SHORT COMMUNICATIONS
The Condor96:552-555
0 The Cooper OrnithologicalSociety1994
ADAPTIVE
SIGNIFICANCE
MANUCODES
OF TRACHEAL
ELONGATION
(PARADISAEIDAE)’
IN
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. kerauThe five speciesof manucode Manucodia (including drenii, in M. atra, M. chalybata,M. jobiensisand M.
comrii this adaptation occursonly in males and is limPhonygammus)(Diamond 1972, Beehler and Finch
ited to elongationof a singleloop. The degreeof elon1985) are monogamous and sexually monomorphic,
glossyblue-black, and are medium-to-large passerines gation varies, in these four, being shortestin M. atra,
which has the highest-pitched call, and longest in M.
of the family Paradisaeidae.They are confined to forcomrii, the call of which has been describedas moumests of New Guinea, certain satellite islands and tropful and low (Beehler et al. 1986).
ical northeasternAustralia (Cooperand Forshaw 1977,
Beehler (unoubl.
data) noted sexualdimornhism in
Beehler et al. 1986, Coates 1990). Of the 37 other,
. conspicuouslysexually dimorphic, birds-of-paradise calls of M. keraudrenii, in which males give a low,
(two monomorphic Paradigalla spp. excepted), 35 are tremulous, hollow note that is answeredby the female
known or presumedto reproducepolygamously.In the with a harsh, coughing,higher-pitchednote; and in M.
latter 35 species,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,Coates1990, higher-pitched woo-oh woo-ohwoo-ohwoo-oh.
Clench (1978) noted that while Manucodia is the
Frith 1992, Frith and Frith 1990, 1992, 1993a, 1993b
and unpubl. data). The remaining two speciesconsti- only passerinegenus in which looped tracheal elongation is known, it is found in a number of non-pastute the little-known monotypic, sexually monomorserinegenera.To assessthe possiblesignificanceof this
phic and monogamous genera Macgregoria and Lyanatomical adaptation in Manucodia, it is helpful to
cocorax.
Manucodes are of considerable interest within the review looped tracheal elongation in non-passerines.
Paradisaeidaebecausethe two speciesthat have been
studied are monogamous and non-territorial, range CRACIDAE
widely, and are gregarious,fig-eatingspecialists(BeehAn elongatedtrachea, located subcutaneouslyatop the
ler 1983, 1985, Beehler and Pruett-Jones 1983). In
contrast, most monogamouspasserinesare 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 amplispp. (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
calls. In some speciesof Cracidae, the elongatetrachea
have’a simple, straight trachea‘ihat develops with increasingageinto an elongate,coiled and looped trachea is exclusiveto 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 females (which have a shorter looped tracheathat bends TETRAONIDAE
laterally acrossthe pectoral musclesbut may not form
Male Rock Ptarmigan(Lagopusmutus),in which some
I Received 21 September 1993. Accepted 2 December 1993.
males are monogamouswhile others are polygynous,
have an elongate,looped trachea that gives their calls
a markedly lower pitch than those of females (Macdonald 1970, Cramp and Simmons 1983).
15521
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553
While not elongatedor looped, dissectionof a single
specimen indicates that the trachea of adult male
Twelve-wired Birds of Paradise(Seleucidismelunoleuca is modified by having eight rings (fourth to eleventh
from the bottom) “slightly dilated and flattenedanteroposteriorly” to be broader and ossifiedalongtheir center. This contraststo their broad cartilaginousborders.
The ossifiedcenter of each ring is slightly concaveand
the interval betweenthesepeculiar ringsis much deeper than those above and consistsof a delicate memNUMIDIDAE
braneto make this modified lengthofthe tracheahighly
In monogamousAfrican guineafowl of the genusGutelastic and “probably correlated with the very loud
harsh note of these birds” (Forbes 1882b).
tera, both sexeshave an elongatedtrachea looped into
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
umbrellabirds (Cephalopterusspp.), and the Calfbird
eruni), which has a call lower in pitch than that of its
(Perissocephulus
tricolor) is modified by being anteonly congenerG. plumifera (Urban et al. 1986). Macriorly expanded. This is greatestin males, to enhance
lean (1985) describedthe call of G. pucherunias “deep“booming” or “bellowing” advertisement/displaycalls
er and more resonant than that of Helmeted Guine(Snow 1982).
afowl” (Numida meleanris).
Severalobservershave noted the deep, loud, or farGRUIDAE
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 associatedsternal modifica1969, Diamond 1972, Anon. 1972, Cooper and Fortion. These correlate with loudness, penetration and
shaw 1977. Coates 1990. Beehler 1991, and oers. obfar-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 Mandefinite 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 dispecies,those with a longer trachea do show less flucsyllabicnote of about 0.3 secondsduration (Coates in
litt.) with the quality of a deep woodwind or brass
tuation of frequencies(Johnsgard1983a).
instrument.
ROSTRATULIDAE
Clench (1978) suggestedthat Manucodia speciescan
Females of the polyandrousPainted Snipe (Rostratula physiologically“afford a greatly elongatedtrachea bebenghalensis)have a subcutaneoustracheal loop that cause they are sedentary (non-migratory) and, being
relatively large forest birds, their daily flight distances
lies partly on the pectoral muscles(Newton 1899, Niethammer 1966). This enablesthem to producea 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
is now known that M. keraudrenii is a peculiar paspossible.
serine in being monogamous,but non-territorial and
ANSERANATIDAE
specializingon feedingupon figs(Beehler 1985). These
The male Magpie Goose (Anserunussemipalmata)has fruits may not be economicallydefendabledue to their
an elongatedsubcutaneoustracheathat 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 bird
in the male (Marchant and Higgins 1990, contra is not sedentaryto the usual extent of territorial and
monogamouspasserines.Rather, it rangeswidely and
Schoddeand Tidemann 1988).
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 speresonanceof 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 sameasin thosenon-passerines
(Scott 1972).
in which it is found: to produce amplified calls with a
lower pitch (as speculatedby Clench 1978) for comDISCUSSION
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 pobirds with an elongatedlooped trachea produce calls lygynousand polyandrousspeciesor to maintain conthat 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 taxomodification. The modified trachea apparently allows nomically diversenon-passerinesstronglysuggests
that
communication over relatively greater distances.
the same function may underlie its origin in a bird-ofMale Capercaillie (Tetrao urogallus),large, polygynous grouse,have a trachea lengthened into a simple
loop (Newton 1899,Johnsgard1983a).Males call loudly
from a traditional courtship area to attract multiple
mates.Moss and Lockie (1979) demonstratedthat male
Capercaillie calls contain a high level of sound at low
frequency that humans cannot hear and that the carrying power of this part of the call has been underestimated.
554
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BOCK,W. J. 1963. Relationships between the birds
of paradise and the bowerbirds. Condor 65:91125.
CHAPIN,J. P. 1932. The birds of the Belgian Conao.
Vol. 1. Bull. Am. Mus. Nat. Hist. 65:1-756. CLENCH,M. H. 1978. Tracheal elongation in birdsof-paradise. Condor 80:423-430.
COATES,
B. J. 1990. The birds of PapuaNew Guinea,
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FRITH, C. B. 1992. Standardwing Bird of Paradise
Semioptera wallucii displaysand relationships,with
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 constructhe King of Saxony Bird of ParadisePteridophoru
tively commenting on a draft of this contribution and
alberti nest, egg and nestling, with notes on pato Glen Ingram for kindly providing literature.
rental care. Bull. Brit. Omithol. Club 110:160164.
FRITH,C. B., ANDD. W. FRITH. 1992. Nestingbiology
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__ , and
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paradise. Thus, an elongated trachea in adult Munucodiu may have evolved as a meansof malesattracting
a mate(s) or to allow these non-territorial birds to
maintain contact among nairs or flock members while
searchinga largeforagingarea. What appearto be manucodecontact notesare relatively simple and are higher-pitched than what are considered to be advertisement calls (Coates 1990). Studies are required to
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notes.
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Society 1994
DETERMINATION
OF NESTLING AGE AND LAYING DATE IN
TENGMALM’S
OWL: USE OF WING LENGTH AND BODY MASS’
B.-G. CARLSSON
AND B. H~RNFELDT
Department of Animal Ecology, Universityof Urned,S-901 87 UmeB,Sweden
Laying date is a central parameter in many ecological
studieson birds. The date of the first eggis commonly
estimated by backdating during laying-from number
of eggsand laying interval. Alternatively, laying dates
of first egg can be calculatedby backdating from age
of oldest nestlingsand length of the incubation period.
The latter method may be advantageous,for example,
in birds which are sensitiveto disturbancesduring the
early phaseof breeding.Wing lengthis a goodindicator
of agein nestlingsof, for example, Willow Grouse (Lagopuslagopus)(Myrberget 1975) House Martin (Delichonurbica)(Bryant 1975) Ural Owl (Striw uralensis)
(Eriksson et al. 1984), Red-tailed Hawk (Buteo jamaicensis)(Bechardet al. 1985) and Northern Harrier
(Circus cyuneus)(Saunders and Hansen 1989). For
Tengmalm’s Owl (Aegoliusfunereus) nestlings, Korpimaki (198 1) presenteddata on wing length and mass
for a few nestlings,suggestingthat wing lengthis a good
estimator of age in this species.
Tengmalm’s Owl is a cavity breeder readily accepting nest boxes. In northern Sweden,voles are the most
important prey, and the breeding successof the owls
reflectsvole abundance(Lijfgren et al. 1986, Homfeldt
et al. 1990). Voles fluctuate in a three- or four-year
cycle(e.g.,Homfeldt 1978, 1994;Hijmfeldt et al. 1986).
Here, we presentage-winglengthand age-masscurves
for wild Tengmalm’s Owl nestlingsin northern Sweden. The resultswere obtained by measuringnestlings
during two years,characterizedby different food (vole)
supply.We explore the consistencyofthese parameters
in different yearsand thus the usefulnessof wing length
and mass for aging nestlings and determining laying
dates.
I Received 29 December 1993. Accepted 10 January
1994.
MATERIALS AND METHODS
The study was carried out in the county of Vlsterbotten, northern Sweden (approximately 64”N, 2O”E),as
Key words: Tengmalm’s Owl; nestlings;aging;laying date; wing length:mass;food supply.