THE AUK A QUARTERLY JOURNAL OF ORNITHOLOGY

VOL. 78 OC•'OBER,1961 NO. 4

INTERSPECIFIC PREENING INVITATION DISPLAY OF PARASITIC

ROBERtK. SELA•DERA•D CHARLESJ. LA RUE, JR. BROODparasitism holds special interest for the student of behavior, sinceadoption of this highly specializedway of life, which has evolved independentlyin five avian families (Miller, 1946), involvesnot only the lossof nestingand parentalbehavior but also the developmentof a complexof new patternsof behavioradapting the parasiteto the host. Specializationfor parasitismis most marked in the European (Cuculus canorus) and related forms of the subfamily Cuculinae (Chance, 1940) and perhapsleast so in the cowbirds(Icteridae) of the New World, which have very closelyrelated, nonparasitic relatives and havehad a comparativelyshort evolutionaryhistory as parasites(Fried- mann, 1929, 1955). A considerablevolume of informationon cowbirds has beenprovided by the pioneerwork of Frledmann (1929) and later studiesby Nice (1943), Harm (1941), Norris (1947), Laskey (1950), Mayfield (1960, 1961a and b), and others,but we are still far short of an adequateunderstanding of the biologyof thesebirds. In particu- lar, the complex behavioral interactions occurring between parasite and host, both at the time of egg laying by the and during the course of developmentof the cowbird in the care of the foster parents, are essentiallyunknown. Early in the courseof studieson the behaviorof the Brown-headed Cowbird (Molothrus ater), beginningin February 1959, we noted that captive cowbirds persistently approached individuals of certain other speciesof and invited heteropreeningof the head and neck by adopting a special head-bowedposture (Figure 1). Surprisingly enough, repeated presentationof this display was often effective in inducingother speciesto preen the cowbirds'. Subsequently, we obtained a number of field records of this behavior in Brown-headed Cowbirds,and a similar displaywas seenin captiveRed-eyed Cowbirds (Tangavius aeneus). It would seem, therefore, that heteropreening invitation is a regular, althoughhitherto unstudied,part of the behavioral

473 [ .Auk. 474 SELANDERAND LA RUE,Preening7 Display of Cowbirds [Vol.78 repertoire of these parasitic . The behavior is all the more unusualin that cowbirdsonly infrequentlydirect the invitationaldisplay to membersof their own speciesand do not themselvesindulge in social heteropreening. The presentreport dealsalmost entirely with preeninginvitation in the Brown-headed Cowbird, and, unless otherwise indicated, the term "cowbird" refers to that species. It is our hope that this paper will stimulateother workers to observeand report further instancesof the use of this displayby cowbirdsin the field, sincethe significanceof this behaviorcan be judgedonly when an abundanceof field recordsis available.

DISCOVERY OF TIlE DISPLAY

The display was first seen on 27 February 1959, while we were observinga group of 22 Brown-headedCowbirds in a large, outdoor aviary. A malecowbird approached a femalecowbird and displayed,at which point the femaleflew. Later in the day, a male directeddisplay to another male resting on a perch; and, as the displayingbird ap- proached,the resting peckedit away. When this behavior was first observed,we suspectedthat it repre- sentedan intraspecificdisplay in someway associatedwith courtship or pair formation. However, this suppositionproved to be erroneous, and the normal use of the displaybecame apparent when other species of birds were placedin the aviary with the cowbirds. On 3 March, a few minutes after a meadowlark (Sturnella) was introduced, several cowbirdsapproached it and displayed. At first the meadowlarksimply retreated to a new position, often flying to another perch, at the ap- proach of the cowbirds; but, later the same day, we •oted that the meadowlarkwas less prone to flee and now often remainedin a fixed position,pecking at the cowbirdsas they displayed. Next day, the meadowlarksometimes responded to the displayby preeningthe cow- birds rather than fleeing from them. And for a period of two weeks during which the meadowlarkwas confinedwith the cowbirds,preening becamethe usualresponse of the meadowlarkto any cowbirdin display. As a consequence,the meadowlarkwas "victimized"to the extent that it spentseveral hours each day in this activity. In late March, several female Red-winged Blackbirds (.4gelaius phoeniceus)were placed in the aviary, where they remained through the summer and fall. A day or two after their introduction, they were seen to preen displayingcowbirds, and this behavior was noted hundreds of times in the following months. Octoberl1961 .I SELANI)ERANI) LA RUE,Preening Display o! Cowbirds 475

DESCRIPTION OF THE DISPLAY

We have usedthe term "display"for this behaviorsince it involves distinctivepostures and movementshaving obvious communication function,inducing, normally, flight, attack, or heteropreeningin the individualto which it is directed,hereafter called the recipient. display (Figures 1A, lB, and 1D), the head is bowedto a point at which the bill is directedeither verticallydownward or in toward the cowbird'sbody. The feathersof the head and nape are conspicuously ruffed, but other body plumage is generally slightly compressedor sleeked. The wings and tail are held in normal resting position,and the cowbirdis often slightlycrouched. Assumptionof the head-bowedposture is accompaniedor shortly followedby a movementof the cowbird toward the recipient. This may be a sidling motion along a perch or a direct head-onapproach. Usually the cowbird halts when its head is about one inch from the recipient,but the approachmay continueuntil the top of the cowbird's headis actuallyplaced against the breastof the recipient (Figure 1A). Orientationof the cowbird'sbody with respectto the recipient'sposi- tion varies: frequentlythe body is oriented along a perch as frontal

Figure 1A. Male eowbird gives preening invitation to female Red-winged B!aekbird. 476 SELi•DER,•D L^ RUE,Pree•i•9 Display o] Cowbirds [tVol. Au•. 78

,I

Figure lB. Female cowbird invites preening from a Shell Parakeet.

½

Fi&•re IC. Displayingfemale cowbirddodges peek by Shell Parakeet. October]1961 J SELANDERAN• L^ RUE,Preening Display of Cowbirds 477 presentationof the head is made (Figure lB), but cowbirdsalso posturewith the body at an angle,often about45 ø , to the recipient. Or the cowbirdmay perchside-by-side with the recipient,bowing the head and cockingit toward the recipient. Oblique presentationsare most likely to be usedwhen the recipientis in the habit of peckingat the displayingcowbird; this permitsthe cowbirdto dodgethe blows by turning rapidly away (Figure 1C). Regardlessof the orientationof the displayingcowbird's body, the cowbirdpostures in a positionin whichthe occipitalregion of the head is directedtoward the head of the recipient. While presentingthe fluffedfeathers of the head,the cowbirdmaintains a rigid pose,avoiding rapid or suddenmovement; and it avoidsdirect visualfixation of the recipient. In the displayingcowbird, the eyeshave a characteristic "glassy"appearance. The displayis not accompaniedby vocalizations. Displayis givenon perches,on the ground,or whileboth the recipient and the cowbird cling to the wire sides of an aviary or cage. If heteropreeningis induced,the cowbirdmaintains the bowedposture and continuesto avoid suddenmovement, although it may make slight changesin positionof the head,as if to encouragethe respondingre- cipientto preen particularregions. THE DISPLAY IN CAPTIVE ]•IRDS All our observationsof the preeninginvitation display in cowbirds confinedto aviariesand cageshave involvedadult and first-year indi-

Figure 1D. Male cowbird displays to dummy V•hite-crowned Sparrow. 478 $•^NDERAXeD LA RyE,Preening Display o] Cowbirds Vol.Auk.78 viduals capturedin the spring in the Austin region, Texas. We have not yet had an opportunityto study this behaviorin juveniles or in immature individualsless than six monthsold; but JamesBaird (pers. comm.) has observedthe display in a two-month-oldjuvenile female held in a cage with a female Red-wingedBlackbird.

INTRASPECIFIC PRESENTATION

As we have indicatedpreviously, a cowbirdonly occasionallydirects the displayto anothermember of its own species. In severalhundred hoursof observationof severalgroups of cowbirdsconfined to aviaries and cagesin the absenceof individualsof other species,we have noted intraspecificpresentation of the displayon no more than 25 occasions. Our records indicate that it is most likely to occur among cowbirds that have beendeprived of contactwith other speciesfor long periods. Also, the frequencyof intraspecificpresentation usually rises for a brief period following the introductionof an individual of another species. In all recorded instancesof intraspecificpresentation, the display was given only a singletime and invariably resultedin withdrawal or

Figure IE. Agoniztic behavior of two male cowbirds, each intent on soliciting preening from d•mn•y •Vhite-crowned Sparrow. The bird on the left is beginning ruff-out display as the other bird gives head-up display; both displays have threal function. Octoberl1961 I SF_.LAI•DERA•V I• RuE,Preening Display of Cowbirds 479

Figure IF. Male cowbird at height of ruff-out display to dummy White- crowned Sparrow.

attack on the part of the recipient cowbird. Most frequently the recipient cowbird pecked at the displaying cowbird as it approached, and this brought an end to the episode. In no instance did intra- specificpresentation of the display lead to heteropreening.

INTERSPECIFIC PRESENTATION

Responseof the recipient. Individuals of other speciesplaced in an aviary or cage containingcowbirds initially respond to the approach and display of the latter either by pecking or fleeing. The reaction of female Red-winged Blackbirds is typical of the latter type of response. As the recipientblackbird retreats a step or two, the cowbird quickly follows and again displaysat close range; and this behavior may occur repeatedlyalong a perch. If the recipient flies, the cowbird may follow at once,or it may remain momentarilyin displaybefore flying after the retreatingrecipient, to displayat the new position. If the recipientmakes no overt responseto the displayingcowbird, the latter movesforward a half inch or so, adjustingits positionto bring the head more preciselyinto direct view of the recipient; and soon the cowbird'shead may cometo rest againstthe recipieut'sbreast (Figure 480 SEL^ND•R^>•D L^ RUE,Preening7 Display of Cowbirds [ Vol.Auk. 78

1A). Usually this contact inducesthe blackbird to retreat or to peck at the cowbird. The usual initial responseof the domesticShell Parakeet (2Vlelopsit- tacusundulatus) when placedin a cagewith a cowbirdis to peck and bite as the latter approaches. In response,the displayingcowbird dodgesby rapidly turniug or leaningaway from the blow (Figure 1C). Unless the recipient actually moves forward in attack, the cowbird usually keeps its head bowed as it dodgesand quickly returns to its former position,with its head about one inch from the recipient. It is remarkable that cowbirds persist in their attempts to induce preeningeven in the face of repeatedhostile responseson the part of the recipient, especiallyif the latter is a small speciesand merely pecks instead of moving forward in attack. To illustrate this point, we have summarizedin Figure 2 the results of a test conductedon 13 June 1959, in which a pale-blueadult parakeetand a female cowbird were placedin an observationcage measuring 60 x 60 x 120 cm (2 x 2 x 4 feet). Neither individual had previouslyhad any direct contact

2 •4 3 10 I0 II 1437 Preens I II II NOresponse I I I[ III J I I Pecks III JillIll

8 rnin

Figure 2. Responses of Shell Parakeet to preening invitation displays of female Brown-headed Cowbird; numbers indicate duration of preening episodes in seconds. • Parakeet strikes cowbird. • Starts to preen, then pecks. with the other species,although both had been housed for several days in separatecages in the same room. In an eight-minuteperiod, during which the behaviorwas filmed, the cowbirddisplayed 58 times and made four intention movementsto display. The latter consisted of brief noddingmovements of the head given at distancesfrom seven to 15 cm from the parakeet. Two of them occurred in the first 30 secondsof the period, before a full display was given, and the other two occurredjust after the cowbird had dodgedparticularly vigorous pecksby the parakeet. To the displaysof the cowbird,the parakeet Octobe•1961 I SELANDERAND LA RUE,Preening Display o[ Cowbirds 481 responded39 times by peckingat the cowbird'shead. Following the fifth, seventh, and tenth presentationsof the display, the parakeet actually struck the cowbird on the head and managed to pull out a before the cowbird escaped. Thereafter, the cowbird seemed better able to judge the intentionsof the recipient and succeededin avoiding all other pecks. The parakeet's responseto the fifteenth presentationwas highly ambivalent; it began to preen the cowbird, then pecked,striking the cowbird'shead. Aboutmidway through the test period, there was an increasein the frequencywith which the parakeet made no overt responseto the cowbird's display; and, finally, a number of preening episodesfollowed. It will be noted (Figure 2) that thesegradually lengthened, with the parakeetcontinuously preening the cowbird for 37 secondsat the end of the period. In the courseof this episode,the parakeet twice attempted to "bill" with the cowbird, but the latter refused,moving its bill aside. During the test period, the parakeet,which was accustomedto small quarters,perched more or lesscalmly; but the cowbird, which had not previously been confined to a small cage, was obviously distressed. Other disturbing factors included our presenceat one end of the cage,four photofloodlamps directedon the cage, and the soundof a movie camera. Between displays,the cowbird flew about attempting to escape,and presentationsin the first few minutesof the period were very brief. In anthropomorphicterms, the cowbird's displays sug- gestedthe performanceof a "nervous"habit, for they were directed in an "offhand" fashionwhenever the cowbird happenedto find itself near the parakeet. In this situationit was particularlyclear that the causal basis of this behavior involved somethingother than a simple "need" for preening of the . That the parakeetwas inducedto preen the cowbird soon after they were placedin the cage shouldbe consideredin light of the fact that heteropreeningis a normal part of parakeet socialbehavior. In subse- quenttests involving the sameindividual parakeet but other cowbirds, the parakeetshowed even lessreadiness to peck on first encounterwith a cowbird. About an hour after the first test, another female cowbird was placedin the cage. It at once assumedthe invitationalposture, and the parakeetresponded by preeningthe headand neckof the cow- bird for a periodof 35 seconds;and severalsimilar episodesfollowed. In a third test a few days later, the parakeetpreened a cowbird's plumagefor a periodof four minutesand 45 seconds,with only two brief interruptionsoccurring as the cowbirdadjusted its positionon the perch. This wasthe longestpreening episode recorded in our study. 482 SEL^•rDER^•D L^ RUF.Preening Display of Cowbirds [Vol.[ Auk.78

Occasionallythe recipientbird may respondto the cowbird'sdisplay by mounting and attempting copulation. Griffin (1959) watched a male House Sparrow (Passerdomesticus) attempt to copulatewith a male cowbird as the latter was, according to our interpretation of Griffin's notes,giving preeninginvitation display. He notes that the cowbird "had its head bowed with the lower mandible touching the breast feathersand the wings slightly raised at the shoulder." The position of the wings, as described by Griffin, is not typical and suggeststhe presenceof some behavioraltendency not noted in our birds, but other aspectsof the cowbird's behavior were typical: it followed the sparrow about and nudged it when no responseto the displaywas forthcoming. Griffin reportsthat the sparrowmounted the cowbird four times and that the episodecontinued for from five to eight minutes; heteropreeningwas not observed. A secondrecord of this type is suppliedby Teale (pers. comm.), who saw a male House Sparrow mount a male cowbird four times on 4 January 1954. Teale's notes do not indicate whether or not the cowbird evokedthis behaviorby giving preeninginvitation display, but it is probablethat this was the case. In addition, Behrendt (1960) reports that House Sparrows that are preening displayingcowbirds sometimes climb on their backs. That male House Sparrowssometimes respond to displayingcowbirds by attempting copulationis not surprising, since, as previouslynoted by Eisenmann(footnote to Griffin, 1959), the display posture bears someresemblance to that of a sexuallyreceptive female. In particular, the rigidity of the poseprobably serves as a potent stimulusreleasing copulatorybehavior. Many birds, including both House Sparrows and Brown-headed Cowbirds, can be induced to mount lifeless dummies (Allen, 1934; Howell and Bartholomew, 1954; Selander and Giller, 1961: Thompson,1960), and, in fact, as noted beyond,captive male cowbirds occasionallyresponded in this way to dummies of other speciespresented in attempts to induce preening invitation display. Variation in frequency of presentation. In testing the reactions of cowbirds to dummiesof other species(see below), we detecteda de- creasein readinessto display in late summerduring the annual molt. This variation we are inclined to regard as a reflection of the reduced general activity level characteristic of molting birds rather than an effectof changinglevels of sex hormoneproduction, for cowbirdswith activegonads in April and May exhibitedno greaterreadiness to display than did sexually inactive birds in Decemberand January. Moreover,• bilateralcastration of malesdoes not affect their readinessto display, October]1961 ] SELANDERAND LA RUE,I9reenin!l Display of Cowbirds 483 as indicatedby a test conductedon 14 April 1960, in which a female Red-wingedBlackbird •vas placedin a small aviary containingseven normal males, ten castrated males, nine normal females, and nine ovariectomized females. The castrations and ovariectomies had been performedin January 1960, and the cowbirdshad been deprivedof close contact with individuals of other speciesfor a period of four months. In two 30-minuteperiods, the number of displaysgiven by the cowbirdswas recorded. Distinctivelycolored bands permitted recog- nition of the normal and castrated males; but, as the females were not color banded,no distinctionwas made betweenthe two groups. The resultsof the first test period and a secondperiod followingthe first by two hours, during which the blackbird remained with the cowbirds, are shown in Table 1. In the first 30-minute period, castratedand normal males gave equal numbersof displays,an average of 2.7 for

TABLE 1

NUMBER OF DISPLAYS DIRECTED TO A FEMALE RED-WINGED BLACKBIRD IN TWO 30-MINUTE PERIODS

First period Secondperiod Mean no. Mean no. No. No. of displays No. of displays of cowbirds displays per bird displays per bird

Castrated males 10 27 2.7 52 5.2 Normal males 7 19 2.7 14 2.0 Total, all males 17 46 2.70 66 3.88 Ovariectomized and normal females 18 64 3.5 55 3.0 Total, all birds 35 110 3.14 121 3.46 each individual. The 18 females gave a total of 64 displays,or an averageof 3.5 per individual. In the secondtest period, the numbers .of displaysgiven by femalesand normal males decreasedslightly, but the mean numbergiven by castratedmales increased to 5.2, largely as a result of the efforts of one especiallypersistent individual that alone .displayed25 times. Preening was not performed by the blackbird, which made repeatedattempts to escapefrom the unfamiliar aviary and rarely spentmore than a few secondsin any one position. Eight intraspecificpresentations of the display were noted in the first test period, and nine were seenin the second,whereas no displays were given in the hour precedingthe first test. 484 SELANVERAND LA RUE,Preening Display of Cowbirds l_[ Vol. Auk. 78

There appears to be no marked sexual difference in readinessto display,although we suspectthat femalesare slightly more persistent in their efforts to approachother species. A considerabledegree of individualvariation in frequencyof display was noted. This is shown by a test made on 4 April 1960, when a female Red-wingedBlackbird was placedin a small aviary containing five male and five female cowbirds that were color banded for individual recognition. The cowbirds had not been in contact with other species for three weeks. The blackbirdhad been housedwith anothergroup of cowbirds for a one-year period and had developedthe habit of preeningin responseto the display. The responseof the cowbirdsto the blackbird was immediate; in a one-hourperiod, the 10 cowbirdsgave a total of 265 displays(Table 2). Of the males,Green gave 93 displays,whereas Red gave only 2. This

TABLE 2

INDIVIDUAL VARIATION IN NUMBER OF DISPLAYS DIRECTED TO A FEMALE I•ED-WINGED BLACKBIRD IN A ONE-HouR PERIOD

Males • No. of displays Females No. of displays

Red 2 Red 3 Orange 17 Orange 23 Green 93 Green 1

Pink 3 Pink 60 Purple 5 Blue 58 Totals 2 120 145 Average number of displays per bird: 24.0 29.0 Males arranged in order of position in dominancehierarchy, Red being the alpha indlvidual. Difference between sexesnot significant at 95 per cent level of confidence. trial supportedprevious observations that had suggestedthat the alpha male in a dominancehierarchy of malesis less prone to display than are birdsmidway in the hierarchy,and that birdslow in the order also display relatively infrequently. In females, there was also notable individual variation in frequencyof display, but we are unable to correlatethis variationwith positionin the femaledominance hierarchy, which was not determined and, in any event, is poorly defined in cowbirds. The data in Table 2 again demonstratethe persistencewith which Octoberl1961 I SELANDERANDLA RUE,Preening Display of Cowbirds 485

cowbirdsdisplay to blackbirds. As in the test conductedon 14 April, the blackbirdalmost invariably flew at the approachof the cowbirds and was greatly disturbedby the unfamiliar surroundings. As the blackbirdflew from perchto perchand to the wire sidesof the aviary, one or more cowbirds followed, displaying whenever she remained perched for a moment. In the courseof the one-hourobservation period, we recordedseveral agonisticinteractions between cowbirds and betweenthe blackbird and cowbirds as follows:

"Green male pecked away two female cowbirds which were displaying simul- taneouslyto the blackbird, then he went into display; when no responsefrom the blackbirdwas forthcoming,he buttedher breastwith his bowedhead; this induced the blackbird to fly. "Orange male, displayingto the blackbird, is displacedwith a peck by Pink male, who then displays. "Greenmale pushesaside a femaleto get near the blackbird. He displaysfor 15 secondsthen pecksthe blackbird once. "Toward the end of the hour, Green male displaystwice, then catcheshold of the blackbird'stail with his bill; she flies and he chasesher back and forth across the aviary; when shecomes to rest on a perch,he displaystwice again. "Blue female, after displaying19 times to the blackbird, pecks,then bites at the blackbird'stail; the blackbirdflies and she follows, displayingfour more times. "Blue female displays,then bites the wing feathers of the blackbird and holds on; the blackbirdflies and she follows,displays, and is peckedon the head by the blackbird. Eight secondslater, Blue female grasps the blackbird's tail with her bill and a fight ensues in which the blackbird dominates after repulsing Blue female with a hard peck to the head. A few seconds later, the blackbird pecks Orange female as she approaches and displays. Blue female again approaches, displays twice, pecks at the blackbird's wing, displays eight more times, and then catcheshold of the blackbird's tail; the blackbird flies and Blue female follows, again pecking and biting at the tail of the blackbird. "Orange male is peckedon the head as he displays; he retreats four inches, starts to display again but stopsas the blackbird gives a peck intention movement; Orange male straightens up and flies away." The effect of an individualof anotherspecies in increasingthe fre- quencyof intraspecificpresentation is illustratedby the following epi- sode: "Green male moves toward the blackbird and begins to display. The blackbirdimmediately flies and Green male turns to displayto Pink female for two seconds; then he flies after the blackbird and again displays." As a general rule, cowbirdsdo not behaveaggressively toward the recipientuntil they have presentedthe displaya numberof times and have failed to inducepreening. In the hour observationperiod, Green male, displayinga total of 93 times, peckedor otherwiseattacked the blackbird three times, and Blue female, displaying 58 times, attacked 486 SELANDERANDLA RUE, ?reening Display of Cowbirds [Vol.Auk. 78 the blackbirdseven times; all aggressivebehavior occurred in the second half of the period. Other cowbirdsdid not behaveaggressively toward the blackbird. Similarly, when presentedwith a dummybird, cowbirds typicallydisplay a numberof times,then behaveaggressively toward it (see below).

THE •fARIETY oF SPECIES ELICITING DISPLAY

We have had opportunity to observethe reactionsof captive cow- birds to a small number of speciesof birds confinedwith them in aviaries for periods ranging from a few weeks to several months or introducedfor brief test periods. In addition, we have attempted to test the reactionsof cowbirdsto a variety of speciesby wiring museum study skins cross-wiseto perches (Figure 1D). Unfortunately, these dummiesproved to be much less effectivethan living birds in evoking the display,and our effortsto applythis techniquewere hinderedfurther by seasonalvariation in responsivenesson the part of the cowbirds,to which we havealready referred. In April, strongresponses were given to a numberof dummies,but, in July and August, even thosedummies to which cowbirdshad been most responsivein April sometimesfailed to inducethe displayand were at best effectivein stimulatingdisplays in only oneor two individualsof a largegroup. Despitethis changein responsivenessof cowbirds to dummies,the level of responseto live birdsremained relatively constant. In a 10-minutetest on 6 July 1960, a female dummy Red-wingedBlackbird failed to evoke the display in sevencowbirds that had beendeprived of contactwith other speciesfor a periodof six weeks. Yet whena live femaleblackbird was substituted for the dummyimmediately following the testperiod, all sevencowbirds at once responded,delivering a total of 160 displaysin a 30-minute period. Observationson the reactionsof captivecowbirds to other speciesare summarizedin Table 3. Sincelittle effort was madeto controlmany of the factors that could affect readinessof cowbirds to display, the results of our crude tests probably have little significanceother than indicatingthat cowbirdswill respondto a wide variety of speciesand suggestingthe existenceof somevariation in the effectivenessof dif- ferent speciesin evokingthe display. We will reservecomment on the possiblesignificance of this variation for the Discussionsection of this paper. In addition to the records shown in Table 3, we have an interesting report from JamesBaird on the behaviorof a captivefemale cowbird that washeld in a cagein a roomwith a smallgroup of tropicalfinches: October}1961 ] SELANDERAm) LA RUE,Preening Display of Cowbirds 487 the latter were confinedto a separatecage on the wall above the cow- bird'squarters. Baird notesthat "the cowbirdspent a great deal of time at the end of the perch closestto the finchesand would remain in a 'head bow' position for long periods (10-15 minutes). This was so regular that . . . she spent an hour or more each day in this position." •t•7•7ressionand copulationin responseto dummies. After displaying to a dummy bird, both male and femalecowbirds sometimes pecked at the dummy (usually at the cotton "eye") or made an outright attack, employingboth feet and bill. Their behaviorwas thus similar to that seen in cowbirds following display to nonresponsivelive birds. In addition, male cowbirdsoccasionally mounted the dummiesin attempts to copulateor showedambivalence between tendencies to copulateand to attack. For example,on 17 June 1959, a male displayedto a dummy Robin (Turdus mi•7ratorius)for 37 seconds,then peckedat the Robin's head, mounted,and attemptedcopulation. Dismounting,the male again displayedbriefly, peckedat the dummy, mounted,and vigorouslyat- tacked the dummy from above. Later the same day, this male also attempted copulationwith a dummy Brown Thrasher (Toxostoma rufum) and followedthis attempt with an attack. A dummy female House Sparrow also elicited ambivalentbehavior in a male cowbird, which displayed,stepped up on the back of the dummy, and peckedat the head. A dummy female Red-winged Black- bird was also mountedby a male cowbird; after the copulationattempt, the cowbirddismounted and attackedthe dummy'shead, pulling cotton from the "eye." Consideringthe wealth of evidencesupporting the thesis that an aggressivetendency underlies the courtshipand mating behaviorof birds and other vertebrates(Morris, 1956; Tinbergen, 1954), overt expressionof this tendencyby cowbirdsresponding sexually to dummies is neither unusual nor unexpected. Among icterids, attack following or during copulationattempts has beennoted on many occasionswhen Great-tailedGrackles (Cassidix mexicanus) or Brown-headedCowbirds are respondingto dummyfemales of their own species(Selander, MS), and similar behaviorhas been reportedin the Brewer's Blackbird, Eupha#uscyanocephalus (Howell and Bartholomew,1954), and other species. An unusualresponse of male cowbirdsto dummiesof other species is the performanceof the ruff-out display (Figure 1F), which is normallyused both as a hostiledisplay in territorialinteractions with other malesand in courtshipof females(Selander and La Rue, MS). This displayconsists of a moreor less"standard" ruff-out (see 488 SELANDERAND LA RuE, PreeningDisplay of Cowbirds tVol.[ Auk.78

TABLE 3 RESPONSES OF CAPTIVE BROWN-HEADED COWBIRDS TO LIVE INDIVIDUALS AND DUMMIES OF OTHER SPECIES

Species individuals Response Live individuals confined to aviary with cowbirds for periods of two or more weeks. 8 8 Red-winged Blackbird ( •t.qetaius phoeniceus) Moderate numbers of displays evoked; preening rarely in- duced. 9 Red-winged Blackbird 3 Frequent display evoked; preening became habitual. Meadowlark (Sturnella sp.) 1 Frequent display evoked; preening became habitual. 9 Red-eyed Cowbird ( Tangavius aeneus) 3 Displays infrequent; no preen- ing. 8, 9 9 Great-tailed Grackle (Cassidix mexicanus) 20 Two brief displays to 9 9 noted; none given to 8 8; no preening. 8 Co-ramon Grackle ( Quiscalus quiscula) 1 Negative (no displays or preen- ing). (Feral) Rock Dove ( Columba livia) 4 Negative 8, 9 9 House Sparrow (Passer domesticus) 4 Displays fairly frequent; preen- ing induced. II. Live individuals confined to aviary with cowbirds for periods of from 10 minutes to one hour. 1 8, 9 Inca Dove (Scardafella inca) Numerous displays followed by attack ill which doves were in- jured; no preening. 8 Cockatiel ( Leptolcphus hollandicus) 1 Many displays; no preening; Cockatiel very aggressive and cowbirds unable to approach closely. 9 Shell Parakeet (blue variety) ( Melopsittacus undulatus) Frequent display evoked; ex- tensive preening induced. ( Zenaidura macroura) 1 Negative Domestic Canary (yellow) ( Serinus canaria) 1 8 cowbird displayed through wire separating adjacent cages; no opportunity for preening. October] 1961 J SELANDERAND LA RUE, Preening Display of Cowbirds 489

TABLE 3--Continued

Species Response III. Dummies (study skins) wired to perch of aviary for 5- to 10-minute periods? 1. Loggerhead Shrike (Lanius ludovicianus) 1 display 2. White-crowned Sparrow (Zonotrichia leu- 11 displays cophrys) 3. Starling (Sturnus vulgaris) Negativea 4. Chimney Swift (Chaetura pelagica) Negative 5. Brown Thrasher (Toxostoma rufum) 1 display4 6. Killdeer (Charadrius vociferus) Negative 7. Meadowlark (Sturnella sp.) 5 displays 8. Cedar Waxwing (Bombycilla cedrorum) 4 displays 9. Blue Jay (Cyanocitta cristata) Negative 10. Robin (Turdus migratorius) 2 displays and a copulation attempt and attack 11. Screech Owl (Otus asio) Negative 12. Yellow-breasted Chat (Icteria virens) Positive s 13. 8 Cardinal (Richmondena cardinalis) Positive 14. 8 Rufous-sided Towhee (Pipilo Positive erythrophthalmus) 15. 8 Hooded Oriole (Icterus cucullatus) Negative; two cowbirds ap- proached but seemed too appre- hensive to display. 16. Eastern Kingbird (Tyrannus tyrannus) Positive 17. 8 Painted Bunting (Passerina ciris) Positive 18. • Prevost (•mblycercus holoscri- Negative CeUS) 19. • Myrtle Warbler (Dendroica coronata) Positive 20. • Ladder-backed (Dendrocopos Negative scalaris) 21. 9 Red-winged Blackbird (•4gelaius phoeni- Positive uP,rs) • In addition to the specieslisted, captive cowbirds were seen to display to Evening Grosbeaks (Hesperiphona vespertina) and lovebirds (•4gapornis sp.) in tests conductedat the Laboratory of Ornithology, Cornell University, in October 1960. 2 The dummy Loggerhead Shrike was presented to a group of 10 cowbirds for 10 minutes and remained in the aviary an additional 60 minutes while dummies of species2 through 7 were presentedin successive10-minute periods on 8 April 1960. At the end of the seriesof tests, a live Cockatiel was placed in the aviary and induced 13 displays in a 10-minute period. Dummies of species12 through 21 were presentedto a group of seven cowbirds in successive5-minute periods on 5 July 1960. s Negative responsealso obtained in previous test in 1959. * Evoked copulation attempt and attack in previous test in 1959. 5 Indicates one or more displays evoked. 490 Ssn^•sa ^m) L^ RUE, PreeningDisplay o! Cowbirds [Vol.[ Auk,78

Williams, 1952) followed by bill wiping, the two separate activities often but not invariably being "welded" in a single, continuousseries of movements. Midway in the display, the cowbird's bill is pointed down as the bow to bill wipe begins. High-speed photographsshow that the bird is momentarilyin a posturesuggesting that of the preening invitation display,but that the body feathersare fluffed and the wings and tail are spread.

TIlE DISPLAY IN NONCAPTIVE BIRDS

We have shown that preening invitation display is seen repeatedlyin aviaries in which cowbirds and other speciesare closely confined together; and we have indicated that the frequency with which the displayis given by captivebirds is directly related to the length of time that they have been deprived of contact with other species. In the field, the display undoubtedlyis given less frequently, but our own casualobservations and thoseof severalcorrespondents indicate that it is a regular featureof the behaviorof noncaptiveindividuals. Follow- ing are summariesof all field observationsof preening invitation that have come to our attention; these are arranged under the speciesto which the displayswere directed. It shouldbe noted that we have no field recordsof intraspecificpresentation of the display.

HOUSE SPARROW

Austin, Texas, 29 April 1959. As La Rue watched three House Sparrows and two male cowbirdsperched on the screenedroof of an outdoor aviary, one cowbird briefly directed display to a female sparrow, which did not respond. 1 July 1959. La Rue saw a male cowbird pursue a female sparrow along the branch of a willow tree, moving closeand displayingwhenever the sparrow stopped;hetero- preening was not elicited. 28 November 1959. Selander saw two males and two females displaying to House Sparrows in mixed flocks at a stockyard. One male displayed to six individuals in turn, going frown one to another in rapid succession. The intensity of the display varied from simply perching with bowed head near a sparrow to full horizontal presentation of the head and nape. The sparrows generally hopped,walked, or flew away as the cowbirds approachedor assumedthe bowed posture; preening was not seen. Norman Bird Sanctuary, Middletown, Rhode Island, 20 December 1958. The following notes were suppliedby James Baird (pers. comm., 4 November 1959). "I was watching a small cowbird (20-30) in the backyard. They had finishedfeeding and were sitting quietly, preening,in the dogwoods. . . or walking about rather aimlessly beneath or near the bushes. With the cowbirds were a number of House Sparrows and White-crowned Sparrows [Zonotrichia leucophrys]. My attention was . . . drawn to a female cowbird which had finished preening and started sidling up the branch toward a male House Sparrow which was sitting a foot away. As she approachedthe sparrow, she pointed her bill toward the ground, thus presenting the back of her head to the sparrow. The OctobeQ1961 J SELAlgDER^•D L^ RUE,Preening Display of Cowbirds 491

wings were held at rest.... The sparrow hopped to the ground and the cowbird immediately followed, running after the retreating male and all the while keeping her head pointed downward. Finally, the sparrow hopped on her back and pecked the back of her head for a short time and then hopped off. The cowbird followed again and the sparrow flew off." Baird notes that he witnessed cowbirds giving the display to House Sparrows on several other occasions in the winter of 1958-1959. •4/einberg •4/ildlife Refuge, New York (date not indicated). Ilse Behrendt (1960), watching House Sparrows and a group of 14 cowbirds, including three males and a number of females and "young birds," in bushes near a feeding sta- tion, saw "one of the male cowbirds settle down on a branch right under a female . . . sparrow, bending his head and taking a kind of crouchingposition. Right away the female . . . sparrow . . . [probed] with her bill deep into his head-feathersand worked down all the way to his bill, cleaning and scratching all the spots the bird could not reach himself. "Sometimes it seemedthat it hurt him, for he would suddenly throw up his head and the . . . sparrow would fly away. But the cowbird went after her, taking a branch right under her . . . waiting. And she started to work on him again, over and over. "I saw four different cowbirds being [preened] . . . by four female . . . sparrows. They worked delicately and gracefully. Sometimes they would climb on the cowbirds'back[s], but then they would slide down and always end up by working from a little higher branch." This behavior was observed for "nearly fifteen minutes." Stillwater, Oklahoma, 26 October 1958. Griffin's observations (1959) of a male cowbird displaying for a period of from five to eight minutes to a male House Sparrow, which respondedby attempting to copulate, have already been dlscussed.

SCISSO}•-T^Ir-EDF•,¾c^?cum• (Muscivora forficata) •tustin, Texas, •tpril 1959. Donald R. Giller saw a male cowbird display to an individual of this species. The flycatcher flew from its nest on a telephone pole to anotherpole acrossa highway where two male and one female cowbirds were perched. As the flycatcherlanded on the pole, one of the male cowbirds began a display that continuedfor about 10 seconds. The episode ended as the cowbird pecked at the flycatcher, which then flew back to its nest.

RED-WINGED BLACKBIRD

Eugene Eisenmann(pers. comm., 22 March 1960) informs us that several peoplehave mentionedto him their observationsof Brown-headedCowbirds being preened by Red-winged Blackbirds; and a full account of observationswas suppliedby Edwin Way Teale (pers. comm., 24 September 1959). Baldwin, Long Island, New York, 21 March 1959. At 0630, a female blackbird was seenpreening a female cowbird as they perchedamong canes. As the cowbird held the invitational pose, the blackbird, which was perched slightly above, preened the cowbird's nape. Teale notes that the blackbird "ran its bill horizontallyback and forth.... At other times it movedit vertically,lifting the neck feathers as it advanced. Again it seemedto work in spots here and there. 492 SEL^•DER^•D L^ RyE,Preenin9 Display of Cowbirds [1. Vol. Auk. 78

Our impression was that it was getting something. At intervals it would stop, withdraw its bill and seem to ." This performance, which was in progress when observationsbegan, continuedfor 10 minutes, terminating as the blackbird suddenlyflew to the ground to feed on scatteredseed. The cowbird followed and displayedthree times again; but the blackbird made no responseand the cowbird soon stoppeddisplaying. At 1630 the same day, a female blackbird (possibly the same individual that was watchedin the morning) was seenpreening the neck, "shoulders,"and face of a male cowbird. "At times the cowbird was pressed close with its head seeminglyagainst the breast of the redwing. The redwing moved about, jumping to other canes in the rose tangle, but always the co•vbird followed, coming up a little below and nudging with its head which was bent down, arching its back, [and] getting as close to the redwing as possible." The male cowbird was later joined by a female cowbird and both displayed together to the blackbird. "At times the two cowbirds were pressing against the redwing," one on each side. Once a third cowbird, a female, approachedthe trio but did not display. Still later, a lone female cowbird displayed to the blackbird and was preened for a few seconds. Kissimmee, Florida, 13 December 1960. Selander saw a male displaying re- peatedly to a first-year male blackbird that backed up along a wire at each approachof the cowbird. Nearby, a female cowbirddisplayed to a female red-wing. Observationswere interrupted when a passingcar causedthe birds to fly.

TtlE DISPLAY IN OTHER SPECIES OF COWBIRDS

In the summer of 1959, two captive Red-eyed Cowbirds were occasionallyseen to respond to a female Red-winged Blackbird by giving preening invitation displays that were closely similar to those of the Brown-headed Cowbird. Heteropreening was occasionally induced, but usually the Red-eyed Cowbirds displayed for only a few seconds at any one time and were not preened. This we attributed to fright on the part of the cowbirds induced by our presenceat the aviary, for, unlike the Brown-headed Cowbird, the Red-eyed Cowbird is difficult to accustom to captivity and remains wary and restless even after weeks of confinement. It is noteworthy that the Red-eyed Cowbirds invariably dis- played in a more or less obliqueposition, which, in the other speciesof cowbird, is the characteristic position of individuals that have demonstrated a relatively strong tendencyto flee as a result of having been attacked by the recipient. Possibly a similar interspecific preening invitation display is employed by the parasitic Giant Cowbird (?somocolaa:oryzivorus), which is, according to Fried- mann (1929), closelyrelated to Tan9avius. Chapman (1928) reports seeinga female Giant Cowbird twice bow her head and present the fluffed feathers of the nape to a female Wagler (Zarhynchus wa91eri) at the latter's nest.

DISCUSSION

The foregoingobservations raise a host of questionsconcerning the motivation,ontogeny, function, and possibleadaptive significanceof heteropreeninginvitation behavior in relation to brood of cowbirds.Final answers to thesequestions must await'further informa- October[1961 ] SELANI)ERAND LA RuE,?reenin!1 Display of Cowbirds 493 tion not only on the use of the displayunder natural field conditionsbut also on other aspectsof the host-parasiterelationship. We are also handicappedin our attempt to interpret this behavior by the paucity of available information on the biologicalsignificance of intraspecific heteropreeningin birds in general. At present we can do little more than offer tentativeanswers to someof the major questionsposed by our findings. If cowbirdsthemselves practiced social heteropreening, their solicita- tion of preening from other specieswould be less surprising; but, as noted previously,intraspecific heteropreening has not been observedin Brown-headedCowbirds, and Friedmann (1929) does not mention its occurrencein other cowbird species. It is also clear that the preening invitation display itself is not regular intraspecificbehavior that is only occasionallydirected to individualsof other species. On the contrary, intraspecificdisplay has not been observedin wild birds; and, working with captive birds, we have found that it is infrequentand may be ex- pected only after cowbirds have been deprived of contact with other speciesfor long periodsor following the introductionof an individual of another species,when the cowbirds' "drive" to display apparently in- creasesto a level at which stimuli provided by menlbers of their own speciesbecome sufficient to elicit the behavior. Often it is clear that the displayis in fact releasedby the other speciesand merely redirectedto another cowbird. Amongother icterids,social heteropreening appears to be uncommon. Our observationshave demonstratedits absencein grackles of the genera Ca,•sidixand Holoquiscalus,and it is not reported in compre- hensive studies of the behavior of the meadowlarks(Lanyon, 1957), Red-winged Blackbird (Nero, 1956), Yellow-headed Blackbird (Xanthocephalusxanthocephalus; Nero, MS), and Brewer's Blackbird (Williams, 1952). To the best of our knowledge,the only icterid in which heteropreeningis recordedis the Wagler Oropendola,studied by Chapman(1928), who on four occasionssaw a femaleworking her bill through the neck feathersof a male as the latter posturedwith bowed headand half-openbill. Since "individual distance" (Hediger, 1950) is absent or weakly expressedin many speciesof birds that have social heteropreening ceremonies,we have consideredthe possibilitythat intraspecifichetero- preeningin cowbirdsis somehowprecluded by their rigid maintenance of spacingof individualsat distancesno lessthan five inches. Violation of this critical interval invariably leads to rapid adjustmentof position, effectedby hostiledisplay or pecking,on the part of one or both of the 494 SELANDERAND L^ RUE,Preenin9 Display of Cowbirds [ Vol.Auk. 78 individuals involved. (As a result, two adult cowbirds come into direct physicalcontact only while fighting and during copulation;and the latter activity is precededby mutual mating displaysfunctioning in part to adjust the behavioraltendencies of the participantsin such a way that individual distancecan temporarily be violated without the induc- tion of overt aggressivebehavior.) Following this line of argument, we might speculatethat young cowbirds initially approachand direct their displaysto other cowbirds when they assemblein flocks in the fall, but that aggressiveresponses stemming from violationof individual distanceresult in the young cowbirdsbecoming conditioned to avoid close approachto others of their species. But arguing against this explanationis the fact that cowbirdspersist in approachingRed-winged Blackbirdsand other speciesin the face of continuinghostile responses resultingfrom the cowbirds'violation of the individualdistance main- tained by the recipient. And sincedisplaying cowbirds are successful in reducingthe aggressiveand/or escapetendencies of individualsof other speciesand are able to induceheteropreening by speciesthat, like cowbirds,do not practicesocial grooming (for example,Red-winged Blackbirdsand meadowlarks),it is difficultto believethat, other factors being equal, persistentdisplay could not evoke the same responsein membersof their owu species. Therefore, it seemsnecessary to intro- duce, as a supportinghypothesis, the suggestionthat cowbirds, as recipients,are on the sensoryside unusually resistant to stimuliprovided by a displayingcowbird, or that another cowbird simply does not normallyprovide the stimuli releasingthe displaybehavior. In either case, the result would be a restriction of use of the display to inter- specificinteractions. It is interestingto note that a sociallysubordinate cowbird that "wishes"to remain in the vicinity of a superiorof its own speciesdoes not adopt the head-bowedposture; instead it assumesa "sick-bird" attitude,crouching with the bodyfeathers fluffed. This type of sub- missivedisplay is commonto many . We have previouslynoted variation in the effectivenessof different speciesin evokingthe preeninginvitation display (Table 3). In our tests,species of large size were ineffective,no responsebeing given to male Great-tailed Grackles or to the Common Grackle, Rock Dove, and Mourning Dove. But individualsof moderatesize, notably female Great-tailed Grackles and the Cockatiel, were effective. And here it is noteworthy that cowbirdsdo not parasitize specieslarger than the Mourning Dove (Friedmann, 1929). Our cowbirdsseemed relatively reluctant to display to black or Octoberl1961 / S•-LA•DERA•D LA RUE,Preening Display of Cowbirds 495 dark-brown individuals, but otherwise color and pattern of the po- tential recipient apparentlyhas minor if any significance. We note that cowbirds respondedless frequently to male than to female Red- winged Blackbirds,and they displayedrarely to Red-eyed Cowbirds and not at all to the Prevost Cacique,Chimney Swift, and Starling, all of which are black. This may indicate that our captive cowbirds had been conditionedto avoid black individuals as a consequenceof previousexperience with malesof their own species. But it is possible that black is a relatively ineffectivereleaser (if not an actual inhibitor) quite apart from any conditioningeffect. Experimentswith individual cowbirds raised in visual isolation from other birds may be required to settle this problem. At present we can only note that the failure of cowbirdsto displayto the Blue Jay and their relativelyweak response to the LoggerheadShrike perhapsprovide some supportfor the idea that the responseis influencedby previousexperience. Both species are notoriouslyaggressive toward other species,and Friedmann (1929) suggeststhat the absolutefreedom from "molothrineannoyance" en- joyed by the shrikesis due to the hawklikehabits of thesebirds. Both shrikesand jays occurcommonly in the Austin region,where our cow- birds were trapped. The whole problemof the influenceof previousexperience on this behavioris indeed complex. In the Austin region, cowbirdsare asso- ciated in winter flocks with Red-winged Blackbirds, and they also have frequentcontact with meadowlarksand House Sparrowsat stock- yards and about farms. It is, therefore,perhaps significant that these specieswere particularlyeffective in evokingpreening invitation display in our cowbirds; but strong responsewas also given to two exotic species,the Shell Parakeetand the Cockatiel,with which the cowbirds had not had previousexperience in the field.

HETEROPREENING IN OTHER SPECIES

Preening invitation postures similar to those of parasitic cowbirds occurin a numberof bird species,where, however,they normallyfunc- tion to induceheteropreening by conspecificindividuals rather than those of other species. In somespecies, heteropreening may have no function apart from feather maintenanceor the control of ectoparasites;the adaptivenessof this cooperativebehavior is apparent since the feathers that are most frequentlypreened are those that the individual cannot itself reach with its bill. In other species,however, heteropreening ceremoniesunquestionably have further significanceon a sexualor other sociallevel. Similarly, in , serves a biologi- 496 SEL^NDeUAND LA Rue,Preening Display of Cowbirds [ Vol.Auk. 78 cal function in removing parasitesand the like, but at least in the higher primates it is generally agreed that social grooming takes on addedsignificance as a "socialservice" (Sahlins, 1959). A displaysimilar to that of cowbirdsis reportedby Lorenz (1938, 1952) in the Jackdaw(Corvus monedula), in whichit has an appease- ment function. 1te notes (1952) that "if one jackdaw wants to show submissionto another, he squats back on his hocks, turns away his head, at the same time drawing in his bill to make the nape of his neck bulge, and, leaning towards his superior, seemsto invite him to peck at the fatal spot." This behaviorillustrates what Lorenz (1952) regardedas "the essenceof all the gesturesof submissionby which a bird or of a social speciescan appeal to the inhibitionsof its superior.... The supplicantalways offers to his adversary the most vulnerablepart of his body.... In most birds, this area is the base of the skull." This interpretationnow seemsquestionable in light of recent analysesby Tinbergenand Moynihan (1952), which suggest that the bowingand head-turningdisplays to which Lorenz refershave appeasementfunction (i.e., reducethe attack and/or escapetendencies of other individuals;see Moynihan, 1955) not in the presentationof a vulnerablepart of the body per se but as the oppositeof threat move- ments,an idea previouslyexpressed in Darwin's principle (1872) of antithesis(see discussionsby Marler, 1956, 1959). Representativeof this classof displayare head-flaggingmovements of (Tinbergen and Moynihan,1952), and, perhapsalso, the bowingof Red-winged Parakeets(Psephotus haematonotus) reported by England (1945). The effectivenessof these displaysin reducing the probability of attack lies in the fact that they minimize stimuli for attack by the recipient (Marler, 1957). A sinfilar end may be achievedby pre- sentingstinmli for responsesthat are incompatiblewith attack, that is, by divertingthe "attention"of the recipientto a nonhostileactivity (the "deceptive"displays of Moynihan,1955). Finally, as notedby Marler (1957 and pers.comm.), reduction of the aggressivetendency of another individualmay be achievedby presentingstimuli that are especially evolved for the inhibition of attack. Returningto Lorenz'sdescription of the Jackdawdisplay, it seems possiblethat the head is presentedas an invitation to preen rather than to peck. Socialheteropreening is commonamong Jackdaws, and, even if presentationof the fluffed feathersof the nape and head to an antagonistdid not actuallyinduce heteropreening, the resemblanceof the displayto that usedto invite "friendly"social heteropreening nfight have a "soothing"effect, as suggestedby Moynihan(1955) in refer- Octobeq1961 SELANDER.aND L,• Ru•, PreeningDisplay of Cowbirds 497 enceto a comparabledisplay of the SpiceFinch (Lonchurapunctulata). Observationson captiveJackdaws by Marler (pers. comm.) have re- cently confirmedour interpretation,for he notes that the display does in fact often elicit heteropreening. Goodwin (1959, 1960) has recentlypublished some interesting notes on heteropreeningin estrildines of the genus ,4mandava. In three speciesstudied, the Avadavat (`4. amandava), the Golden-breasted Waxbill (A. subtiara), and the Blue-breastedWaxbill (,4. angolensis), mutual heteropreeningis common; and, in agonistic situations,the subordinateof any two birds is likely to offer its head as an appeasing responseto actual or threatenedaggression. Goodwin has advanced the thesisthat heteropreening"involves sublimated. . . aggressionon the part of the preener and submissionon the part of the preenee," and he notesthat individualswill only permit heteropreeningfrom indi- vidualsthat are regardedas superiorsor equals. Surprisinglyenough, "weaker" birds, especiallywhen apparently"feeling depressedor so- cially insecurethrough having been defeatedin a fight," will approach "stronger"individuals of their own or of other speciesof Amandava and deliberatelyoffer the head for preening. In the solicitationof other species,the behavior of these estrildinesresembles that of cowbirds,but it would be premature to concludethat the similarity extendsto motivationalfactors or that the functional significanceof the behavioris the samein thesetwo different groupsof birds. In the highly gregariousBronze Mannakin (Lonchura cucullata), socialheteropreening of the headfeathers occurs both in pair members and in nonreproductiveindividuals in flocks(Morris, 1957). A bird invitespreening by movingclose to anotherindividual and tilting the headas the two birdsperch side-by-side. Similar behavioris recorded (Moynihan and Hall, 1954) for the Spice Finch, in which "a bird wantingto be preenedtries to incite its immediateneighbor(s) to do so by raising the feathersof the whole head and neck equally, and turningthe napeor chin towardsthe other bird(s)." It is noteworthy that neither speciesof Lonchura maintainsindividual distance;fre- quentlyindividuals come into closebodily contact, clumping together on perchesto restor sleepand to cleanone another. Analagousbehavior is reportedin the Groove-billedAni (Crotophaga sulcirostris)by Skutch (1959), who notesthat "while one stretches up its neck its neighborcarefully bills and nibblesat the feathers, possiblysearching for insectpests; and when the first hasfinished its kind officeto the second,the latter reciprocatesthe favor." Again it is noteworthythat anisare socialbirds showing no individualdistance. 498 SELANDERAl'•r} LA RUE,Preening Display of Cowbirds L[ Vol. Auk.78

In several speciesof wrens of the genus Campylorhynchus,hetero- preening ceremoniesare a regular feature of the behavior of pair members and presumably function in pair-bond reinforcement (Se- lander, 1956). When pair membersmeet after periods of separate foraging or other activity, the female holds a rigid pose as the male carefullypreens her headand neck. Preeningby the male is interpreted as a ritualized "substitute"for pecking, which actually occurs in one species,C. brunneicapillus,in the absenceof the heteropreeningcere- mony. Among psittacines, heteropreeningceremonies initiated by head- bowed invitationaldisplays are widespreadand frequentlyseem to have appeasementfunction. We have recently observedheteropreening in captive Cockatiels,Shell Parakeets,and African Grey (Psitta- cus erithacus); and Dilger (1961) describesthis behavior in lovebirds (•4gapornis). In Cockatiels,a mutual preening and billing ceremony precedescopulation of mated pairs. In a manner suggestiveof a cat solicitinghead scratchingfrom a human, hand-raisedAfrican Grey Parrots will invite "preening" from humansby bowing the head and fluffing the feathers of the head and neck. Analagous behavior is reported in captive Bateleur Eagles (Terathopius ecaudatus),which greet humansby bo•vingthe head and inviting scratching(Moreau, 1945).

THE COWBIRD'S DISPLAY AS AN ADAPTATION FOR PARASITISM

We come finally to a considerationof the possibleadaptive signifi- canceof preeninginvitation display as manifestedby parasiticcowbirds. Perhapsthe simplestinterpretation is that the behaviorrepresents an exploitationof other speciesfor skin and feather care, with the benefit to the cowbird being limited to the preening that is obtained. But there is no reason to believe that the cowbirds have unusual require- ments for preeningof the feathersof the head region; nor are they subject to unusuallyheavy infestationsof lice or other ectoparasites (Friedmann, 1929). Moreover, if we assumethat cowbirdshave specialneeds for featherand skin care, it is perhapssurprising that the problem of obtainingpreening has not been solved by of intraspecificheteropreening ceremonies. Consideringall aspectsof the problem,we wish to suggestthat, while the occasionalheteropreen- ing obtainedby cowbirdsmay be beneficialfrom the standpointof feather and skin maintenanceand may serve to reinforcethe cowbirds' tendencyto displayto individualsof other species,the prime adaptive significanceof the behavioris in the effectit hasin reducingthe hostile October}1961 J SELANDERAND LA RUE,Preening Display of Cowbirds 499 tendenciesof individualsof other speciesthat are potentialhosts for the cowbirds' brood parasitism. In the cowbird'sdisplay, appeasing elements tending to minimize stimuli for attack include the lack of movement, the careful avoidance of direct visual fixation of the recipient,and the partial or complete concealmentof the bill (a major aggressiveweapon) by bowingthe head. (In contrast,a highly aggressivecowbird that is about to attack moves rapidly, visually fixates the opponent,and adopts a posturein which the bill is directedforward.) At the same time, accordingto our interpretation,the presentationof the fluffedfeathers of the headmay be "designed"further to reducethe probabilityof attackby divertingthe recipient's"attention" to the act of preening. The fact that cowbirdsactively seek out and approachrecipients may at first sightseem inconsistent with the thesisthat the behavior reducesthe likelihood of attack; but, as suggestedby Marler (pers. comm.),this may actuallyfacilitate the processof appeasementif the cowbirdapproaches quickly and confidentlybefore the recipientbe- comesaggressive. The potentialadvantages of an interspecificappeasement display are apparent,for it is well knownthat femalecowbirds are attackedby their hostswhen they are discoveredat the nests; and the furtive behaviorof a femalecowbird approaching a nest that she intendsto examineor in whichshe will depositan egg in itself suggeststhat the femaleis exposedto the dangerof discoveryand attack by hostindi- viduals(Mayfield, 1960). Accordingto Friedmann(1929) "mostbirds are so vigilantof their neststhat oftena layingCowbird must be subject to considerableattack, or at least be the witness of many intimidation displays on the part of the victims." As an exampleof the reaction of hosts to the female cowbird at the nest, we may cite Friedmann's observation of a Robin (Turdus rnigratorius)that "began yellingits distresscall" and droveher off the nest. AnotherRobin (the mate), two Catbirds(Dumetella carolinensis), three Yellow Warblers(Dendroica petechia), and one Blackpoll Warbler (Dendroica striata)joined in thechase of thefemale cowbird, "each screaming its loudest." Anotherexample is providedby Prescott'srecord (1947) of attacksby a ScarletTanager (Piranga olivacea) and two Red-eyed Vireos(Yireo olivaceus)on a femalecowbird at a nestof thevireos. Largelyas a resultof researchby Hann (1941),it is knownthat the femalecowbird not only visitsthe host'snest to lay but alsospends a considerableamount of time in the vicinity of nests,waiting for the appropriatetime to deposither eggs. Shewatches nest building by 500 SELANDERAND LA RUE,Preening Display of Cowbirds [ Vol.Atxk. 78 potentialhosts for extendedperiods and makesregular trips of inspec- tion to nestsin the absenceof the owners (Mayfield, 1961a). In the forenoonof the day beforeshe lays, on the day of laying, or, rarely, on the followingday, sheusually visits the nestand removesone of the host'seggs; and she may visit a nest in which she has depositedan egg even after incubationhas begun (Mayfield, 1961a). Male cowbirds presumablydo not visit the nestsof hosts,but they do spendtime in the territories of host speciesand are also subject to hostile responses by the hosts. For example, we have seen Red-wingedBlackbirds chasingboth male and femalecowbirds from their territories on several occasions;and hostility of blackbirdsto cowbirdsis also reportedby Sutton (1928). Hostileresponses of SongSparrows (Melospiza melodia) to cowbirds have been describedby Nice (1943), who notes that the sparrows habituallyreact to the presenceof adult cowbirdsin their territories with vigorous warning notes and threat postures;and, as a female cowbirdapproaches the nest, the sparrowsfrequently attack. The fol- lowing are representativeof Nice's field noteson cowbird-SongSpar- row interactions:

Mar. 30. A female Cowbird spendsabout 10 minutesin 1M's territorlty. 1M and 142 [a pair] tchunk [warning note] continually, following her closely in trees, on burdocksand on the ground. K2 [female] seemsmore zealous than 1M. 4M and K3 [a second pair occupyingan adjacent territority] are also tchunking. 1M flies as though to drive off 4M; returns within a meter of Cowbird with tail spread. K2 utters zhee [threat note].... Apr. 3. Male Cow- bird comeswithin a few centimetersof 1M and K2 feedingon the hillside; one of the pair peckshim in the breast; he leaves. Nice also reports that a presumedfirst-year Song Sparrow on its territory in the spring was "greatly disturbed" over the courting activitiesof cowbirdsearly in the seasonbefore nestinghad begun. In American Redstarts (oCetophagaruticilla) on their territories, Hickey (1940) foundthat "maleswere silentin the presenceof female cowbirds,but females reacted with sharp hisses,a rapid snappingof the bill and much spreadingof the tail." Additional records of hostile responsesby potential hosts to female cowbirdsin the vicinity of nestsare given by Leathers (1956) and Mayfield (1960). Apparentlynot all host speciesrespond aggressively to cowbirds, for Harm (1937) determinedthat Oven-birds (Seiurus aurocapillus) are heavily parasitizedbut "do not recognizethe Cowbirds at sight as enemies,"and he observed(1941) one Oven-bird flee from the nest as a femalecowbird approached. October]1961 SELAm)ER^•V L^ RUE,t'reenin9 Display of Cowbirds 501

In advancing our speculativeinterpretation, we are not unduly dis- couragedby the fact that we have no observationsof cowbirds actually using the display to appeasehostile host individualsin the vicinity of nests, for few observers have studied the behavior of the cowbird. Moreover, brief presentationsof the preening invitation display, espe- cially where heteropreeningis not induced,may easilybe overlookedor confusedwith other behaviorpatterns of the cowbirdby an observernot familiar with the display. Sincethe effectivenessof displayin inducingpreening increases with repeated exposure of the recipient to it, the cowbirds' persistent use of the display in the nonbreedingseason may be adaptive in condi- tioning potential hosts to respond in a "friendly" manner, thus in- creasingthe likelihood that the display will be effective in forestailing attack in the breeding seasonwhen the cowbirds are in the territories of the host species. Additionally, by using the displayin winter flocks, the cowbirds may gain some advantage over individuals of other speciesin potentially agonisticsituations involving food or roosting sites.

ACKNOWLEDGMENTS

This and other researchon the behaviorof icteridsis supportedby grants from the National ScienceFoundation (G-7121 and G-15882) and the Hartz Mountain Products Corporation. We are indebted to Dr. Peter Marler for a critical review of an early draft of this paper and especiallyfor his commentsconcerning the form and function of appeasementdisplays. We also express our appreciationto Mr. Donald R. Giller for assistanceand to Mr. Eugene Eisenmannfor his interest and his help in contactingother workers who have recordedthe displayin cowbirds. Mr. JamesBaird and Mr. Edwin Way Teale kindly suppliedcopies of their field notes describing preeninginvitation in cowbirds.

SUMMARY

Brown-headedCowbirds (Molothrus ater) approachindividuals of other speciesof birds and solicit heteropreeningby giving a special head-boweddisplay. Through persistentpresentation of the display, heteropreeningmay be induced from a variety of species,including meadowlarks, Red-winged Blackbirds, and other forms that do not engagein intraspecificheteropreening. Intraspecificpresentation of the preeninginvitation display is uncommonamong cowbirdsand does not result in the induction of heteropreening. 502 SEL^NDERAND LA RUE,Preening Display o] Cowbirds L[ Vol.Auk. 78

In captivity, the readinessof cowbirds to display is increasedby depriving them of opportunityfor close contact with individuals of other species. There is no marked seasonalvariation in frequency with which the displayis given, and bilateralcastration of malesdoes not affect their readinessto display. Preliminary tests with live birds and dummiesof other speciessuggest that cowbirdswill not display to specieslarger than a Mourning Dove and are relatively reluctant to displayto birds that are blackin color. A similar preening invitation display was seen in captive Red-eyed Cowbirds(Tangavius aeneus). Avian appeasementdisplays are discussed,and it is suggestedthat the interspecificdisplay of parasitic cowbirds is an adaptation for parasitism,functioning to decreasethe probabilityof attack by indi- vidualsof host speciesby decreasingtheir aggressivetendencies.

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