SHORT COMMUNICATIONS

The Condor96:552-555 0 The Cooper OrnithologicalSociety 1994 Downloaded from https://academic.oup.com/condor/article/96/2/552/5124082 by guest on 28 September 2021

ADAPTIVE SIGNIFICANCE OF TRACHEAL ELONGATION IN (PARADISAEIDAE) ’

CLIFFORD B. FRITH “Prionodura‘ ”, P.O. Box 581, Malanda, Queensland,4885 Australia

Key words: Manucodia; trachea;vocalization. a coil), and males apparently develop it faster than females. Clench found that, in contrast to M. kerau- The five speciesof Manucodia (including drenii, in M. atra, M. chalybata,M. jobiensisand M. Phonygammus)(Diamond 1972, Beehler and Finch comrii this adaptation occursonly in males and is lim- 1985) are monogamous and sexually monomorphic, ited to elongation of a single loop. The degreeof elon- glossyblue-black, and are medium-to-large gation varies, in these four, being shortestin M. atra, of the family Paradisaeidae.They are confined to for- which has the highest-pitched call, and longest in M. ests of New Guinea, certain satellite islands and trop- comrii, the call of which has been describedas moum- ical northeasternAustralia (Cooper and Forshaw 1977, ful and low (Beehler et al. 1986). Beehler et al. 1986, Coates 1990). Of the 37 other, Beehler (unoubl.. - data) noted sexual dimornhism in conspicuously sexually dimorphic, -of-paradise calls of M. keraudrenii, in which males give a low, (two monomorphic spp. excepted), 35 are tremulous, hollow note that is answeredby the female known or presumedto reproducepolygamously. In the with a harsh, coughing,higher-pitched note; and in M. latter 35 ,males are promiscuous,and females chalybatawhich apparently duets by one sex giving a attend the nest, egg(s)and young alone and unaided seriesof hoo notes while the other follows that with a (Gilliard 1969, Cooperand Forshaw 1977,Coates 1990, higher-pitched woo-oh woo-oh woo-oh woo-oh. Frith 1992, Frith and Frith 1990, 1992, 1993a, 1993b Clench (1978) noted that while Manucodia is the and unpubl. data). The remaining two speciesconsti- only in which looped tracheal elon- tute the little-known monotypic, sexually monomor- gation is known, it is found in a number of non-pas- phic and monogamous genera Macgregoria and Ly- serinegenera. To assessthe possiblesignificance of this cocorax. anatomical adaptation in Manucodia, it is helpful to Manucodes are of considerable interest within the review looped tracheal elongation in non-passerines. Paradisaeidaebecause the two speciesthat have been studied are monogamous and non-territorial, range CRACIDAE widely, and are gregarious,fig-eating specialists(Beeh- ler 1983, 1985, Beehler and Pruett-Jones 1983). In An elongatedtrachea, located subcutaneouslyatop the contrast, most monogamouspasserines are territorial. pectoralmuscle(s), is found in a number of Neotropical The rare avian phenomenon of an elongated and curassowsand relatives. Delacour and Amadon (1973) looped trachea has been long-known in Manucodia note that this is assumedto be associatedwith ampli- spp. (Lesson 1826 [cited in Forbes 1882a], Pavesi 1874 fication or modification of the voice, and that a long [cited in Forbes 1882a1,Forbes 1882a, Beddard 1891). trachealowers the pitch of a call. Marion (1977) found This adaptationin Manucodiais well-described(Clench that the elongationof the tracheawith agein male Plain 1978). Clench noted that vouna male M. keraudrenii ChachalacasOrtalis vetula lowered the pitch of their have’a simple, straight trachea‘ihat develops with in- calls. In some speciesof Cracidae, the elongatetrachea creasingage into an elongate,coiled and looped trachea is exclusive to males, while in others it occursin both that lies subcutaneouslyupon the pectoral muscle(s). sexesbut is slightly shorter in females. Trachea elongation is far greater in males than in fe- males (which have a shorter looped trachea that bends TETRAONIDAE laterally acrossthe pectoral musclesbut may not form Male Rock Ptarmigan (Lagopusmutus), in which some males are monogamous while others are polygynous, have an elongate,looped trachea that gives their calls I Received 21 September 1993. Accepted 2 Decem- a markedly lower pitch than those of females (Mac- ber 1993. donald 1970, Cramp and Simmons 1983).

15521 SHORT COMMUNICATIONS 553

Male Capercaillie (Tetrao urogallus),large, polygy- While not elongatedor looped, dissectionof a single nous grouse, have a trachea lengthened into a simple specimen indicates that the trachea of adult male loop (Newton 1899,Johnsgard 1983a). Males call loudly Twelve-wired Birds of Paradise(Seleucidis melunoleu- from a traditional courtship area to attract multiple ca is modified by having eight rings (fourth to eleventh mates.Moss and Lockie (1979) demonstratedthat male from the bottom) “slightly dilated and flattened antero- Capercaillie calls contain a high level of sound at low posteriorly” to be broader and ossifiedalong their cen- frequency that humans cannot hear and that the car- ter. This contraststo their broad cartilaginousborders. rying power of this part of the call has been underes- The ossifiedcenter of each ring is slightly concave and timated. the interval between thesepeculiar rings is much deep- er than those above and consists of a delicate mem- NUMIDIDAE brane to make this modified length ofthe tracheahighly Downloaded from https://academic.oup.com/condor/article/96/2/552/5124082 by guest on 28 September 2021 In monogamousAfrican guineafowl of the genus Gut- elastic and “probably correlated with the very loud tera, both sexeshave an elongatedtrachea looped into harsh note of these birds” (Forbes 1882b). the hollow of the furcula (Chapin 1932). This feature The tracheaof the polygynouscotingas (Cotingidae), is better developedin the CrestedGuineafowl (G. puch- the Red-ruffed Fruit Crow (Pyroderusscututus), the eruni), which has a call lower in pitch than that of its umbrellabirds (Cephalopterusspp.), and the Calfbird only congenerG. plumifera (Urban et al. 1986). Mac- (Perissocephulustricolor) is modified by being ante- lean (1985) describedthe call of G. pucherunias “deep- riorly expanded. This is greatestin males, to enhance er and more resonant than that of Helmeted Guine- “booming” or “bellowing” advertisement/displaycalls afowl” (Numida meleanris). (Snow 1982). Several observershave noted the deep, loud, or far- GRUIDAE carrying quality of Manucodia spp. calls (Seth-Smith Both sexesof crane speciesexhibit various degreesof 1923, Rand 1938, Rand and Gilliard 1967, Gilliard tracheal elongation and associated sternal modifica- 1969, Diamond 1972, Anon. 1972, Cooper and For- tion. These correlate with loudness, penetration and shaw 1977. Coates 1990. Beehler 1991, and oers. ob- far-carrying quality of call notes (Bollonius in Topsell serv.).Coates (pers. comm.) considersthe ParadiseCrow 1972, Johnsgard1983b). While there is apparently no (Lycocoraxpyrrhopterus) most closely allied to Man- definite relationship between tracheal length and the ucodia.It has a remarkable advertisement call which, typical frequency of call notes by the various crane on Obi and Bisa Islands, is a loud, deep, resonant di- species,those with a longer trachea do show less fluc- syllabic note of about 0.3 secondsduration (Coates in tuation of frequencies(Johnsgard 1983a). litt.) with the quality of a deep woodwind or brass instrument. ROSTRATULIDAE Clench (1978) suggestedthat Manucodia speciescan Females of the polyandrousPainted Snipe (Rostratula physiologically“afford a greatly elongatedtrachea be- benghalensis)have a subcutaneoustracheal loop that cause they are sedentary (non-migratory) and, being lies partly on the pectoral muscles(Newton 1899, Nie- relatively large forest birds, their daily flight distances thammer 1966). This enablesthem to produce a deep- are probably short and predators can be avoided by er, more far-catrying call than males (Johnsgard198-1, short dodging flights around foliage.” This scenario Cramn and Simmons 1983). The elongated trachea would, however, appearto fit numerousnon-migratory probably assistsmature females in attracting multiple and larger rainforest-dwelling passerines;yet no other mates from a greater area than would otherwise be passerineexhibits an elongatedand looped trachea. It possible. is now known that M. keraudrenii is a peculiar pas- serine in being monogamous, but non-territorial and ANSERANATIDAE specializingon feeding upon figs (Beehler 1985). These The male Magpie Goose (Anserunussemipalmata) has fruits may not be economically defendabledue to their an elongatedsubcutaneous trachea that lies in a double unpredictability in space and time within the forest coil on the pectoral muscle. The honking call of this (Beehler 1983, 1985, Beehler and Pruett-Jones 1983) nomadic flocking speciesis louder and lower-pitched thus making territoriality impractical. Thus, this in the male (Marchant and Higgins 1990, contra is not sedentary to the usual extent of territorial and Schodde and Tidemann 1988). monogamouspasserines. Rather, it rangeswidely and may be semi-nomadic when not breeding. Manucodia ANATIDAE chalybataalso feeds predominantly upon figs (Beehler Both sexesof the four Cygnusspp. have a convoluted 1985) and probably over a large area. tracheainside the sternumwhich increases“greatly the The function of the “spectacular anatomical spe- resonanceof the call” (Johnsgard1968) or “account(s) cialization” (Clench 1978) of tracheal elongation in for the powerful calls, in the manner of a trombone” Manucodia may be the sameas in thosenon-passerines (Scott 1972). in which it is found: to produce amplified calls with a lower pitch (as speculatedby Clench 1978) for com- DISCUSSION munication over ereater distances. Such calls would From this brief review, it is clear that non-passerine enable birds to attract mates to a courtship site in po- birds with an elongated looped trachea produce calls lygynousand polyandrousspecies or to maintain con- that are louder, lower in pitch, or carry farther than tact in monogamousor flocking speciesover distance. the calls of close relatives that lack this anatomical This common function of trachea elongation in taxo- modification. The modified trachea apparently allows nomically diverse non-passerinesstrongly suggests that communication over relatively greater distances. the same function may underlie its origin in a bird-of- 554 SHORT COMMUNICATIONS paradise. Thus, an elongated trachea in adult Munu- BOCK,W. J. 1963. Relationships between the birds codiu may have evolved as a means of males attracting of paradise and the bowerbirds. Condor 65:91- a mate(s) or to allow these non-territorial birds to 125. maintain contact among nairs or flock members while CHAPIN,J. P. 1932. The birds of the Belgian Conao. “_ searchinga largeforaging area. What appearto be man- Vol. 1. Bull. Am. Mus. Nat. Hist. 65:1-756. - ucodecontact notes are relatively simple and are high- CLENCH,M. H. 1978. Tracheal elongation in birds- er-pitched than what are considered to be advertise- of-paradise. Condor 80:423-430. ment calls (Coates 1990). Studies are required to COATES,B. J. 1990. The birds of PapuaNew Guinea, determine i&a- and inter:sexual differencesin adver- Vol. 2. Dove, Alderley, Australia. tisement calls relative to deeree of trachea eloneation COOPER.W. T.. ANDJ. M. FORSHAW.1977. The birds and to determine social fuiction of these and other of paradiseand bowerbirds. Collins, Sydney, Aus- Downloaded from https://academic.oup.com/condor/article/96/2/552/5124082 by guest on 28 September 2021 notes. tralia. Bock (1963) noted that the skull morphology of CRAMP,S., AND K.E.L. SIMMONS.[EDS.] 1983. The Manucodia and Lycocorux stronglyindicates that these birds ofthe westernPalearctic, Vol. 3. Oxford Univ. birds are not primitive within the family, but are as Press, Oxford. highly specializedas Purudisaeu. He doubts that these DELACOLJR,J., AND D. AMADON. 1973. Curassows generadiverged from the main line ofevolution leading and relatedbirds. Am. Mus. Nat. Hist., New York. to the true birds-of-paradise (Paradisaeinae) “before D~OND, J. M. 1972. Avifauna of the easternhigh- the development of the specialized courtship [polyg- lands of New Guinea. Nuttall Club Publications. yny].” Clench (1978) agreedwith Bock that the trachea Cambridge, MA. modifications in Munucodiu are also highly special- FORBES,W. A. 1882a. On the convoluted trachea of ized. two species of manucode (Manucodiu utru and Thus, the greater trachea elongation in male Man- Munucodiu gouldi); with remarks on similar struc- ucodiu may have evolved as a physiologically costly turesin other birds. Proc. Zool. Sot. Lond. (1882): (Clench 1978) secondary sexual character as a result 347-353. of sexualselection (i.e., “honest advertising” of Zahavi FORBES,W. A. 1882b. Note on a peculiarity in the 1975). If elongate tracheas are a relict of discarded tracheaof the Twelve-wired Bird-of-Paradise (Se- polygynous mating sytems, the main function would leucidis nigru). Proc. Zool. Sot. Lond. (1882):333- presumably still be for courtshipby males. In the case 335. of M. keruudrenii, however, the trachea may also be FRITH, C. B. 1992. Standardwing Bird of Paradise modified for communication over an extensive, non- Semioptera wallucii displaysand relationships,with territorial, foraaina__ home ranse. comparative observations on disnlavs of other Paradisaeidae.Emu 92~79-86. _ . I am most grateful to Bruce Beehler, Mary Clench, FRITH, C. B., AND D. W. FRITH. 1990. Discovery of Brian Coatesand Dawn Frith for kindly and construc- the King of Saxony Bird of ParadisePteridophoru tively commenting on a draft of this contribution and alberti nest, egg and nestling, with notes on pa- to Glen Ingram for kindly providing literature. rental care. Bull. Brit. Omithol. Club 110:160- 164. LITERATURE CITED FRITH,C. B., ANDD. W. FRITH. 1992. Nesting biology of the Short-tailed Paradigalla Purudigallu brevi- ANONYMOUS. 1972. Third omithlon results. New cuudu. Ibis 134:77-82. Guinea Bird Sot. Newsl. 74: l-5. FRITH, C. B., AND D. W. FRITH. 1993a. Nidification BEDDARD.F. E. 1891. Ornithological notes. II. On of the Crested Bird of ParadiseCnemophilus mac- the convoluted trachea of Mu&odiu comrii. Ibis gregorii and a review of its biology and system- (1891):512-514. atics. Emu 93:23-33. BEEH‘LER,B. 1983. Frugivory and polygamy in the FRITH,C. B., ANDD. W. FRITH. 1993b. Notes on the birds of naradise. Auk 100:l-l 2. nesting biology of the Ribbon-tailed As- BEEHLER,B. -1985. Adaptive significanceof monog- trupiu muyeri (Paradisaeidae).Emu 93: 12-22. amy in the , Munucodiu ker- GILLIARD,E. T. 1969. Birds of paradise and bower audrenii (Aves: Paradisaeidae),p. 83-99. In P. A. birds. Weidenfeld and Nicolson, London. Gowaty and D. W. Mock [eds.], Avian monoga- JOHNSGARD,P. A. 1968. Waterfowl: their biology and my. Ornithological Monographs No. 37. AOU, natural history. Univ. of Nebraska Press,Lincoln. Washington, D.C. JOHNSGARD,P. A. 1981. The movers. SandDiDerS.__ , and BEEHLER,B. M. 1991. A naturalist in New Guinea. snipesof the world. Univ. of Nebraska Press,Lin- Univ. of Texas Press, Austin. coln. BEEHLER,B. M., AND B. W. FINCH. 1985. Species- JOHN~G~, P. A. 1983a. Grouseof the world. Croom checklist of the birds of New Guinea. Australas. Helm, London. Omithol. Monogr. No. 1. RAOU, Melbourne. JOHNSGARD,P. A. 1983b. Cranesofthe world. Croom BEEHLER,B. M., T. K. PRATT,AND D. A. ZIMMERMAN. Helm, London. 1986. BirdsofNew Guinea. PrincetonUniv. Press, LESSON,R.-P. 1826. Voyage autour du monde . Princeton, N.J. sur . . la Coquille pendant . . . 1822-25 . par BEEHLER,B., ANDS. G. PRUETT-JONES.1983. Display M.L.I. Duperrey. Zoologie. Vol. 1, Paris. dispersion and diet of birds of paradise: a com- MACDONALD,S. D. 1970. The breeding behaviour parison of nine species. Behav. Ecol. Sociobiol. of the Rock Ptarmigan. Living Bird 9: 195-238. 13:229-238. MACLEAN,G. L. 1985. Robert’s birds of Southern SHORT COMMUNICATIONS 555

Africa. Trustees of the John Voelcker Bird Book ofparadise in the wild. Amer. Mus. Novitates 993: Fund, Cape Town. l-8. MARCHANT.S.. AND P. J. HIGGINS. 1990. Handbook RAND, A. L., AND E. T. GILLIARD. 1967. Handbook of Australian, New Zealand and Antarctic Birds. of New Guinea birds. WEIDENFELD& NICOLSON, Vol. l., Part B. Oxford Univ. Press, Melbourne. London. MARION. W. R. 1977. Growth and develoument of SCHODDE, R., AND S. C. TIDEMANN. [EDS.]. 1988. the Plain Chachalacain south Texas. Wilson Bull. Reader’s Digest completebook of Australianbirds. 89:47-56. Reader’s Digest, Sydney. Moss, R., AND I. LOCKIE. 1979. Infrasonic compo- SCOTT,P. 1972. The swans.Michael Joseph,London. nents in the song of the Capercaillie Tetruo uro- SETH-SMITH,D. 1923. The birds of paradiseand bow- gallus. Ibis 121~95-97. er birds. Avicult. Mag. Ser. 4, 1:41-60. Downloaded from https://academic.oup.com/condor/article/96/2/552/5124082 by guest on 28 September 2021 NEWTON,A. 1899. A dictionary of birds. Adam and SNOW,D. 1982. The Cotingas. Br. Mus. (Nat. Hist.), Charles Black, London. London. NIETHAMMER,G. 1966. Sexualdimorphismus am TOPSELL,E. 1972. The fowles of heaven, or history Osophagusvon Rostrutulu. J. fur Omithol. 107: ofbirds. T. P. Harrison, and F. D. Hoenhiger [eds.]. 20 l-204. Univ. of Texas Press, Austin. PAVESI,P. 1874. Intomo ad una nuova forma di tra- URBAN.E. K.. C. H. FRY. AND S. KEITH. IEDS.~ 1986. chea di Manucodia. Ann. Mus. Civ. Stor. nat. The birds of Africa. Vol. 2. Academic Press,Lon- Genova 6:3 15-324. don. RAND, A. L. 1938. Results of the Archbold Expedi- ZAHAVI, A. 1975. Mate selection-a selection for a tions. No. 22. On the breedinghabits of somebirds handicap. J. Theor. Biol. 53:205-214.

The Condor96:555-559 0 The Cooper Ornithological Society 1994

DETERMINATION OF NESTLING AGE AND LAYING DATE IN TENGMALMS’ OWL: USE OF WING LENGTH AND BODY MASS ’

B.-G. CARLSSONAND B. H~RNFELDT Department of Ecology, Universityof Urned, S-901 87 UmeB, Sweden

Key words: Tengmalms’ Owl; nestlings;aging; lay- Tengmalm’s Owl (Aegoliusfunereus) nestlings, Kor- ing date; wing length:mass; food supply. pimaki (198 1) presenteddata on wing length and mass for a few nestlings,suggesting that wing length is a good Laying date is a central parameter in many ecological estimator of age in this species. studieson birds. The date of the first eggis commonly Tengmalm’s Owl is a cavity breeder readily accept- estimated by backdating during laying-from number ing nest boxes. In northern Sweden, voles are the most of eggsand laying interval. Alternatively, laying dates important prey, and the breeding successof the owls of first egg can be calculated by backdating from age reflectsvole abundance(Lijfgren et al. 1986, Homfeldt of oldest nestlingsand length of the incubation period. et al. 1990). Voles fluctuate in a three- or four-year The latter method may be advantageous,for example, cycle(e.g., Homfeldt 1978, 1994;Hijmfeldt et al. 1986). in birds which are sensitive to disturbancesduring the Here, we presentage-wing length and age-masscurves early phaseof breeding.Wing length is a good indicator for wild Tengmalm’s Owl nestlingsin northern Swe- of agein nestlingsof, for example, Willow Grouse (La- den. The resultswere obtained by measuringnestlings gopuslagopus) (Myrberget 1975) House Martin (Deli- during two years,characterized by different food (vole) chonurbica) (Bryant 1975) Ural Owl (Striw uralensis) supply.We explore the consistencyofthese parameters (Eriksson et al. 1984), Red-tailed Hawk (Buteo ja- in different yearsand thus the usefulnessof wing length maicensis)(Bechard et al. 1985) and Northern Harrier and mass for aging nestlings and determining laying (Circus cyuneus)(Saunders and Hansen 1989). For dates.

MATERIALS AND METHODS I Received 29 December 1993. Accepted 10 January The study was carried out in the county of Vlsterbot- 1994. ten, northern Sweden (approximately 64”N, 2O”E),as