An Analysis of Vocal Communication in the Adult Brown Noddy (Anous Stolidus)

AN ANALYSIS OF VOCAL COMMUNICATION IN THE ADULT BROWN NODDY (ANOUS STOLIDUS)

DIANE E. Rm•.A Departmentof Biology,University of California,Los Angeles, California 90024 USA

AI•STRACT.--Ianalyzed vocal signals of marked adult Brown Noddies (Anousstolidus) throughout their nesting seasonin the Dry Tortugas,Florida from 1979 to 1982. The basic unit of the adult repertoire is a wide-band click, less than 4 msecduration, ranging in frequencyfrom 200 to 3,300 Hz. I identified nine temporal arrangementsof these clicks, which form the notesof the calls.These calls differ little in frequencyrange, but they differ in the mean frequencyof the most intense sound energy band, in note duration, in the number of clicksper note, and in internote interval. These calls are usedin different contexts, which sometimesoverlap. Frequency, note duration, and internote interval do not differ between sexes.Mean frequencyand note length varied among individuals for somecalls. No tonal elements characteristicof calls of Brown Noddy nestlingsremain in the adult repertoire. Received5 July 1985, accepted15 November1985.

THE Brown Noddy has been considered to in the earlier works of Collias (1960) and Mar- share behavior patterns with gulls and terns ler (1961). The "message"is information en- (Moynihan 1959), but apart from pioneer stud- coded in the signal that is descriptive of the ies by Watson (1908) and Lashley (1915) in the signalerand independent of the context.It can Dry Tortugas, Florida, the study by Dotward be determinedby examiningthe featurescom- and Ashmole (1963) on Ascension Island, and mon to all contexts in which it is used. The Moynihan's (1962) review of sexual and ag- "meanings"(to the receivers)are basedon the gressive behavior, little is known of the com- specificdetails of the contextin which a call is munication behavior of this species.Approxi- given (e.g. location, presenceof other individ- mately 100,000Sooty Terns (Sternafuscata) nest uals, sex and age class,prior experience, sea- sympatricallywith the BrownNoddy in the Dry son,concurrent activities, or identity of the sig- Tortugas.Their vocalizations,of higher ampli- naler) and may be interpreted from the tude than those of the noddies, dominate the responsesof the recipientsto the signal.Other acousticatmosphere in the colony early in the workers,such as Ainley (1975)and Smith (1972), breeding season,and perhapshave led to the have alsoadopted this approach. impressionthat vocalizationsare relativelyun- Gull and tern vocalizationstraditionally were important in the Brown Noddy. Using video described verbally, but since the mid-1960's and sound recordingsI recordedvocalizations they have been portrayed visually on sound and the contextsin which they occurduring spectrograms(Stout et al. 1969, Massey 1976, interactions of individuals of known sex and Conover and Miller 1978, Moseley 1979, Hand breeding status. 1981). Studies of the vocalizations of Sterninae There is a long tradition of study of com- generallyhave been of shortduration and lim- municationin the Laridae. After examining a ited to a few kinds of vocal signals,or to vocal- number of closelyrelated speciesof gulls, Tin- izations of unmarked individuals, and they bergenand othersproposed hypotheses about have not analyzed the entire vocal repertoire the function and evolution of social signals spectrographically. (Tinbergen1952, 1959; Cullen 1957;Moynihan In this study I identify the vocalizationsand 1962; Beer 1975, 1976, 1977, 1979). Some anal- the type of informationcarried by these sig- ysis also has been done on the social behavior nals.The study servesas a basisfor a compar- of terns in the subfamily Sterninae (Cullen ative analysisof Brown Noddy vocal commu- 1956). Smith (1970, 1977) concentrated on other nicationwith that of the SootyTern and other avian taxa and stressed that contexts in which members of the Sterninae (Laridae). An under- social signals are given are important to the standingof vocal communicationof the Brown informationconveyed by the signals(message- Noddy, unusualitself among larids, will be an meaning analysis).This conceptwas suggested important addition to the information avail-

359 The Auk 103: 359-369. April 1986 360 DIANEE. RISKA [Auk,Vol. 103

TABLE1. Numbers of individual malesand femalesanalyzed and numbersof notes per individual.a

RC LC VIB HK LK SB RV RT BT

No. of males 8 10 8 6 10 3 7 8 2 No. of females 5 4 3 6 6 8 3 2 2 No. of notes measured/individual 10 5 30 10 15 1 i 5 9 Total no. of notes measured 130 70 330 120 240 11 10 50 36 a RC = R-call, LC = Long Caw, VIB = Vibration, HK = High Ker, LK = Low Ker, SB = Soft Buzz, RV = RegurgitationVocalization, RT = Rattle, BT = Bite Call. able on breeding strategiesemployed by mem- tablet with a density of 1,550 cross-wires/cm2. The bers of this family, thereby increasingour un- advantageof this techniqueover the traditionalgrid derstandingof the origin and evolutionof these overlay is that the grid is finer, and the computer signals. readsand recordsthe x-y coordinatesdirectly. I measured frequency range, frequency of most intense soundenergy band (the darkestband in the narrow- STUDY SITE AND METHODS band tracing),interclick interval (from midpoint to Observationsand recordingswere made in a col- midpoint of adjacent clicks, for all intervals), note ony of approximately 15,000 adult Brown Noddies length (from the midpoint of the first click in a note to the last), and internote interval (from the terminal on Bush Key, Dry Tortugas, Florida during four breeding seasonsfrom 1979 through 1982. This in- click of one note to the first click of the following cluded the period before adults frequentedthe col- note). All frequency measurementswere from spec- ony during the day, pair formation, nest building, trograms made using the 45-Hz narrow band-pass malesfeeding femalesbefore egg laying, incubation filter, and all temporal measurementswere from and hatching, feeding young, and young birds be- spectrogramsmade using the 300-Hz wide band-pass ginning to fly. In this colonyBrown Noddiesnest in filter. Average numbersof clicksper note and click treesand bushes,and SootyTerns nest on the ground rateswere calculated.Sample sizes differ among calls (Robertson1964). In a selectedarea of the colony, I becauselow-amplitude callswere difficult to separate permanentlymarked active nestsand, using individ- from the backgroundnoise of the colony (Table 1). Calls of known individuals of known sex were se- ually distinctivecolor combinations, color-banded 137 adults caughtby hand, with pull-string wire traps, lected for analysisbased upon the relative clarity of or with butterfly nets. I determined the sex of 90 recordings. adults using behavioral cues,such as males feeding or mountingfemales. I observedno reversalsof either RESULTS during my study. BecauseI observedthe sameindi- viduals and the same nest sites over the four study The basic unit of the Brown Noddy vocal seasons, I believe this to be a reliable method of sex- repertoire is a broad-bandclick, lessthan 4 msec ing this species. in duration (Fig. 1), ranging from 200 to 3,300 Recordingsof vocalizationswere madewith a Uher Hz. Clicks occursingly, in doublets,triplets, or Report L5000 tape recorder at 19 cm/s with a Senn- in short runs, and individual clicks are not re- heiser ME88 directional condensermicrophone. Vid- solved completely by the human ear. Sounds eo recordingswere made with a Sony (AVC-3450) black-and-white portable camera and a JVC (CR- formed by a rapid seriesof pulseshave many 4400U) portablecassette recorder, with the Sennheis- sidebands when analyzedusing a narrow-band er microphone. In all recording situations,the mi- filter on the soundspectrograph. Many of these crophone head was 0.75-1.5 m from two to four nests bands are harmonically unrelated, and there is under observationat one time. It was imperative that unequal emphasis (or intensity) of the bands. the microphonebe close to the nest to pick up low- This pattern depends on the repetition pattern amplitude calls against the high-amplitude back- of the clicks (Watkins 1966). ground noise of other birds, wind, and surf. Obser- I identified nine calls composed of different vations on the nature and context of the behavior of temporal arrangementsof these clicks. These individuals were recorded from a blind where a different temporal arrangements I refer to as number of nestscould be viewed simultaneously.I observed 33-39 nests with color-banded adults each notes. A call is composedof one or more notes. year. Among the clicks, different frequency bands Spectrogramswere made on a Kay Sona-Graph were emphasized,giving complexsubstructure model 6061B.These spectrograms were digitized on to the notes. Notes within a call differed little a Tektronix4081 Graphic System (Tektronix, Inc. 1978) in the overall frequency range, but the fre- ,april 1986] VocalBehavior of AdultBrown Noddies 361

3000- 3OOO

1000- ' '

3000-

1000- ,c,.;ffffl•f.,

i{ • • > 200msec

Fig. 1. Spectrogramsof individual dicks of vocal- Fig. 3. Frequencyof mostintense sound energy izationsof adult BrownNoddies (frequency in Hertz band of callsfrom adult Brown Noddy vocalreper- vs. time). The upper trace (filter band width 45 Hz) toire. Includes mean, 95% confidence limits (horizon- showsbetter frequencyresolution. The lower trace tal line aboveand below mean), _+SD(delineated by (filter bandwidth 300 Hz) showsbetter temporalres- box), and range. Sexes(m and f) are labeled where olution, illustrating the basic structureof the call. analyzedseparately. Clicks may be grouped in "notes," one or more of which make up each call. of the wing remainedcovered by the contour body feathers. quency of the most intense energy band differed (Fig. 2). Posturesof birdswhile calling CALLS OF ADULT BROWN NODDIES also differed among calls,as did positionsof thebill andyellow-orange tongue, but the bend Soft Buzz(Fig. 2).--Soft Buzz is a slow train of clickswith the mostintense energy band at

4000-

2000-

4000-

tõ00 20O0-

4000-

2000-

4000-

2000.

4OOO-

2000. 5OO

4000-

2000-

msec

Fig. 2. Spectrogramsof six calls from the vocal repertoireof the adult Brown Noddy. Filter band width is 300 Hz. Interval between tick marks on x-axis is 200 rnsec.Whistles with side bandsare Sooty Fig. 4. Note lengthsof adult Brown Noddy rep- Tern in background (at arrows). The third note of ertoire. Includes mean, 95% confidence limits (hori- High Ker is precededand followedby Low Kersof zontal line aboveand below mean), _+SD(delineated anotheradult noddy. by box), and range. 362 DIANE E. RISKA [Auk, Vol. 103

TABLE2. Situationsof adult Brown Noddy vocalizations.a

Situation RC LC BT HK LK RT VIB SB RV Male and/or female on nest as a noddy flies over low or lands on or close to their nest X X X X Adult on nest to intruder (human, egret, Sooty Tern, rat) at or approachingnest X X Adult landingat nestafter shortabsence (attack, feather-wet, defecate,circle) or long absence (feeding) X X Adult on nest to nestlingin neighbor'snest X X Parent on nest to own chick out of nest; not ap- proaching X X Adult to any fledglingflying awkwardlyto and from nests X X Adult in air, diving at and strikingintruder (human, egret,Sooty Tern, other noddy) X X Adult hand-held by human, biting X Adult attackinganother noddy, using bill to jab or bite X Adult mountedby nonmate;bites throat and bill of intruding male; callsuntil male dismounts Adult, while fleeingor pulling from graspof attack- ing noddy or Sooty Tern Adult flying overwater or colony,alone or with other noddies Adult leavingthe nest,at initiation of shortflights (collectnest material,circle, defecate, attack, feather-wet) or longer (feeding, suchas after relieved by mateor in early morning),whether or not mate is present Adult flying behindanother noddy in high flight, following closelywith synchronouswing beats X Adult returningto nestwith nestmaterial, flying or walking; mate present,absent, or none X Adult placingnest materialon nest X Adult on groundor in bush,in colonyor on beach, probing potential nest material X Adult on nest as mate returns with nest material X Adult as it approachesmate on nest, suchas during exchange X X Adult as it approacheschick on nest X Adult on nest as mate approaches X Adult on nest as mate leaves the nest X Adult as it leaves mate or chick on nest, such as after relieved or after chick fed X Parentfeeding, preening,brooding, or shading chick X Parentapproaching chick alone on nest or out of nest X Parentas chick appproachesit on or out of nest X Male or female between bouts of courtship feeding, nest building, copulating X Adult while mate VIB as noddy intruder standson edge of nest X Male on nest, mate or unmated female near his nest; female may approachmale X Male while copulatingwith female on nest X Female while begging from male Male and/or female as one preensthe other Male and/or female prior to mountingby male Male feeding female,just beforeor during regurgitation of food X Parent regurgitating to chick X aRC = R-call,LC = LongCaw, BT = BiteCall, HK = High Ker,LK = LowKer, RT = Rattle,VIB = Vibration, SB = Soft Buzz, RV = RegurgitationVocalization. April 1986] VocalBehavior of AdultBrown Noddies 363

4000-

2000-

BITE

4000- 2000- - 2000-

4000- RATTLE z

2000- 4000-

2000- rnsec

Fig. 5. Spectrogramsof three callsfrom the vocal 4000- repertoireof the adult BrownNoddy. Two examples of RegurgitationVocalization from different birds il- 2000- lustratethe rangeof variabilitywithin the call.Filter band width is 300 Hz. Interval between tick marks on x-axis is 200 msec. Whistles with side bands are high-amplitudecalls of Sooty Tern in the back- msec ground (at arrows). Fig. 6. Four examplesof R-callby male L-dgSon his nestas neighboring female lgO-S approaches her own nest. Filter band width is 300 Hz. Interval be- 1,364Hz (Fig. 3). It may lastas long as 2 s but tween tick marks on x-axis is 200 msec. All record- is highly variablein length (Fig. 4). The am- ings made at one session. plituderises and fallsas the call progressesbut remainslow relativeto other calls.It is given by birds preeningor being preenedby their The mostintense energy band is around 1,610 mates,by femalesseeking food from males,or Hz (Fig.3), but the frequencyof thismain band by birdsapproaching their mates(Table 2). The mayrise or fall duringthe call.It is givenwhen caller is usuallyin physicalcontact with the there is an intruder at or near the nest, and also otherbird and standswith the bodyand neck when a bird's own chick of any age is out of low and horizontal. The bill is extended to- the nest (Table 2). The caller turns toward the wardthe mate but remains closed or opensonly receiver,either turning the entirebody or only slightly.Recipients of preeningoften Soft Buzz the headand neck, just before the callis given, or Low Ker (seebelow) with the bill pointed but turns the head forward again,along the downward.Before mounting females for cop- axisof its body,while calling.The neck is ex- ulation, males preen the female while Soft tendedwith the tip of the bill raisedslightly, Buzzing, but Soft Buzz does not continue andis retractedat the endof delivery.The call- through copulation. er'sbill isopen wide and the baseof the tongue RegurgitationVocalization (Fig. 5).--Regurgi- is raised,but the tip is lower inside the anterior tation Vocalizationhas the lowest amplitude endof the mandible.It is oftenfollowed by an and the lowestfrequency of all calls(1,128 Hz, attack. Fig. 3). Long interclick intervals occur in the Adult BrownNoddies and SootyTerns turn middleof somecalls, giving them a segmented away from the R-calleror leave. Birdsthat are structure,and they are highly variable in length attemptingto land continueflying or, if they (Fig. 4). The call is given by a male or female land, turn away. Birds on the nest when an as it begins to lower and stretch its neck for- R-callingmate lands turn away but may turn wardto a beggingnestling, or to a femalebeg- back and gape, exposingthe bright orange gingfrom a male(Table 2), andthe caller may tongue and mouth. Chicks in or out of the nest continueuntil the recipientbegins to feed. either approachthe R-callingparent or the nest R-call(Fig. 2).--This call consistsof single (if the parent is out of the chick's reach, such notesof meanduration 687 ms (Fig. 4) and of as on a limb abovethe nest),walking with the high amplitude.The click rate speedsas the bodyand neck horizontal, or remainstanding call progressesbut mayslow again at the end. and turn away.Mates and nestlingsalso point 364 DIANEE. RISKA [Auk,Vol. 103

4000- L-Sdb

2000-

4000- IgO-S

•ooo 2000-

z 4000- Olg-S

2000- z '"qtllllllII I i hi

4000-

500 2000-

msec

Fig. 7. R-calls from four individual adult Brown Noddies.L-Sdb and lgO-S are female;Olg-S and Rlg-S are male. Filter band width is 300 Hz. Interval between tick marks on x-axis is 200 msec. the bill down vertically, and the caller usually respondsin turn. These Foot-looks,which are similar to those observed in other larids (Le Fig. 8. Internote intervals for callsin adult Brown Croy 1976),also occur among neighboring birds Noddy vocal repertoire. Includes mean, 95% confi- after R-callsare exchanged. dence limits (horizontal line above and below mean), Both the high degree of variation and the _+SD(delineated by box), and range. consistencyamong one individual's R-calls is obvious in spectrogramsof 4 R-calls of male pointed toward or away from the receiver. The L-dgS (Fig. 6). Variation in R-call among 4 in- tip of the tongue is depressedand the broader dividuals is illustrated in Fig. 7. Note that all base is elevated, as in the R-call, but the bill individuals differ from L-dgS, and from each doesnot closecompletely between notes.The other, in changesin the major energy bands caller may attack and continue calling while throughoutthe calls. gripping its adversaryin its bill. The Long Caw LongCaw (Fig. 2).--The notes of the Long seriesis often precededor followed by R-calls, Caw, which occur in a series, are shorter than and responsesto Long Caw are similar to those the R-call. The number of notes delivered var- of R-call,although redpients of Long Caw that ies from 2 to many, depending on the re- are not neighbors,mates, or offspring leave al- sponsesof the intruder or receivers.These notes most immediately unless they are grabbed by have the highestamplitude, but the amplitudes the caller. of the notes in a series differ. The most intense BiteCall (Fig. 5).--This is a specificcall with energy band is around 1,495 Hz (Fig. 3), and the highest click rate (Table 3). It resembles the mean note length (Fig. 4) is twice that of individual Long Caw notes but is shorter and the internote interval (Fig. 8). These calls are is not repeatedin a series.It is given each time given in situations similar to those of R-calls a bird grabsan intruder or strikesfrom the air (Table 2). The body of the bird extendsupward (Table 2). The mostintense sound energy band obliquely but becomeshorizontal as the call averages1,354 Hz (Fig. 3), and, as with R-call progresses.When calls are directed at a given and Long Caw, the amplitude is high. Recipi- individual, the caller, as in the R-call, turns to- entseither Long Caw in return, return the peck, ward the individual while calling; the bill is or attempt to escape. April1986] VocalBehavior ofAdult Brown Noddies 365

LowKer (Fig. 2).--Low Ker is a seriesof short TABLE3. Mean numbersof clicksper note and click rates within notes. a notes of mean length 49 ms (Fig. 4), and its most intense energy band is around 1,452 Hz Mean (Fig. 3). The internoteinterval is highly vari- Mean clicks/100 able (Fig. 8), and ! have heard Low Ker notes n clicks / note msec emittedsingly. These calls are given during nest RV 11,670 95 14 building, changesin incubationand brooding LC 3,631 57 16 shifts,and during interactionswith a mate, po- VIB 1,389 5 19 tential mate, or chick on the nest (Table 2). The HK 1,982 21 13 LK 1,409 9 17 bird stands either with the neck arched and bill SB 1,103 101 8 pointed down, or with the body and head low RV 343 35 8 and oblique, and the bill pointed forward. The RT 1,277 23 13 caller may be turned as much as 180ø away. BT 1,466 40 21 Even when facing the receiver,the bill is ori- aRC = R-call, LC = Long Caw, VIB = Vibration, ented away (down or to the side) and is opened HK = High Ker, LK = Low Ker,SB = SoftBuzz, RV = only slightly. RegurgitationVocalization, RT = Rattle, BT = Bite Call. Low Ker is nearly always given at the nest site,the exceptionbeing in nonterritorial areas, suchas the beachand the ground beneathnest with the bill pointed down until the High Ker sites, where birds collect nest material. Birds caller leaves the nest, after which the mate im- Low Ker while building on the nest even if mediatelyceases Low Ker. Neighboringbirds their matesare temporarilyaway or if they have often begin to High Ker and fly after the orig- no mate. Unpaired males use loud Low Kers, inal caller; some circle and return immediately which attract other birds to the nest site. Fe- to their nests while the remainder fly out of males approach the nest standing on the edge, the colony. facing away from the nest and the male, and Vibrationand Rattle (Figs. 2 and 5).--Vibra- they continueapproaching if the male doesnot tion is a seriescomposed of the shortestof the R-call, Long Caw, Bite Call, or attack. This pat- notes. Internote intervals are also shorter than tern of approachand retreat continueswith a any other call (Fig. 8), and the click rate within seriesof femalesbefore a pair is formed. Phys- notesis high (Table3). The mostintense sound ical contactusually is madebetween matesdur- energy band averages1,429 Hz (Fig. 3). This ing changesin incubation shifts as they pass call is given by a resident when a noddy in- on the nest, both Low Kerring; however, the truder arrives at the nest while both adults, or mate ceasesLow Kerring or shifts to the High an adult and its chick, are present.I never heard Ker (below) once it is relieved. When parents this call when a resident was alone as an in- Low Ker their nestlings approach or remain truder approached.The calling bird standswith close,and the nestlingsmay seek brooding or its neck and head obliquely forward and up, food from the calling adult. and with the bill held slightly above horizon- High Ker (Fig. 2).--High Ker is a series of tal. It turns its head slowly from side to side notesgiven beforea bird takesflight and while and opensthe bill only slightly, giving the ap- it is in flight. The most intense energy band is pearancethat the bill and body are vibrating. 1,800 Hz (Fig. 3), the highest of all calls. The The tongue and mouth lining are not visible. caller standsin a normal upright posture with When the caller is not turning its head, its bill the bill at or slightly above horizontal, facing is turned away from both the intruding bird forward or turning its head slowly from side and the other resident bird. The posture and to side. The bill closes completely between side-to-sidemovement of the head may contin- notes.The tip of the tongueis raisedhigh above ue after the bird ceasescalling. the mandible, but its base is lower in the back Vibration usually grades into Rattle; how- of the mouth. Birds that give this call from a ever, Rattle may occuralone. It resemblesthe perch or from the ground almost without ex- High Ker but has shorter internote intervals ceptiontake flight while calling,or are in flight (Fig. 8), and the individual notes often are not either over water or over the colony. High Ker resolvedby the human listener,giving the call is given beforelong and short flights (Table 2). a rolling quality. The posture and movements The mate of the High Ker caller may Low Ker of the bill are the same as for Vibration, or the 366 DIANEE. RISKA [Auk,Vol. 103

and Bite Call occuras single notes,and the oth- ers are series of repeated notes. Bite Call, Rat- 1ooo tle, and High Ker are notesof similar length, but Bite Call is composedof twice asmany clicks per note as either Rattle or High Ker (Table 3), and it is not repeatedin a series.Notes of Rattle BOO and High Ker have similar numbers of clicks, but the mean internote interval of High Ker is twice that of Rattle (Fig. 8). Long Caw notesare repeated at the same internote intervals, are BOO longer, and have 2.5 times as many clicks as Rattle does. Low Ker and Vibration notes, the shortest notes in the repertoire, overlap in their note-

400 length ranges but differ in internote interval by a factor of 8 (Table 3). The samenumber of clicks in the Soft Buzz (mean values of 101 clicks in 1,205ms) are compressedin the shorterR-call (mean values of 95 clicks in 687 ms). 200

COMPARISON OF SEXES

There were no sex differences in the frequencyof the mostintense sound energy bands for the five callsfor which sexeswere analyzed separately (Fig. 3). Male notes tended to be slightly longer in duration than those of fe- Fig. 9. Note lengths of adult Brown Noddy vocal malesin all calls exceptVibration, but the 95% repertoire. Males (m) and females(f) are labeled. In- confidenceintervals overlappedfor all callsex- cludes mean, 95% confidence limits (horizontal line cept Low Ker (Fig. 9). Thus, the mean values above and below mean), +SD (delineated by box), for males and females are the same. and range.

COMPARISON WITH YOUNG NODDIES bill may be momentarily vertically downward. Amplitude rises and falls throughout the se- Vocalizations of Brown Noddy nestlings ries. Call length varies,and boutsof Vibration (Riska 1986) are different from those of adults and Rattle often alternate with little pause. If in that they are composedof tonal elements the caller's mate is present, it may join in with with side bands as well as bursts of sound over the Vibration and Rattle, or it may give a bout a wide frequencyrange, and the major sound of Low Ker with the head low and bill pointed energy bands are 500-2,000 Hz higher. Short downward. Intruders turn away and leave or discrete clicks like those in adult notes are ex- continueflying if they were attemptingto land. tremely rare. Vibration and Rattle continue until the intruder leaves, or until a resident Long Caws and DISCUSSION then attacks. In the Dry Tortugas, the amplitude of the TEMPORAL PATTERNS OF CALLS noise of the SootyTern colony is higher than that of the Brown Noddies, and without a mi- The calls can be distinguishedeasily from crophoneat the nest many of the noddy vocal- one another by a combination of factors in- izations would be missed. For Low Ker, Soft cluding note length, internote interval, num- Buzz, and Vibration, direct observation of the ber of clicksper note,and whether the call con- birds is often necessaryto determine which are sistsof a single note or a seriesof notes. calling. The structureof the vocalizationsalso Soft Buzz,R-call, Regurgitation Vocalization, leads to confusion when the calls are first heard April1986] VocalBehavior ofAdult Brown Noddies 367 by a human observer,but they becomeunmis- agingpartners and facilitate locating schools of takably distinguishableto the listener with ex- fish. At sea,High Ker may signal the location perience. In dense coloniesit is difficult (and of individuals. often would be wrong) to say that a caller is The messageof Low Ker may be willingness directing its messageto only a single bird. Re- to approach, allow approach, or maintain con- cipientspick up signalsfrom manyindividuals tact or interaction.When given by a bird gath- calling simultaneously.When analyzing calls, ering nest material near territories of other one must account for an obvious individual near birds, the meaning to recipients may be that the nest and also for birds flying low over the the individual intends to move near without nest and birds active at neighboringnests. challenging.To mates,potential mates,or off- R-call and Long Caw may have similar mes- springLow Ker may meanthat it is safeto con- sagesthat warn an intruder of attack if the call- tinue approachor remain near the caller, but er is approachedor if the intruder fails to re- to intrudersthe meaning may be basedon the treat. Birds that give Long Caw while they are inference that the caller is part of an estab- being attackedwarn of possiblereturn attacks. lished family unit or that the nest site has cur- The meaningsto receiversalso may be similar. rent residents. Intruders should retreat from the caller be- The messageof Vibration and Rattle may be causethe latter will attack if approachedfur- readinessto attack an intruder, for they occur ther. It is difficult to state which of these calls only when an intruder is at the nest.The mes- is of higher intensity becauseboth Bite Call sage is also readinessto remain with the site and Long Caw are given during actual fight- and associate.The meaningsof thesecalls dif- ing. When approachedon the nest by a human fer for the intruder and for the chick or the intruder, R-calls are given well before Long mate of the caller, as the responsesare differ- Caw, and Long Caw may not be given until the ent. To the intruder, it means the caller will intruder is next to the calling bird. When a bird attack. Because the caller drives off an intruder gives the Long Caw as it flies to its nest, the but not the mate or offspring,to matesand off- meaning to neighbors may be that it is ready spring it meansthey will not be attacked.Vi- to defend its territory, or it may be responding bration resembles Low Ker in that notes are to birds that R-call and Long Caw as it flies over short and repetitive, but the shorter internote their nests.In addition, Long Caw may signal intervals may give Vibration some character- readinessto interact with its mate (in nest ex- isticsof R-callwhile retaining featuresof Low change)or chicks(feeding, brooding, shading). Ker. Multiple meaningsof R-call and Long Caw The messageof RegurgitationVocalization are also illustrated in the context of calling to may be that the caller is about to disgorgepar- chicksoutside the nest. While an adult may use tially digestedfood. The meaning to females these calls to warn of attack to any potential and nestlings may be that they must move into sourceof harm to its chick, the meaning to the positionto take the food. Birds seekingfood chick may be that the adult is ready to defend enter with their own bill at a right angle to the it and that its route to the nest or to the adult feeder'sbill, scoopingout partially digested is safe. The chick can detect intruders as well food. This orientation is similar to the Black- as detect an adult on its nest, and it may use legged Kittiwake (Rissatridactyla; Cullen 1957) this contextual information to determine the when feeding offspringat the nest. relative safety of moving toward the nest. The messageof Soft Buzz is that the caller The messageof High Ker is intent to leave seeksor seeksto maintain close physical con- the nest for short or long periods.Because it is tact for some nonattack interaction. To the re- never given by birds returning to the nest, to ceiver,it meansthe caller wants food, is ready the caller's mate or its nestling it may mean to preen or mate, or will remain in contact;the that the caller is leaving the territory and ter- specificsdepend on the consequentor subse- minating interaction.It may alsomean that the quent behavior of the caller. bird flying over other nestsis not a territorial Darwin (1872) hypothesizedthat in a species' challenger.Brown Noddies feed in flocksat sea, communicationrepertoire, signals of opposite and data based on marked individuals show function would be sufficiently distinguishable that neighborsreturn to their nestsin groups. in form to reduce or prevent ambiguity. R-call Thus, advertising a departure may recruit for- and Long Caw are given during attack or as a 368 DIANEE. RISKA [Auk,Vol. 103 warning of attack, while the short repetitive BEER,C. G. 1975. Multiple functions and gull dis- notes of Low Ker are given during closeinter- plays. Pp. 16-54 in Function and evolution in action between mates or between parents and behaviour (G. P. Baerends, C. G. Beer, and A. young. Soft Buzz is the longestnote in the rep- Manning, Eds.). London and New York, Cam- bridge Univ. Press. ertoire, longer than R-call,and facilitatesclose 1976. Some complexities in the communi- contactbetween membersof a pair. Vibration, cation behaviourof gulls. Ann. New York Acad. which is a regularand rapid seriesof the short- Sci. 280: 413-432. est notes in the repertoire, drives conspecific 1977. What is a display? Amer. Zool. 17: intruders away from the territory of a mated 155-165. pair. Soft Buzz is, however, lower in amplitude 1979. Vocal communication between and in frequency than Long Caw and R-call Laughing Gull parentsand chicks.Behaviour 70: (Fig. 1). 118-146. The posturesof the bird during these calls COLLIAS,N. E. 1960. An ecological and functional are also different. During Vibration, the bill is classificationof animal sounds.Pp. 368-391 in raisedslightly above horizontal while the neck Animal sounds and communication (W. E. Lan- yon and W. N. Tavolga,Eds.). Washington, D.C., is stretched obliquely upward. During Long Amer. Inst. Biol. Sci. Caw and R-call, the neck and bill are stretched CONOVER, M. R., & D.E. MILLER. 1978. Acoustical nearly horizontal.During Low Ker, the neck is propertiesof the swoop-and-soarcall of the Ring- either stretchedobliquely downward and the billed Gull. Auk 95: 599-602. bill is in line with the neck, or the neck is with- CULLEN,E. 1957. Adaptations in the Kittiwake to drawn and the bill is pointed downward, often cliff-nesting. Ibis 99: 275-302. vertically. CULLEN,J.M. 1956. A study of the behaviour of the Moynihan's (1962) extensiveobservations in Arctic Tern (Sternamacroura). Unpublished Ph.D. the central Pacific offered much insight into dissertation, Oxford, Oxford Univ. Brown Noddy behavior. However, he did not DARWIN,C. 1872. The expressionof emotion in man record vocalizations at the nest. He divided and animals. London, Murray. noddyvocalizations into three categories:Long DORWARD, D. F., & N. P. ASHMOLE. 1963. Notes on Caws,which I believe are the sameas my cat- the biology of the Brown Noddy Anousstolidus on Ascension Island. Ibis 103b: 447-457. egory of R-call; Rapid Caws, the same as my HAND, J. L. 1981. A comparison of vocalizations of categoryof Long Caw; and Rattles,a grouping Western Gulls (Larus occidentalisoccidentalis and of my categoriesof Low Ker, Vibration, Rattle, L. o. livens). Condor 83: 289-301. and perhaps Soft Buzz. Moynihan may have LASHLEY,K. $. 1915. Notes on the nesting activities observedonly one context in which Low Ker of the Noddy and Sooty terns. Publ. Carnegie occurs(Choking display) and no Soft Buzz or Inst. No. 7: 61-83. High Ker becausehe statedthat all Rattles"are LE CRO¾,M. 1976. Bird observationsin Los Roques, almost certainly threat." He also stated that Venezuela. Amer. Mus. Novitates No. 2599. landing birdsare often silent, even when land- MARLER,P. 1961. The logical analysis of animal ing beside other birds. In the Dry Tortugas, communication. J. Theoret. Biol. 1: 295-317. Long Caw, R-call, and Low Ker are given reg- MASSEY, B. W. 1976. Vocal differences between ularly upon returning to the nest, whether or American Least Terns and the European Little Tern. Auk 93: 760-773. not the mate is present, and the loudest Low MOSELEY,L. J. 1979. Individual auditory recogni- Kersare given in this context.Moynihan stated tion in the Least Tern (Sternaalbifrons). Auk 96: that RapidCawing is "by far the mostcommon, 31-39. almost only, call uttered by birds during real MOYNIHAN,M. 1959. A revision of the family Lari- aerial flights," suggestinghe lumps High Ker dae (Aves). Amer. Mus. Novitates No. 1928. with Long Caw;as indicated in my study,how- 1962. Hostile and sexual behavior patterns ever, the usesof these calls do not overlap. of South American and Pacific Laridae. Behav- iour Suppl. 8: 1-365. LITERATURE CITED RISKA,D.E. 1986. An analysisof vocal communication in young Brown Noddies (Anousstolidus). AINLEY,D.G. 1975. Displays of Adelie Penguins: a Auk 103: 351-358. reinterpretation.Pp. 503-534 in The biology of ROBERTSON,W. B., JR. 1964. The terns of the Dry penguins (B. Stonehouse,Ed.). Baltimore, Uni- Tortugas.Bull. Florida State Mus. 8: 1-94. versity Park Press. SMITH, S. T. 1972. Communication and other social April 1986] VocalBehavior ofAdult Brown Noddies 369

behavior in Parus carolinensis. Publ. Nuttall Or- sation,biological significance, origin, and eman- nithol. Club No. 11. cipation during evolution. Quart. Rev. Biol. 27: SMIT•, W.J. 1970. Displaysand messageassortment 1-32. in Sayornisspecies. Behaviour 37: 85-112. --. 1959. Comparative studies of the behaviour 1977. The behavior of communicating. of gulls (Laridae): a progressreport. Behaviour Cambridge,Massachusetts, Harvard Univ. Press. 15: 1-70. STOUT,J. F., C. R. WILCOX,• L. E. CREITZ.1969. Ag- WATKINS, W. A. 1966. The harmonic interval: fact gressivecommunication by Larusglaucescens. Part or artifact in spectralanalysis of pulse trains. Pp. 1, Sound communication. Behaviour 34: 29-41. 15-42 in Marine bio-acoustics, vol. 2 (W. N. Ta- TEKTRONIX,INC. 1978. 4081 Graphic Systemopera- volga, Ed.). New York, PergamonPress. tor's reference. Manual #3 070-1950-00. Beaver- WATSON,J. B. 1908. The behavior of Noddy and ton, Oregon, Tektronix, Inc. Sootyterns. Publ. Carnegie Inst. No. 2: 187-255. TINBERGEN, N. 1952. "Derived" activities: their cau-