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An Hypothesis Concerning the Relationship of Syringeal Structure to Vocal Abilities

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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 syrin- geal 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
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