An Hypothesis Concerning the Relationship of Syringeal Structure to Vocal Abilities

AN HYPOTHESIS CONCERNING THE RELATIONSHIP OF SYRINGEAL STRUCTURE TO VOCAL ABILITIES

ABBOT S. GAUNT Departmentof Zoology,The Ohio State University, Columbus, Ohio 43210 USA

ABSTRACT.--Neitherthe possessionof large vocabulariesor repertoiresnor the ability to learn phonationscan be precisely correlatedwith the structural complexity of a syrinx. Hence,some recent investigators have suggestedthat avianvocal plasticity arises solely from a neurologicalshift. A simple syrinx, i.e. one with only extrinsicmusculature, is subjectto certain constraints,however. Its configurationchanges as a unit, and the factorsresponsible for modulatingsounds cannot be independentlyvaried. Thus, the temporal characteristics of soundpatterns can be varied easily,but rapid juxtapositionof different modulatorypat- terns is difficult. Intrinsic musculaturepermits isolation and independent control of syringeal componentsand thereby simplifiescontrol of modulations.Syringeal complexity may not be an adaptation (i.e. did not evolve under selection)for plasticvocal behavior, but it is permissiveof and probably prerequisite for such behavior. Received17 November1982, ac- cepted16 May 1983.

BOTHthe vocal behaviors and vocal organs meritsinvariably on a syringeal element, usu- (syringes)of birds range from very simple to ally a bronchial bar. Ames (1971) limited the very complex. The extremes of both coincide. term to those musclesarising entirely within Complex syringeshave evolved independently the syrinx, but that characteristicis not easily at leastthree times, in the psittacids,trochilids, determined by gross dissectionof preserved and passerines. Each of these lines contains specimens.Further, in a rather diverse group speciescapable of complexvocal behavior, and of birds, the tracheolateralis extends caudad such behavior is virtually confined to these onto the syrinx (Yarrell 1833,Wunderlich 1884, lines. These coincidencessuggest a close(caus- Beddard 1898). In doves, only the caudal por- al?) linkage between the two phenomena.The tion of the tracheolateralis is well developed, intent of this paper is to examine the possible and it extends from the insertion of the extrin- nature of that linkage. sic sternotrachealis caudad onto the lateral Before continuing, I will define my use of tympanic membranes(Warner 1972). Many au- several terms. By "vocabulary," I mean the set thors have treated such extensions of the trach- of sounds and modulations a bird can make. eolateralisas intrinsic muscles.This practicehas Essentiallyany soundrecognizable as a specific led to some rather elaborateand confusing cat- figure in a sonogramis an element of a vocab- egorizations(Gadow 1896). I considera muscle ulary (Fig. 1). A "song" is a repeatedpattern of to be intrinsic if it can affect the syringeal con- vocabulary elements (= phrase, song or song- figurationby somemeans other than adjusting type of others).Sequences of vocabularyevents the position of the caudal end of the trachea. of different rhythm, tempo, or emphasis, or This definition eliminates those extensions of containing different numbers of repeated ele- the tracheolateralis that insert craniad to the mentsare consideredversions of the samesong, membranes but includes extensions past the but any change in the sequenceof elements tympanum onto the bronchial rings, a situation constitutesa new song. A "repertoire" is the existing in many of the sub-oscinepasserines number of calls and songsused by an individ- (seealso Fig. 4 for the conditionin oscines).If, ual bird.. as is generally supposed,intrinsic musclesare A fourth term, "intrinsic muscles"of the syr- derived from the tracheolateralis, then such inx, is somewhat more difficult to define. In ambiguitiesshould be expected. mostpresent usages, it refersto a seriesof short "Simple vocal behavior" is an ambiguous muscles with cranial attachments on or imme- term that has been used to refer to small vo- diately cranial of the syrinx and caudal attach- cabularies, small repertoires, or stereotyped

853 The Auk 100: 853-862. October 1983 854 ABBOTS. G^UNT [Auk, Vol. I00

2 3 a

0 I I I I TIME 0.0 1.0 2.0(sec)

Fig. I. Widebandsonograms of simpleand complexvocalizations. A. Callsof a Killdeer(Charadrius vocifer- us),a specieswith a simple syrinx. This vocalizationshows some frequency modulation but is composed essentiallyof a single,simple vocabulary element that is prolongedat the endof the call.B. Songof a White- crownedSparrow (Zonotrichia leucophrys). This specieshas unusuallycomplex, short songs that dramatically demonstratethe ability of a complexsyrinx to utter quite differentsounds in rapid sequence.The example containsat leastfour different vocabularyelements, of which the secondcould be further subdivided.

repertoires. Clearly, these restrictions are, to (Nottebohm and Nottebohm 1978). Dialects are some degree, interdependent. My use of the common. Vocabulariesand repertoires may be term incorporatesthem all but emphasizesthe extensive,with hundredsof songsreported for lack of plasticity, whether that be an inability somespecies, over a thousandfor a few (Verner to produce or to learn vocabulary elements. In 1975; Kroodsma 1975, 1978; Kroodsma and Par- thosespecies with simple behavior, geographic ker 1977). Such abilities are widely distributed variation occursat the subspecificlevel (Smy- among oscines. thies 1960, Armstrong 1973, van der Weyden The configuration of a simple syrinx is usu- 1973, Hand 1981), but I have found no report ally determinedby the actionsof two pairs of of culturally maintained, local variants (dia- extrinsic muscles, the aforementioned sterno- lects). trachealis and tracheolateralis, but in a few Complex vocal behavior is characterized by speciesthe extrinsic cleidotrachealisalso helps plasticity of both vocabulary and repertoire. (Youngten et al. 1974, Locknet and Youngren Acquisition of a normal repertoire depends to 1976, Gaunt and Gaunt 1977, Gaunt et al. 1982, some degree on learning (Nottebohm 1970, Suthers and Hector 1982). The configurations Lemon 1975). In some species,the repertoire of complexsyringes are controlledby more than may be modified during an individual's life two pairsof muscles,at leastone pair of which October1983] SyringealStructure and Performance 855

is intrinsic. The very complex syringes of os- syrinx of tyrant flycatcherscontains several in- cines contain 4-9 (depending on what you trinsic muscles and is "simple" only in com- choose to count) pairs of intrinsic muscles parison with an oscinesyrinx. The calls of his (Ames 1971,Dtirrwang 1974) in addition to the nonpasserineexamples are all rich in AM but sternotrachealis and tracheolateralis. show little or no FM. Although AM can be traced directly to the activity of intrinsic syr- THE PROBLEM ingeal muscles(Gaunt and Gaunt 1982), the use of extrinsic musclesfor this purpose has not The fact that the mostcomplex syringes are been demonstratedwith certainty. Moreover, foundin the oscines,a groupcontaining many complex patterns of AM can be produced by species noted for their vocal abilities, leads to changesof the driving pressureor by flow- the easy supposition of a cause-and-effectre- driven oscillations of syringeal components lationship. The notion that there is a direct cor- (Gauntet al. 1982).Greenewalt specifically dis- relation betweensyringeal complexity and vo- tinguished between complex modulations and cal virtuosityis commonlyexpressed in popular variety of modulations. He observed that os- literature and some recent textbooks(Welty cines do have a wider frequency range and 1975: 118) and, indeed, finds support in some more varied kinds of modulation. critical analyses(Miskimen 1951; N.B.: Ames These observations have led to an impres- was unable to confirm the myological differ- sion that vocal behavior is not limited by the ences reported by Miskimen). Yet ornitholo- morphology of vocal structures, but rather is gistshave long recognized(e.g. Beddard1898) regulated and restricted by neurology. Ames that the relationshipis hardly precise.Con- (1971) summarizeda discussionof syringealvs. trary evidence may be gathered from several vocal complexitywith the statement,"Evident- observations. ly the major factor in vocal diversificationin First,vocal plasticity is not absolutelylinked the oscines has been changes in the nervous to the number of intrinsic muscles. Parrots have system,rather than syringealstructure." Simi- only two pairs of intrinsic muscles(Nottebohm larly, Lemon (1975) stated, "My point is that 1976). Among passerinesnoted for their mi- the apparentinnateness in the callsof fowl and metic abilities,the Lyre Bird (Menuranovaehol- dovesmay reflect a much simpler situation than landiae)has three pairs of intrinsic muscles,but in oscineswhere normally the song elements the Indian Hill Myna (Graculareligiosa) and require a much higher level of neuromuscular Mockingbird (Mimuspolyglottos) have at least control." But this supposition leads to some- four (Ames 1971).Second, although all oscines thing of a conundrum. Nottebohm (1972a) have complexsyringes, some have only a sin- wrote that, as commonly acceptedadvantages gle song(Bertram 1970). Third, closelyrelated for the evolution of complexbehavior "may be species may have quite different abilities. expected to be of broad occurrence, we are left Within Emberizinae, different speciesof Ai- to wonder why somebirds evolved vocal learn- mophilahave as many as 200 songs(Groschupf ing while othersdid not."In neitherthe exten- and Mills 1982) or as few as 12 (Groschupfin sive discussionof 1972nor in a list of physio- litt.). In the genus Zonotrichia,males usually logical constraintson vocalizationappearing in have one song,but that songis culturally trans- a later (1975) review did he even allude to the mitted and divided into many dialects(Marler possibility that morphology per se might be and Tamura 1964,Lemon and Harris 1974,Bap- limiting. tista 1977). Fourth, song complexity and repertoire size can vary geographicallywithin a SYRINGEAL MECHANICS single species,e.g. the Winter Wren (Troglo- dytes troglodytes;Kroodsma 1980). Finally, To seek a solution to this problem, we must Greenewalt (1968: 180) stated that if complex- begin by considering how syringes make ity is equated with elaborate modulations, then sounds. Either or both of two major mecha- numerous nonoscines have complex calls. Of nisms, vibrating membranes or vortex series, his examples,however, the songsof only the may form the soundsource (Gaunt et al. 1982). two tyrant flycatchers show both amplitude The former may be responsible for complex (AM) and frequency (FM) modulations. The tones,often (and sometimeserroneously) called 856 ABBOTS,GAUNT [Auk,Vol. 100 harmonic tones, in which energy is simulta- nators, the properties of which are easily neouslydistributed into severalfrequencies; the changed.If the membranesof the syrinx act as latter usually produces pure tones. The two resonators, then pitch may again be deter- mechanisms can interact, and sometimes determined by membranetension. In complextones, mining which is dominant is difficult. In both increasedairflow may shift the energy distri- cases, sound is modulated at the source; tra- bution toward the higher frequencies, thus cheal resonanceplays little or no role (Hersh raising the pitch. 1966, Greenewalt 1968, Abs 1980). Loudness is regulated similarly in both The classic hypothesis states that sound is membrane and vortex systems.Of the several produced by vibrations of the membranous factors that may affect loudness,the pressure portions of the syrinx. The sound'spitch is de- differential through the syrinx, which is deter- termined by the tension of the membrane, mined by a combinationof the driving pres- loudnessby the amplitude of the oscillation. sure and the resistanceof the passageway,is As a first step, the taut membranes are relaxed. the most important (i.e. to sing louder, blow Compressionof the airsacs by the bodywall harder). The driving pressureis controlledby musculature createsa pressurehead to drive air the bodywall musculature; resistance can be through the trachea. Flow inducesa Bernoulli adjustedby changing the position of the flexi- effect as air passesthe membranes. Becausethe ble portions of the syrinx, which alters its av- syrinx is suspendedin the interclavicular air- erage cross-sectionalarea. As previously dis- sac,a substantial pressure differential may de- cussed,however, position of the membranesis velop acrossthe membranes,drawing them into determined by a complex interaction of air- the lumen until tensile forcesbalance the pres- flow, interclavicular airsac pressure,and activ- sure differential. The final tension is deter- ity in syringeal muscles.A second factor reg- mined by the elastic properties of the mem- ulating loudnessis the presenceof devicesthat brane, the action of the syringeal muscles,the augment or inhibit the sound once it has been rate of airflow through the syrinx, and the produced.Many speciespossess throat pouches pressurein the interclavicularairsac (Gaunt and of one or another kind, and these may contrib- Wells 1973). The latter two parameterswill also ute to the disseminationof sound(Chapin 1922, affect the loudness of the sound. Finally, the Gross1932). The acousticsof thesepouches have average diameter of the bore of the lumen op- not been well studied,however. Another pos- positethe membranewill influenceairflow and sibility for augmentationis a resonantrelation- limit the oscillation of the membrane. In some ship between a membrane and a whistle in cases,especially where they are directly op- which the vortices stimulate the membrane's posite each other, the membranes may com- oscillations. Sound will be loudest at the nat- pletely occlude the lumen and act more like ural frequency of the membraneand will drop mammalian vocal cords. off to either side. This common relationship The whistling model supposesthat the ini- could explain the coupling of AM and FM de- tial changesin syringealconfiguration form one scribed by Greenewalt (Gaunt and Wells 1973, or more slots through which the airstream is Klatt and Stefanski 1974). Brackenbury(1979a) forced (Gaunt et al. 1982). Shearing forces at has proposed a somewhat different interaction the slot establish a vortex series that constitutes of airflow and membrane vibration that also the sound source.How frequency is modulated leadsto augmentationof the elicited sound.The has not been established with certainty. In most probable muffling structures are the lat- many mechanicalwhistles, the configurationof eral and medial labia or, where labia are absent, the slot is important (Wilson et al. 1971).In any lateral tympaniform membranes. These struc- configuration,the frequency of a whistle tends tures are set into oscillation by the same air- to increaseonly slightly as airflow increasesto stream that activates the sound source and some critical rate at which the frequency jumps would occlude the sound passagewayin a pat- abruptly to a new stable value, usually an oc- tern depending on their vibratory properties. tave higher. Both real and modelled dove sy- Finally, many birds can activate sourcesin both ringes show this pattern (Abs 1980). Many right and left bronchi simultaneously.Species whistles used by humans as musical instru- with appropriate musculature can produce ments are controlled by coupling them to reso- completelydifferent soundsfrom the two sides, October1983] SyringealStructure and Performance 857

sounds.Suppose that the sound is producedin the vicinity of the median tympaniform mem- ST branes(Fig. 2) and that a pattern of AM is im- posed on that sound by oscillations of the lateral tympaniformmembrane. The simplestway TL to changethe modulating pattern would be to changethe position and tension of that membrane, presumablyby adjustingthe activity of the syringeal muscles.Because both pairs of LTM controlling musclesinsert craniad of all membranousportions, any change in muscularac- tivity will also affect the position and tension of the medial membranes and the diameter of the lumen oppositethem, thus changingthe sound source. Moreover, both pairs of membranes must relax or stiffen together, though not necessarilyto the same extent. Neither individual nor divergent changesseem possible. Nor is this the only linkage in the system.The tension on the membranesis determined by a complexinteraction of airflow, interclavicular airsac pressure,and activity of the syringeal muscles.If the new setting alters the diameter of the syringealbore, the resistanceto flow and airsacpressure will change,thereby changing the tension on and the local turbulence patterns near the membranes.Because the syrinx changesshape as a unit, the componentsof the Bo system are not independent, and even appar- Fig. 2. Frontal sectionsof an idealized, simple ently minor changesof its configurationmay syrinx. A. Relaxedposition. B. Vocalizing configura- have unpredictedconsequences. tion. Note that the forces(arrows) producedby con- This is not to say that no changesare possi- traction of the extrinsic sternotrachealis (ST) and ble, for many require no adjustmentsin syrin- tracheolateralis(TL) musclesmust affect the position geal configuration.For instance,distinctly dif- and tension of both the lateral and medial tympanic ferent patterns can be obtained by changing membranes (LTM and MTM) simultaneously. B, bronchus; T, trachea. the tempo, rhythm, accent, or number of elements.The latter is especiallyeffective if elements are repeated.A major shift in frequency can be achieved by overblowing, a technique an ability termed the "two-voice" phenome- that may be exploited in producing a gull's non (Greenewalt 1968;Nottebohm 1971, 1972b). Long Call. All kinds of FM, continuous, Seemingly, various combinationsof mechani- stepped,oscillatory, or patterned, are found in cal and aerodynamic vibrations should allow the vocabulariesof different specieswith sim- even a simple syrinx to producea wide variety ple syringes.The range of soundsuttered by of sounds. The exact kinds would be deter- different specieswith simple syringessuggests mined by three factors:the rate of airflow, the that any specificacoustic effect can be achieved diameter of the lumen oppositeflexible por- by some combination of simple structure and tions of the syrinx, and the elasticproperties of neuromuscularactivity. What is not achieved those flexible portions. What, then, limits the is the production of diverse effects from any vocabulariesand repertoires of species with one simple structure.Therefore, the rapid jux- simple syringes? tapositionof different vocabularyelements, es- The constraintsof a simple syrinx become peciallythose involving FM, is rare in the calls apparentwhen one considershow it modulates of such species. 858 ABBOTS. GAUNT [Auk, Vol. 100

Evidently a simple structure imposessevere limitations on the ease of compiling and re- arranging seriesof different kinds of vocabulary elements.Hence, we may supposethat neurologicalprogramming to elicit a seriesof T ST different specificeffects from a single structure is either impossibleor impractical,i.e. suffi- ciently difficult to override the advantagesof plasticity.Yet the useof an organthat can pro- INT duce diverseeffects but is extremely difficult to control need not yield cacophony.A syrinx of LTM a given structureand size, activatedby muscular contractionsof a given intensity and with a given airflow, will produce certain sounds B more readily than others.Selection should act on both the structure and the flow pattern to producespecies-specific sounds appropriate to Fig. 3. Frontal section of an idealized, psittacid a given environment.The easewith which the syrinx. The extrinsicsternotrachealis passes directly ventilatory musculaturecan control airflow over the body of the syrinx and inserts onto the oblique septum rather than to the sternum. The should encouragethe developmentof a second tracheolateralis is absent. INT, intrinsic muscles. approach,the use of simple codes,e.g. loud soundsvs. soft sounds,high vs. low pitch, or modulated vs. constant tones. Some variables potentialfor sucha dissociationand, thus,their might be continuous,e.g. repetition rate or du- presenceis a necessary,structural prerequisite ration. Even these simple codes,however, use to the evolution of vocal plasticity. more than a single syringeal setting. Hence, sufficientcontrol to insure at least minimal pre- DISCUSSION dictability would be required. The genetic inheritance of at least a basic Precisionof control in a parrot's syrinx is in- neuromuscularpattern insuresboth that a be- creasedby two means (Fig. 3). First, the num- havior can be performed and that it will be ber of componentsis reduced.As the syrinx is appropriatelyperformed. Specieswith stereo- tracheal rather than bronchial, it is not bilat- typed vocal behavior can be expected to pro- erally divided, and parrots cannot speak with duce the correctsound pattern when first pre- two voices. It also contains but one pair of sented with the correct stimulus (assuming membranes,thereby eliminating the potential appropriate age and hormonal state). This, in- for interactions between two simultaneously deed, is the casefor two species,chickens (Kon- adjusted oscillators. Such an elimination of ishi 1963) and doves (Nottebohm and Notte- components is not unique to parrots, but it is bohm 1971), that have been tested. Stereotypy rare, and few of the other speciesthat show it is also typical of the calls of all birds. In con- are noted for their vocal virtuosity. Second,two trast to songs, calls often convey information of the three pairs of musclescontrolling a par- that must be correctly sent and received with rot's syrinx are intrinsic, and one, the tracheo- no practice. bronchialis, spansthe membranes.Its contraction rotates a set of fused bronchial bars to

AN HYPOTHESIS constrictthe syringeal lumen regardlessof the position of the trachea.This changein arrange- If the foregoing analysisis correct,then com- ment, not the addition of another pair of mus- plex vocal behavior depends on the ability to cles,is critical.The syringeusmuscle arises from controlsound production precisely. Control of the syringeal tympanum and insertson a high- sound production would be eased by any ar- ly modified tracheal bar imbedded in the lat- rangementthat dissociatesacoustic linkages and eral membrane.The action of the syringeusop- isolatesthe effectsof structural components.! poses that of the tracheobronchialis and hypothesizethat intrinsic musclesprovide the providesfor an extremely preciseregulation of October1983] SyringealStructure and Performance 859

ent manner by adjustingthe position of bronchial bars (Chamberlain et al. 1968). The lateral lablure encloses one bronchial bar. Rotation of the bar moves the lablure into the lumen where it determines the configuration of the airway. That configurationmay causethe airflow to vi- brate a membrane,form a vortex-sheddingslot (Gaunt et al. 1982), or induce the formation of harmonic tones (Greenewalt 1968). The lablure may also act as an oscillatorof relatively slow period (Stein 1968). According to Chamber- lain's analysis,the positionof the labial bar and the tension of the overlying tissuesare determined by the interactions of several muscles and can be adjustedindependently. Control of the tension of the internal membrane appears Fig. 4. Frontal section and lateral view of an to be far less precise,but it involves the posi- idealized, oscine syrinx. Muscles of the left side are tion of another bronchial bar and another com- not shown. The presumedintrinsic muscleshave been bination of muscles. numbered. Many authorsconsider la and b separate muscles,but they seemto be portionsof a single mass The isolation of the flexible portions and the of tissue.Similarly, 2 and 4 are universally consid- specializationof muscular function permit an ered as intrinsic muscles, but do seem to be direct extremelyfine control of the oscinesyrinx. That extensions of TL. B, bronchial bar; BD, bronchides- control doesnot enable oscinesto produce new mus; TYM, tympanum. kinds of' sounds,but it does simplify the con- version from one to another. Here a proliferation of componentshas simplified control, and both the syringealbore and the tensionon the with that simplification vocal plasticity and roedial ends of the rotating bronchial bars. large repertoiresbecome practical. Nottebohm (1976) has suggestedthat the de- Although psittacidsand oscinesmay seemto terminationof whether the syrinxwill produce have quite different syringes,the key innova- a harsh tone or a whistle dependson the action tion permitting vocal plasticity in both is the of the syringeusmuscle. Although this has not aquisition of musclesthat directly alter syrin- yet been demonstrated,both the intrinsic mus- geal configuration,which becomesindepen- cles show considerably different electromy- dent of the position of the trachea. Thus, the ographicpatterns from the extrinsicsternotra- independenceof syringeal componentsfrom chealis (Gaunt and Gaunt 1982, in prep.). eachother is greatly increased. Contraction of the sternotrachealis relaxes the I have been able to find accountsof only a caudal end of the trachea and permits a free few casesof presumedvocal learning in birds interplay of the two intrinsic muscles. other than psittacids or passerines(see also The structureof a songbird'ssyrinx is quite Krebs and Kroodsma 1980). The first is in the different (Fig. 4). Its most obvious feature is a Emerald Toucanet (Anulacorhynchusprasinus), proliferation of intrinsic muscles.The seven to which is reported to mimic local speciesin its nine pairs listed by someauthors, often on the immediate presence (Wagner 1944). All the basis of supposed functions, are certainly too supposedmimicked calls consisted of loud, two- many. Ames (1971) recognized four pairs, one pulsed sounds, e.g. "yow-yow," "rayg-rayg," divided into roedial and lateral portions. He "dir-rit," etc. The quality of the mimicry was states,"Until more is known about the opera- unsubstantiatedby spectrographicanalysis. I tion of the syrinx, it seemsunwise to name the have examined the syringes of two Emerald muscleson a functional basisor employ func- Toucanets and found no evidence of intrinsic tional groupings of muscle fasciculi."Yet, rec- muscles. Indeed, the musculature is remarka- ognition of at least four functional units seems bly simple. The sternotrachealisis unusually justified. large and closelyapproaches the cranial end of Each intrinsic muscle seems to affect the the syrinx. The tracheolateralisis absentor se- membranousportions of the syrinx in a differ- verely reduced. 860 ABBOTS.GAUNT [Auk,Vol. 100

A more substantialreport is that of the pres- idently requires two sets of modifications: a ence of learned songsin populations of Little syringeal structure that permits the isolation Hermit Hummingbirds (Phaethornislonguerna- and individual control of elements and a neu- reus;Snow 1968). Each portion of a breeding rological shift that can exploit the potential of lek of this specieshas its peculiar song. Young that structure. Although I judge the develop- birds entering the lek adopt the song of their ment of intrinsic musculatureto be the key in- neighbors.The report containedsound spec- novation permitting vocal plasticity, I do not trographs of unique groups. Wiley (1971) ex- wish to imply that it is an adaptation for that tended Snow's observations and confirmed the function. Many of the suboscinepasserines that similarity of songs within a song-group with possessintrinsic muscles, and even some os- an additional spectrographicanalysis. Signifi- cines, have small repertoires and stereotypic cantly, hummingbirds are one of the few non- vocal behavior. Evidently, a complex syrinx passerine groups to possessintrinsic muscles only permits plasticvocal behavior. Aside from (M/filler 1847, Zusi pers. comm., pers. obs.). the fact that a syrinx is part of a respiratory A third case,deserving close examination, is systemand may have functions associatedwith that of the Greater Prairie Chicken (Tyrnpanu- airflow, intrinsic musculaturemay provide oth- chuscupido), Sharp-tailed Grouse(Tympanuchus er advantagesto a vocal system. It may permit phasianellus),and their hybrids. Sparling (1979) a bird to sing louder or longer for a given reported that wild male Greater Prairie Chick- amount of air (Gaunt et al. 1973) or energy ens adopted a three-note call uttered by hy- (Brackenbury 1977). Brackenbury (1979b) has brids. The mimicry may have been accom- also suggestedthat the passerine syrinx may plished by modifying the "number of notesper have evolved under pressure from allometric bout, mean note duration, strongestfrequency constraints. According to his calculations, a and... form of frequency modulation" of the small bird might have difficulty producing a Prairie Chicken's "Whine." Sonogramsshowed significant sound with a simple syrinx. If so, the mimicked calls to be close but not perfect then the independent evolution of complex sy- copiesof the model. ringes in hummingbirds is less surprising. In a second example, a hybrid responded to Having evolved, for whatever reason,intrin- either Prairie Chickens or Sharp-tailed Grouse sic musculaturehas the potential to release the with appropriate calls. Vocal learning is not constraintsof a simple syrinx. Now Ames' pre- certain here, although the hybrid may have viously quoted statement may be appreciated learned which responsewas appropriate. in a somewhatdifferent manner. The proper Finally, Sparling showed that a Sharp-tailed emphasis is on "oscines" rather than on "di- Grouse was able to mimic playbacks of altered versification," for the oscines possessa struc- calls "so faithfully that his calls could not be ture with functional potentials that could be distinguished from recorded ones," even by exploited for an appropriate change in the ner- spectrographicanalysis. Of great interest is the vous system. fact that, again,the callswere altered by chang- I have neither the intent nor expertiseto dis- ing the duration of notes and internote inter- cussthe presumedneurological shift or the se- vals. Similarly, the learned, covey-specific lective factorsfavoring it. The aforementioned "hoy" and "hoy-poo" calls of Northern Bob- studiesof Bailey and Baker,Sparling, and Wag- white (Colinusvirginianus) differ in temporal ner suggest that some modifications of vocal components (Baily and Baker 1982). Both the performance, perhaps even crude forms of number of elements in a call and their tempo- mimicry, are possible even for species with ral propertiesare more easilyderived from pat- simple syringes.Parrots, though they may learn terns of airsac compressionthan from changes to imitate human speech, are not noted mimics in syringeal configuration (Gaunt et al. 1973, in the wild. Latent, genetic potential for a neu- 1976, 1982). Such variations may be common rological shift may be widespread. Given an among specieswith simple syringes,and much appropriate releasefrom structural constraints, of the subspecificdiversity in the vocalizations such a proclivity could be exploited. of species with simple syringes consists of ACKNOWLEDGMENTS changes in numerical or temporal properties (Smythies 1960, Armstrong 1973). The sonogramsin Fig. 1 were provided by the Bor- The evolution of complex vocal behavior ev- ror Laboratoryof Bioacoustics.Kenneth C. Parkesof October1983] SyringealStructure and Performance 861 the CarnegieMuseum, Pittsburgh, and RichardL. Zusi of the syrinx in Gallusgallus. I, A comparisonof of the U.S. National Museum provided specimensof pressureevents in chickensto those in oscines, toucanetsand hummingbirdsfor dissection.Lincoln Condor 78: 208-223, Fairchild and Donald E. Kroodsma commented on an •, R. C, STEINß& S. L. L. GAUNT, 1973. Pressure earlier draft. Three reviewers selectedby the editor and air flow during distresscalls of the Starling, provided valuable suggestions.Sandra L. Lß Gaunt Sturnusvulgaris (Aves; Passeriformes), J,Exp. Zool. critiqued all drafts and drew the illustrations. This 183: 241-262. work was supportedby N.S.F. Grant DEB-7911774. GREENEWALTßC. H. 1968, Bird song: acousticsand physiology,Washington, D.C,, SmithsonianInst. LITERATURE CITED Press, GROSCHUPF,K., & G. S. MILLS. 1982. Singing behav- ABS, Mß 1980. Zur Bioakustik des Stimmbruchs bei ior of the Five-stripedSparrow. Condor 84: 226- V•3gelnßZooL Jb. Physiol. 84: 289-382ß 236. AMES,P.L. 1971. The morphology of the syrinx in GROSS,A. O. 1932, The Heath Hen. Pp. 264-280 in passerinebirds. Peabody Mus. Nat. Hist. Bull. Life histories of North American gallinaceous 37. birds (A, C, Bent and collaborators). U,S, Natl. ARMSTRONG,E.A. 1973ß A study of bird songs,sec- Mus, Bull, 162, ond ed. New York, Dover Publ. Inc. HAND,J. 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