crouchis not performedoften, but it occasionally occursin associationwith the obliqueand attack. Gape.--The bill is held open silentlyfor at leasta secondor 2 and is orientedtoward the intruder. The gape is associatedwith the oblique and with the ack, the latter associationusually taking the form of oc- casionalcalls emanating from a continuouslyopen bill. Head toss.--Thehead is rotated as high as verticallyupward and is then droppedto itsoriginal position. It is usuallyperformed a few times in quick succession,and it can be performed in a normal standingposition,in the erect,or in the bent (seebelow). Often, the tern givesack- chirupcalls (below), and sucha performanceelicits erect posturing from nearbyterns; occasionally, the head tossprecedes attack. Vol.b2, No. • Gull-billedTer•t Di,•play [ 195

Sleekedupright.--The neck is extendedvertically upward, and the bill is horizontal. The feathers of the neck are sleeked,and the wings are held tightly against the body. In this posture, the tern often looks around sharplywith the eyelidsunusually wide open in reactionto dis- turbancecaused by, for instance,an airplane flying overheador other terns fighting nearby. Footlook.--Thismovement is usuallyperformed in a normal standing posture.It consistsof a singlerotation of the head down and up. Like the sleekedupright, the footlookoccurs relatively rarely and in contexts that are probablymildly disturbing. Landingbent.--This is a distinctivemanner of landing. During the final few metersof descentand briefly after alighting,the tern partially extendsits neck and pointsits bill downward. The landing bent occurs when a tern lands near another individual prior to a courtshipinteraction, a nest exchange,or feeding a chick. It is almostalways immediately followed by either the forward-erector up-erect (below) (Figs. 1, 2, Table 2). Head nod.--The head nod is a distinctivemanner of taking flight. During the secondor so immediatelyfollowing liftoff, the tern rotates its bill downward, sometimesto a vertical position, and immediately raisesit. The head nod is performed after courtshipinteractions involving the erect, bent, or courtshipfeeding (seebelow). A tern also frequentlyhead nods after feeding one of its chicks.In the courtship context, a tern often followed one that had just performed the head nod, but there was no apparent responsein the nestingcontext. Erect.--This displayconsists of near verticalextension of the neckand abductionand sometimesdrooping of the wings.The bill is either horizontal, pointed almostvertically upward, or pointed ahnostvertically downward.Thus, 3 erect posturescan be distinguished:the forward- erect, the up-erect, and the down-erect.These categoriesintergrade with one another (Fig. 3), and particularlyin the forward-erect,intention movementsto sideways-throw(Sears 1978), to incubate,and to fly seemto affect the orientationof the neck, and a tendencyto fly sometimes increasesthe degree of wing abduction.The intermediateerect posturesare assumedand held, however;they are not simplydynamic transitions. The erectpostures, particularly the forward-erect,are the mostcommon in the species'repertoire. In large part, terrestrial courtshipcon- sistsof eachtern walkingabout the other, walkinga few stepsaway, and returning. The down-erectis performed during theseapproaches. The down-erectis also performed during the male precopulatoryherding display(Fig. 1), when the male approachesprior to mounting(below). The up-erectis characteristicallyassociated with the initial approachof a tern toward another. A tern lands near another or walks toward another and then performs the up-erect (Fig. 1). In contrast,a tern in the forward-erectis relativelyinactive. Headtilt.--This displayconsists of a singlerotation of the head to one 196] H. F. Sears j. Field Ornithol. Summer 1981

90 • •

oblique

sl.

erect

90 ø down I I 0 ø 45 ø 90 ø up

NECK ORIENTATION

FIGURE3. Variation in bill and neck orientation in the oblique, sleekedupright, and erect postures.Each of the 3 shadedareas indicates the range of variationin the 2 parametersfor that posture.Note the degree to which the forms of thesepostures overlap one another. Vol.22, •o. • Gull-billedTern Diaplay [ 197

side on the long axis of the bill. A tern head tilts only when laterally orientedwith respectto its partner, alwaysaway from the partner, and only in the forward- or down-erect.Its partner performs the erect and sometimes head tilts also. Headturning.--This displayconsists of rapid rotationof the headback and forth on the long axis of the neck. Head turning occursonly in associationwith the erect, usuallythe up-erect,but sometimesthe forward-erect.It is performed when one tern hasjust approachedanother or when it hasjust been approached. The associationbetween head turning and the erect is so closethat the erect displaycould be said to contain 3 major members:the down- erect, the forward-erect,and the up-erectwith head turning, the forward-erectwith head turning being a dynamictransitional form (Table 1, Fig. 1). These 3 posturestend to occupyunique positionswithin any bout of socialbehavior (a sequenceuninterrupted by performanceof the rest posture).Thus, the down-erectoften beginsa bout but rarely endsone, the forward-erectoften beginsa bout but is very likely to end it as well, and the up-erectwith head turning neither beginsnor ends such a bout (Table 1). Courtshipfeeding.--Food items ranging in size from lessthan 1 cm (insects)to several cm (lizards, crabs, and fish) are carried in the bill, and usuallythe erect or bent is performed. The tern presentsthe food to its partner, repeatsthe erect, and often herds its partner (below); however,courtship feeding rarely leads to copulation,and it is rarely performed after the eggs are laid. The tern being fed performs the hunched and whine (below). Bent.--The body is approximatelyhorizontal, the wings are slightly abducted,the tail is oriented anywhere from horizontal to vertically upward, and the bill is pointed as far as verticallydownward. This is similar to the postureadopted as a tern entersthe nestor as it feedsits mate or chick.The bent is frequentlyaccompanied by the murmur; it is alsoassociated with the erectand scrape(Figs. 1, 2). The tern'spartner performsthe erect, bent or scrape. Scrape.--Thetern drops forward from a standingposition onto its breastand extendedneck. The hindbodyand tail are high, and the legs are kept extended. Often the tern kickssand back with alternate move- ments of its feet. The tern may stand, turn, and repeat the scrapein the samespot, thus creatinga depressionin the sand. Unlike the bent, the scrapeis rarely the first displayperformed in an interaction.The scrapeis associatedwith the bent (Figs. 1, 2), and the tern's partner performsthe erect, bent, or scrape. Hunched.--The tail, body, head, and bill are all approximatelyhorizontal. The head is withdrawn toward the body, the wingsare slightly abducted,and the backis humped.Young ternsbeg for food in a posture very similarto the hunched.The hunchedis usuallyaccompanied by the whine (below). The performer's partner performs the erect; sometimesthe partner also feeds or herds and mounts. 198] H. F. Sears J. Field Ornithol. Summer 1981

o I

• • +o

01ilO + ++101 o I

o oo + oo i

oo+ool + i +o+ o I I Vol. 5•, No. 3 Gull-billedTern Display [ 199

TABLE 2. Chi-squareanalysis of transitionfrequencies between broad categoriesof behavior in the Gull-billed Tern.*

Following Aggres- Landing Female Male Preceding Rest s•ve bent Erect Bent Scrape cop cop

Rest O O O + + - Aggressive ¸ + - ¸ - Landing bent - + Erect O - + .... Bent + O - O - Scrape + - + Female cop ¸ ¸ Male cop .... +

* Transitionfrequency is greaterthan (+), lessthan (-), or equal to (0) that expected if variablesare independent(P < 0.05, df -- 1, n -- 1296). The broad categoriesof be- haviorsused are defined as follows:"rest" -- rest, head toss,land, head nod, fly, and nest material handling; "aggressive"= oblique and attack; "erect" = down-erect,forward- erect, forward-erect with head turning, up-erect, and up-erect with head turning; "bent" = bent and bent with head toss;"female cop" = hunched and mounted (9); and "male cop" = herding, mount, mounted (•), copulate,and dismount (see also Table 1 footnote).

Headjerk.--The head jerk is a small upward tossof the head. In its orientationtoward the partner'sbill, the headjerk is similarto the grab- bing of food during a courtshipinteraction, and these2 behaviorssome- times occur together in the same interaction.The head jerk is performed in the hunched posture,and it seemsalways to be accompanied by simultaneousperformance of the whine (below). Herding.--The presumedmale standsat one side of the presumed female, oriented perpendicularlyto her, and he pusheswith his breast againsther side.The female may move, whereuponthe male maintains contact,and thus appearsto herd the female about the immediatearea. Herding is performed in an erect posture, and the bill tends to be oriented downward.The male particularlytends to lower his bill when his partner whines or head jerks and to raise it somewhatafter such a performance.Herding is often followedby mounting.The female almostalways performs the hunched,the whine, and the headjerk. Copulation.--Themale mountsfrom the rear, positionshimself above the female'slegs and parallel to her body, and standson his feet or rarely on the length of his tarsometatarsus.He abductshis wingsslightly and orientshis bill towardsthe female'scap or bill. About half of all mountingslead to attempted copulation(Fig. 1). The male wagshis tail from sideto side and then againstthe edge of the female'stail. The female raisesher tail and lowers her forebody. The male then lowers and rotates his tail to make cloacal contact. He keepshis head low and bill orienteddownward during this process,and 5>00] H.F. Sears J.Field Ornithol. Summer 1981

__ c d e

I I 0.1

FIGURE4. The vocal displaysof the Gull-billed Tern. (a) grack, (b) rattle call and 2 isolatedrattle notes(the vocalizationsof a chickare alsopresent), (c) a portion of an intermittent performanceof the murmur that lastedfor severalminutes, (d) whine, (e) ack triplet, (f) chirup,(g) chipquadruplet, (h) vocalizationsgiven by a tern as it landed and fed its mate. They soundedlike "slurred ack calls,"and their graphic representationdoes suggest3 clustersof ack notes. However, the bimodal nature of the secondnote and of the final doubletof eachcluster suggests the chirup,as does the temporal relationshipbetween the first and secondnotes of each cluster. he often attemptscopulation several times, with long pauses(up to several minutes)before each,before dismounting.I could not judge the successof these copulation attempts. Following dismount, the terns sometimesperform the obliqueor forward-erect,but usuallythey do not displayfurther. Vol.52, No. • Gull-billedTern Di. splay [201

VOCAL DISPLAY Grack.--This harsh call (Fig. 4a) is relativelyvariable in both duration (2 = 0.15 sec, s = 0.048, n = 41) and internal structure. The most dis- tinctivefeature is the initial noisecomponent that givesthe call its harsh quality. Though the grackappears to be distinctfrom the acknote (seebelow), the 2 vocalizationsare clearly related (compareFig. 4a and 4e). The mostconspicuous difference between them is the lack of the noisecomponent in the ack; the ack note also tends to be shorter than the grack (below).Frequently a grackcall is immediatelyfollowed by a seriesof acknotes. These grackcalls are significantlyshorter and therefore more similar to the ack (2 = 0.12 sec) than those more temporally isolated from other vocalizations(2 = 0.17 sec) (t -- -4.54, df -- 34, P < 0.001). The grackis uttered at the low point of an aggressivestoop, directed at suchpredators as dogsor humans.It is not usedduring interactions between conspecifics,nor is it used against flying intruders. The re- sponseof an intruder to the stoopand grackis almostinvariably retreat. Rattle.--This vocalization(Fig. 4b) consistsof a variablenumber of quicklyrepeated notes, each of short duration and similar form. I have heard callsonly 1 or 2 notesin length and others 20 or 30 times that long. The rate of delivery averages15.5 notes per sec (s = 2.88, n -- 25). These 2 variables,duration of the call and rate of delivery, are significantlycorrelated (r = 0.568, df = 23, P < 0.01). The rattle is associated with both attack and threat behaviors. A standing or incubatingtern sometimesrattles at an approachingtern, gull, or similar intruder, and the rattle is often used during rapid aerial pursuit.This contextdiffers markedlyfrom that of the grack,where the fbcusof the disturbancetends to be larger and probablymore intimidating. The rattle alsoelicits retreat. Murmur.--This is a chatteringcall of extremelyvariable duration composedof a seriesof short soft notes (Fig. 4c). Performancessometimes last for severalminutes of almostconstant calling. The rate of delivery averages13.4 notesper sec(s = 1.54, n = 32). Consideringthe context of the murmur (below), its form is surprisinglysimilar to that of the rattle. The notes of the murmur are softer than the notes of the rattle, this smalleramount of energy is concentratedin lower frequencies,and there is no harsh noisecomponent in the murmur. The murmur occursprimarily in associationwith the bent, the scrape, and incubationand brooding behavior. During its performance,the tern's mate often performs the murmur, bent, or scrape,or a chick pushesunder the performer, but this is not clearly in responseto the call. The murmur often appearsto be a responseto the behaviorof the mate or chick. Whine.--This call (Fig. 4d) consistsof a single, soft, nasal note of relativelylong duration (about0.3 sec).The central portion of the call is characteristicallyless intense than the beginningor end. The whine is closelyassociated with the hunched and with the headjerk and there- 202] H. F. Sears J. Field OrnithoL Summer 1981

TABLE 3. Durations of notesand rates of delivery in the ack call.

Mean Duration Rate (seconds +_ 1 SD) (notes/s+ n Note 1 Note 2 Note 3 Note 4 1 SD)

Singlet 35 0.09 -+ 0.022 Doublet 24 0.08 _+ 0.023 0.07 _+ 0.021 8.7 _+ 1.58 Triplet 28 0.08 _+ 0.013 0.08 _+ 0.022 0.07 -+ 0.019 8.8 _+ 1.45 Quadruplet 10 0.06 _+ 0.026 0.07 -+ 0.011 0.06 _+ 0.007 0.06 _+ 0.009 10.2 -+ 0.82

fore with interactionsinvolving courtship feeding or mounting (see above). Ack,chirup, and chip.--The ack callsare a family of callswhich have as their commonelement the sharp acknote. The ackcalls are quickly repeatedseries of thesenotes varying in length from 1 to 4 or more notes(Fig. 4e, Table 3). The chirup(Fig. 4f) consistsof a singlebimodal note (duration= 0.16 sec,s = 0.009, n = 70), usuallygiven at a lower intensitythan the ack.The chip(Fig. 4g) is similar in form to the ack, but composedof shorternotes (0.03 and 0.07 secrespectively) delivered more rapidly (about 11.5 notes/sec). Many vocalizationshave features of both the ackand chirup,and they are hard to characterizeeither by ear or by eye (usingsonograms) (Fig. 4h). For this reason, I consider these vocalizationsto be members of an ack-chirupcomplex of calls.This complexincludes the ack,the chirup, the chip,and the individualcomponents of thesecalls, which can occur in atypicalcombinations. The ack and chirupare the mostcommon of all the callsof the Gull- billedTern, occurringin almostevery type of interactionobserved. The chirupis particularlyassociated with the nest, being almostinvariably givenas a tern landsat the nestand the incubatingmember of the pair often calling in return. In contrast,the ack is associatedmore with the oblique, attack, sleekedupright, and other reactionsto disturbance. There seemsto be a correlationbetween the lengthof the ackcall and the degree of disturbanceto the tern. The grackand the longer ack series(quadruplets and longer)were given more often in reactionto my presencewithin a colonythan elsewhereon the island (X2 -- 5.07, df = 1, P < 0.05 andX 2 = 29.5, df = 1, P < 0.001).Ack triplets and ackdou- bletswere given more often at a distancefrom the colonies(X z = 7.19, df = 1, P < 0.01 and Xz = 9.44, df = 1, P < 0.01). The chipis alsoassociated with disturbances,particularly at the nest.

DISCUSSION In an observationalstudy, generalizations regarding the physiological control, adaptivevalue, and evolution of displaysmust be basedon indirect evidence. This evidence comes from consideration of the form Vol.52, No. 3 Gull-billedTern Display [203 of the display,the behaviorstemporally associated with the display,in- cludingresponses given, the contextsin whichthe displayoccurs, and comparisonswith other species(e.g., Tinbergen 1959, Blurton Jones 1968, Cracraft 1972, Cullen 1972, McKinney1978). Aerialdisplay.--Early in the breedingseason, it is likely that the arriv- ing ternsare unwillingto makecontact with one anotheron the colony site and that the aerial displaysfacilitate the pairing up of individuals. A striking aspectof aerial displayin the Gull-billedTern is the infre- quencywith whichthe more ritualizedcomponents are performed.At the sametime, I havenoticed that the Gull-billedTern engagesin con- siderablymore terrestrialdisplay early in the seasonthan doesthe Com- mon Tern (Sternahirundo). The evolutionof the Gull-billedTern might haveinvolved a shiftin emphasisfrom earlyaerial to terrestrialdisplay. Sucha shift might occurin a speciesthat typicallyfeeds over land (Jen- sen 1946,Rohwer 1968); otherwise, aerial activity could present an am- biguoussignal to conspecifics,signaling either feeding or colonyforma- tion. Agonisticdisplays.--The oblique, the crouch,and gapeare aggressive displays.They are temporallyassociated with one another and with attack,and theyinvariably occur in agonisticcontexts. These postures are also structurallyrelated to attack behavior,incorporating intention movementsto fly and to strike with the bill. The low obliqueis most likelyto leadto attack;it appearsto be the moststrongly motivated and seemsto have the greatestrepelling effect. The gapeis the moststatic of the 3 displaysand probablyhas the leasteffect. The head tossis not associatedwith other agonisticbehaviors. It is howeveran activedisplay, it isoften accompanied by loud ackand chirup calls,and it elicitserect posturingin other terns. Thus, the head toss callsattention to the performer.It mightbe mildlyintimidating as well. The sleekedupright and footlook are alarm postures.The sleeked plumageof the sleekedupright both preparesthe tern for flight and makesthe tern appearsmaller and lessintimidating (cf. oblique).The footlookremoves a disturbingstimulus from the performer'sview (see Chance1962, Harrison 1965) and so, in a broadsense, constitutes flight. It alsoremoves the bill from its aggressiveorientation, and avertsthe performer'sgaze (cf. Scaife1976). Erectand associateddisplays.--The erect is largely sexuallymotivated and is the mostimportant display facilitating contact among individuals. The up-erectand down-erect are particularlyassociated with approach, courtshipfeeding, and mounting.Also, in thesepostures, the bill is directedaway from the performer'spartner, a probableappeasement signal.The up-erectwith head turning (seebelow) suggests flight and appearsespecially appeasing. This is consistentwith the fact that the up-erectwith headturning tends to occurupon initial approachwhen appeasementwould be maximallyadaptive. The landingbent, head nod, head tilt, andhead turning are 4 displays associatedwith the erectthat havethe effectof appeasement.All remove the bill and/or cap from the aggressiveforward orientation,and they 204] H. F. Sears J. Field Ornithol. Summer 1981 are used during approach (landing bent, head tilt, head turning) or during suddendeparture (head nod), when appeasementis needed. Bentand scrape.--These2 displaysinitiate the establishmentof a ter- ritory and the building of a nest. They are temporallyassociated with one another and with the handlingof nestmaterial, and they are structurally similar to a variety of behaviorsassociated with the nest. The bent, with its downwarddirected bill and early positionin the interaction, is the more appeasingof the 2. Precopulatorydisplays.--The hunched appearsto have evolvedfrom juvenile beggingbehavior, but it is closelyassociated with beingmount- ed, aswell aswith courtshipfeeding, and it probablyelicits both mounting and courtshipfeeding from the male. The head jerk appearsto have been ritualized from the taking of food during courtshipfeeding; it is no longer restrictedto this context,and it too elicitsherding, copulation, and courtshipfeeding. Herding is the male precopulatorydis- play; it appearsto test the female'swillingness to be mounted. Vocaldisplay.--The grack is aggressive,and it actsto protectthe nest or young from predators.The call'sdistinguishing feature, the noise component,contributes to the repellingeffect, as does the intensityand the relativelylong (comparedto the ack)duration of the note.The rattle is usedto repel smallerintruders, especially conspecifics. The whine is sexuallymotivated and elicitscourtship feeding, herding, and mounting. The murmur is similarto the rattle in structure,but it is usedin very different contexts. It never repels others; it appears to facilitate the comingtogether of matesor of parentsand chicks. The ack and chipare agonisticvocalizations. The ack is structurally similarto the grackand rattle and seemscharacterized more by aggres- sion than fear. The chip is a quiet reaction to mild disturbanceand seemscharacterized more by fear. The chirupfacilitates approach. Its associationwith arrival suggests that it is used to announcethe arrival of the individual; it probably permitsindividual recognitionas well. Evolutionof majorvisual displays.--One of the mostdistinctive features of the terns is their aerial courtshipdisplay, thought to have evolved from a varietyof aerial and terrestrialbehaviors still seenin gullsand terns (Moynihan 1959, Cullen 1956, 1960). All speciesof tern (ref. cited below)seem to have a male advertisementflight, whichattracts unmated females. The advertisementflight of the noddies (Anous)(Moynihan 1962)is the wanderingflight (secondarilylost in the BlackNoddy, Anous tenuirostris,Cullen and Ashmole1963), a very different interactionthan the correspondinglow flight of the black-cappedterns (Sterna,Chlidon- ias,Gelochelidon). The wanderingflight hasclearly evolved from aggres- sivechase (Moynihan 1962), while the low flight is related to slowflight with food as a lure (Cullen 1960). In many black-cappedterns, the low flight has not evolved beyond this simple advertisementwith food; but in the Common Tern and Vol.52, no. • Gull-billedTern Display [205

Arctic Tern (Sternaparadisaea) (Palmer 1941, Cullen 1956, 1960), it has becomeritualized into a complexstereotyped interaction, incorporating v-flying, the complex pass involving both the aerial bent and aerial straight postures,and swaying.In this form, the low flight must be considereda relativelyderived character,and the Gull-billedTern appearsto be fully as advancedwith respectto this characteras the Arctic Tern. The secondmajor aerialcourtship interaction is the high flight, which usuallyconsists of a spiralascent and a spiralor zig-zag,gliding descent. It usually incorporatesjerk-flying, and in its most derived form, the complexpass and swaying.The widespreadspiral ascent and jerk-flying suggestthat the high flight hasevolved from hostileaerial chase(Cullen 1960).Therefore it is interestingto seethat the high flight is stilllargely hostilein the noddies(Moynihan 1962, Cullen and Ashmole 1963), and at leastsomewhat so in the Black Tern (Chlidoniasniger) (Salter 1948, Cuthbert 1954, Baggerman et al. 1956, Goodwin 1960), Whiskered Tern (Chlidoniashybrida) (Swift 1960), SandwichTern (Sternasandvicen- s/s)(van den Assempers. comm., Smith 1975), and LeastTern (Sterna albifrons)(Moseley 1976). Overt hostilityis lessevident in the Common, Arctic,and Roseate(Sterna dougallii) terns (Palmer 1941, Bullough 1942, Cullen 1956, 1960), and in the Gull-billedTern (thisstudy). This eman- cipationmust be a relativelyderived feature of tern aerial display. The complexpass (with aerialbent and aerialstraight) is probablythe most complex componentof any tern's aerial courtshipbehavior, and the componentleast like ordinary flapping flight. It also has a limited distributionamong the terns (reported in the Least, Arctic, Common, Roseate,and Gull-billed terns). Therefore, although the Gull-billed Tern doeslack some fundamental features of the high flight (it interacts at considerable altitudes, but I have seen no evidence of ritualized ascent or descentexcept the arc soar, which might be homologouswith the gliding and often curveddescent of other terns), it is particularlysig- nificantthat it doesperform the complexpass. It appearsthat the aerial displayof the Gull-billedTern is as derived as that of any tern. The upright and the obliqueare agonisticpostures found throughout the suborderLari (skuas,skimmers, gulls, and terns).It is likely that the differentiated aggressiveand anxiety uprights of the gulls and terns were derived from the simple upright, and that the erect of the terns, a courtshipdisplay, was derived from the anxiety upright (Moynihan 1962). Moynihan(1962) recognizedthe aggressiveupright, anxietyupright, and obliquein the BlackNoddy and Brown Noddy (Anousstolidus). He alsodescribed a rarely performed erect in the Brown Noddy. The Inca Tern (Larosternainca) also has the aggressiveand anxiety uprights,the oblique,and the erect (Moynihan 1962); this seemsto be a primitive condition within the terns. Throughout the black-cappedterns, we find a singleaggressive display apparentlyderived primarily from the oblique(the oblique,gak- 206] H.F. Sears J.Field Ornithol. Summer 1981 kering,and slantdisplays of variousspecies) (Marples and Marples 1934, van den Assem pers. comm., Bergman 1953, Chapin 1954, Cuthbert 1954, Baggermanet al. 1956, Cullen 1956, Goodwin 1960, Swift 1960, Lind 1963,Dinsmore 1972, Smith 1975, Moseley1976, this study). The erect is also found throughout the black-cappedterns, but it displays significantvariability. In mostspecies, as in the noddiesand Inca Tern, the erect is of the simplebill-up form (Lewis 1920, Wolk 1954, Cuthbert 1954, Chapin 1954,Baggerman et al. 1956, Cullen 1956,Goodwin 1960, Sch6nert1961, Dinsmore 1972, Moseley 1976); the SandwichTern (van den Assempers. comm., Bergman 1953) and the Gull-billedTern (Lind 1963, this study)alone have a distinctbill-down erect, surely a derived character within the terns. Most terns perform a breast-loweredscrape posture late during pair- formation. It is apparentlyuncommon in the noddies;most scraping is just a componentof nestconstruction (Moynihan 1962, Cullen and Ash- mole 1963). The Inca Tern never scrapesin a courtshipcontext (Moy- nihan 1962). In contrast, the black-cappedterns perform the scrape during pair-formationbefore the actualbuilding of the nest (ref. cited below). The head-loweredbent postureoccurs only amongthe black-capped terns. The Black and Whiskered terns do not have a differentiated bent and scrape,but their stoopingis performed in contextsin which the bent and scrapeof other terns are performed (Cuthbert 1954, Bagger- man et al. 1956, Goodwin 1960, Swift 1960, Fuggles-Couchman1962). In the SandwichTern, the bent and scrapeare closelyassociated (van den Assempers. comm.) The 2 posturesoccur but are lessclosely paired with one another in the LeastTern (Wolk 1954, Moseley1976), Arctic, Common,Roseate, and Sooty(Sternafuscata) terns (Palmer 1941, Cullen 1956, Dinsmore 1972), and Gull-billed Tern (this study). In these groups,the bent is associatedwith both the erectand scrape. The distribution of thesedisplays within the terns suggeststhat the scrapedisplay evolved from the scrapingof the nest depression.The bent evolvedfrom the scrapeor from someother nest-relatedbehavior, and it later came to be used in non-scrapingcontexts, such as in the commonerect-bent greeting ceremony (this study).With respectto the bent and scrape,the Gull-billedTern is clearlyadvanced. In summary,the Gull-billedTern has been traditionallyconsidered primitiveamong the black-cappedterns, apparently because of its relatively unspecializedform and feeding habits (Peters 1934, A.O.U. 1957, Moynihan 1959, Voous 1973). However,the abovecomparative discussionargues against this hypothesis.In its displaybehavior, the Gull-billed Tern is fully as advancedas any other black-cappedtern. Mostsignificantly, the Gull-billedTern's aerialdisplay, while apparently secondarilysimplified, includes v-flying, the aerial bent, aerial straight, complexpass, and swaying;the Gull-billedTern performsan extremely deriveddown-erect posture; and it has a morphologicallyand temporally distinctbent and scrape.This suggeststhat the feedingadaptations Vol.52, •o. s Gull-billedTern Display [207 of the Gull-billedTern are convergentwith thoseof the gullsand that the speciesshould be includedwithin the genusSterna.

SUMMARY I recognize33 categoriesof display,including 7 vocaland 26 visual displays.The aerial displaysfacilitate the comingtogether of individuals early in the season.In addition to the commonhairpin courseand simple pass,the aerial displayrepertoire includesv-flying, the aerial bent, aerial straight,swaying, complex pass, and arc soar. However, these6 relativelyritualized displays are only infrequentlyperformed in the vi- cinityof the breedingarea. The oblique, crouch, and gape are aggressivedisplays adapted to repellingintruders. The head tosscalls attention to the performer and is probably mildly intimidating. The sleekedupright and footlook are alarm postures,appeasing in socialcontexts. The erect facilitatesthe comingtogether of individuals.The up-erect with head turning is specializedfor use in situationswhere the ternsare relativelyinsecure in their closeproximity, the down-erectfor situations when the terns are more secure.The landing bent seemsto facilitate approachin the sameway that the down-erectdoes. The head nod, head tilt, and head turning are all appeasing. The bent and scrapeplay a part in the initiationof nest-building.The hunched,head jerk, and herding all facilitatemounting and copulation. The grackand rattle are loud calls that repel intruders, the whine solicitscourtship feeding and mounting, and the murmur facilitates closecontact among members of the family. The ack-chirupcomplex is the mostcommon category of vocalization:the ackand chiprepel others; the chirupfacilitates approach. Comparisonof the displaysof the Gull-billed Tern with thoseof other speciessuggests that the Gull-billedTern is not as primitive as its form and feeding strategysuggest; it shouldbe considereda member of the genus Sterna.

ACKNOWLEDGMENTS Many people have assistedme in this study. I particularly want to thank Drs. H. C. Mueller and R. H. Wiley of the Universityof North Carolina at Chapel Hill, Dr. A. F. Chestnutof the U.N.C. Institute of Marine Sciences,and my wife, M. L. Sears.The Frank M. Chapman Memorial Fund of the American Museum of Natural History and the H. van PetersWilson Fund of U.N.C. provided partial monetary sup- port.

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