Behav Ecol Sociobiol (1995) 37: 249-254

250

manner. Therefore, the remaining two measures ofperformance included the variability in the acousticstructure of the alpha male's song contribution, andthe variability in the beta male's contribution. We testedthe relationship between these four properties of songperformance and female visitation rate using correla-tion and step-wise discriminant function analysis.

Methods

Instead, they attempt to show a role of sexual selec-tion in generating interpopulation and interspeciesdifferences in song (Payne 1983; Eastzer et al. 1985;Baker et al. 1987).

In our study of long-tailed manakins (Chiroxiphialinearis) we examined the relationship between songperformance and courtship success. We avoided theabove limitations by measuring four acoustic proper-ties of manakin songs independently of female songpreference. Furthermore, we tested whether courtshipsuccess of males within a population varied with thesefour measures of song performance.

The lek mating system of the long-tailed manakinsis unusual in that males display cooperatively to attractfemales to display perch-zones (lek arenas) solely forthe purpose of mating. Perch-zones are separated by75-300 m, and each is occupied by a different alphamale who is dominant to other males in the lek. Thealpha male displays most often with the beta male.Both of these top-ranking males have definitiveplumage and are usually 8 years old or older. As manyas 12 other males, including predefinitive males, maybe affiliated with a given lek. The partnerships betweenalpha and beta males develop and become stable overa period of several years (McDonald 1989a). The part-ners perform a unison song that attracts females anda joint dance that precedes copulation (Trainer andMcDonald 1993). With very rare exceptions all copu-lations are by alpha males. Alpha males from differentperch-zones vary greatly in their success at attractingfemales and at obtaining copulations (McDonald1989a, 1993b). We used the rate at which femalesvisited perch-zones as a measure of courtship success.The relationships among visitation rate, copulation rateand characteristics of the dance display were examinedelsewhere (McDonald 1989b).

The female attraction song is given by two maleswho sing nearly identical components almost in uni-son while perched 10-15 cm apart. Thejoint song ono-matopoetically resembles the word "toledo", with thefirst and last syllable sung at a flat F and the middlesyllable rising to a flat A on the diatonic musical scale.The songs of some teams sound to the human ear morecoordinated and harmonious than those of otherteams. Harmonious songs sound like one bird singing,but have a noticeably full sound, easily distinguishedfrom the rare solo songs. Non-harmonious songs sounddissonant, or out of tune, and sometimes sound poorlysynchronized. Examination of sonagrams shows thatin songs that sound harmonious to human ears, thefrequencies of the two male's components are wellmatched. Two measures of song performance, thedegree of frequency matching and the degree to whichthe two males' song contributions were synchronized,were designed to quantify the audible differences insong quality. Quality song performance probablydepends not only on the ability to sing in acoordi-nated fashion, but on the ability to sing in a consistent

The study area, in Monteverde, Costa Rica (100 18'N, 840 48'W),is 80 ha of premontane tropical moist forest (Holdridge 1966) atan elevation of 1300 m. Female visitation at seven of the most activeperch-zones was observed over 2 years. Recordings of the jointtoledo songs were made at five of the perch-zones in the 1st year,and at two additional zones the 2nd year. At each perch-zone, boththe alpha and the beta males were color banded, as well as manyof the affiliate males. The sex and age of manakins were determinedas described in McDonald (1989b, 1 993b).

Perch-zones were compared on the basis of visitation rates perunit time because sample sizes varied. Observers conducted sched-uled 2-h observations between 0600 and 1500 hours while sitting inblinds made from black plastic placed 8-12 m from display perches.From 9 to 19 scheduled observation periods were conducted at eachof the seven perch-zones. During the scheduled observations, anobserver recorded the number of females present on the perch dur-ing each 5-min block. These numbers were added over all obser-vation periods to determine the total number of female visits to theperch-zone. The relative female visitation rate at a given perch-zonein a given year was calculated as follows: number of visits per obser-vation period at that zone/total number of visits per observationperiod for all focal perch-zones during that year. In addition, toshow how visitation changed over time, we calculated the numberof visits per observation period at perch-zone Z over a period of 5years.

Toledo songs of seven alpha-beta partnerships were recordedwith a Sony WM D6C cassette recorder and a Sennheiser ME 80directional microphone. Ten songs from each team were analyzedusing a Kay Elemetrics Model 5500 Sonagraph with a grey scaleprinter. Singers were identified on the basis of their color bands.Occasionally during a bout of singing, one of the two males wouldgive a small number of solitary toledos. By analyzing the frequencycharacteristics of these solitary toledos, we were able to identify theindividual singer of each contribution to the toledo songs.

The two males of a team sing almost identical song contribu-tions, each approximately 0.6 s in duration. The song contributionsare sung nearly in unison, with one male commencing approxi-mately 0.1 s after the first male begins. In sonagrams, each male'scontribution begins at about 1700 Hz and sweeps down to form atrough, then sweeps rapidly up to form an arch, and finally endswith an element at about 1450 Hz. The trough in a sonagram hastwo nodes of highest amplitude corresponding to two dips in fre-quency (Fig. la).

Our analysis of song structure was based on samples of ten uni-son songs from each team of males. For each male, we character-ized his contribution to a toledo song by measuring four parameters:the minimum frequency reached in the first dip of the trough, theminimum frequency reached in the second dip of the trough, themaximum frequency reached in the arch, and the time intervalbetween the onset of the song and the rapid frequency ascent(Fig. Ib). To determine the minimum or maximum sound fre-quency, the Sonagraph was set to display the narrowband (15 Hz)audiospectrogram and the power spectrum of a selected O.IO-ssample. The power spectrum where the minimum or maximumfrequency occurred was displayed, and the frequency with the high-est amplitude was noted. Frequency was measured with a minimum

251

Table Variables of song performance in long-tailed manakins

Variable DescriptionN:I:~>(.)CQ);J0-Q)It

Index of frequency matching

Onset interval(singing synchrony)

0.5 1.0

Time (seconds) Song variance of alpha male(inversely related to singingconsistency)Song variance of beta male

Sum of the disparities betweenthe alpha and beta males in 3frequency parameters subtractedfrom 200

Time interval between theonsets of alpha and beta males'song contributions

Generalized variance in 4parameters of alpha male's songcontribution

Generalized variance in 4parameters of beta male's songcontribution

b2.0, C GDN

:t:~>t)CGO='c-O)

It

tested using Pearson's coefficient, r. To determine which of theabove variables best explained the variance among teams in thefemale visitation rate, we used a step-wise discriminant function.We divided the seven teams into fwO groups, one containing theteams with visitation rates above the mean (x = 0.82), and one con-taining the teams with visitation below the mean. Because the songvariables were not normally distributed, we used the rank values inthe discriminant function analysis. This analysis revealed whichvariables or combinations of variables helped discriminate betweenteams with high or low visitation rates.

A E J ~1.5

1.00.5 1.0 1.5

Time (seconds)

Fig. 1 a Audiospectrogram of a long-tailed manakin dual "toledo"song. b Drawing of the above spectrogram with the contributionof one male shown solid, and the other male shown outlined.Parameters A, B, C, and D were measured for each manakin male.D indicates the time interval between the onset and the ascendingfrequency sweep of a male's song contribution. A, B, and C indi-cate time points at which the sound frequencies were measured.These frequencies were compared to similar measurements at E, Fand G of the partner's contribution to generate the index of fre-quency matching. The index of frequency matching in Hz = 200 -(iA -EI + IB -FI + IC -GD

Results

Either male in a team could commence the duet song.In most of the teams, the alpha was the male that ini-tiated nearly all of the duet songs. However, in twoteams (A and Y), the alpha and beta males initiatedsongs about equally often. No significant differenceexisted between the song variance of alpha males(x = 19.39; SD = 2.59) and that of the beta males(x = 19.17; SD = 2.51).

There were no significant correlations among thefour variables of singing performance (Table 2). Whenall four variables were included in a discriminant func-tion analysis, average frequency matching alone wasuseful in discriminating between teams with high visi-tation rates and those with low visitation rates (step-wise discriminant function analysis; F(I.5) = 15.0;P = 0.012) (Table 3). In addition, only average fre-quency matching was significantly correlated withvisitation rate (Pearsons r = 0.92; P = 0.003) (Table 2).

After the 1st year of the study, the beta male atperch-zone Z disappeared and was replaced by thegamma male in subsequent years. This gave us theopportunity to observe the impact of a partner changeon frequency matching and courtship success. Prior tothe disappearance of the beta, team Z had the songswith the highest degree of frequency matching, high-est visitation rate (Table 2), highest song rate, bestdance, and highest copulation rate (McDonald 1989b).The replacement beta had an abnormal, incomplete

resolution of 10 Hz and time was measured with a minimum res-olution of 6.25 m. These variables could be repeated reliably formany teams of males.

To quantify the audible differences in song quality, we devisedan index of frequency matching. The index was calculated by tak-ing the sum of the disparities between the two males' song contri-bution in the three minimum and maximum frequency variables.This sum was then subtracted from 200 so that the magnitude ofthe frequency matching index would increase in magnitude as thedisparities in frequencies decreased. In addition, we measured threeother variables of singing performance (Table 1). One of these, thetime interval between the onsets of each contribution to the song,indicated the extent to which the partners' songs were synchronized.The other two variables measured the amount of variability in thesinging of each partner, and indicated how consistently each malesang his contribution to the duet song. To estimate the amount ofvariability in the singing of each male, a multivariate measure ofvariance in the four song parameters was calculated for each male'ssample of songs. The measure was calculated as the log of the deter-minant of the variance/covariance matrix of the four parameters(Sneath and Sokal 1973). To ensure that each parameter wasweighted equally, the time interval measurements (ms) were multi-plied by 10 so that they would have a magnitude similar to the fre-quency measurements (Hz).

The correlations among female visitation rate, average frequencymatching index, average onset interval between song contributions(synchrony), song variance of alpha, and song variance of beta were

252

Table 2 Correlation (Pearsonscoefficient, r) matrix amongfemale visitation rate and fourvariables of song performancein long-tailed manakins

Frequency matchingOnset intervalSong variance IXSong variance p

0.92-().45-0.59-0.03

0.0030.310.170.95

-0.53

-0.53

-0.30

0.220.220.95

0.550.40

0.280.38 0.57-0.26

Table 3 Female visitation and song performance variables of long-tailed manakins. (+) designates visitation rates above the mean

(x = 0.82); ( -) designates visitation rates below the mean.The num-bers in parentheses are ranks

Songvariance ;x

Team Visitationrate

Average frequencymatching

Average onsetinterval

Songvariance P

16.8 (6)21.1 (3)22.0 (2)18.1 (4)16.4 (7)22.2 (1)17.6 (5)

0.10.10.10.]0.]0.]0.]

18.3 (5)19.3 (4)15.0 (7)18.0 (6)20.6 (3)22.1 (2)22.4 (I)

17411710799829146

abnormal song contribution of the new male did notcontain the analogous elements necessary for compar-ison with his partner's contribution, an index of fre-quency matching could not be computed. Figure 2shows the complete lack of frequency matching in thedual song. The number of visits per observation perioddeclined dramatically during the new male's first sea-son as beta, and continued to decline over the next fewyears (Fig. 3). Copulations per observation period fellfrom 0.41 in year 1 to 0 in succeeding years, after thenew beta male took over.

2.0

J::>u 1.5c:~:JC"..It

0.5 1.0 1.5

Time (seconds)

Fig. 2 Audiospectrogram of the song of team Z in 1986. The abnor-mal song contribution of the beta male occurs above approximately1.75 kHz

Discussion

"0.g 3.00 I

0)Co 2.50

CII.00 2.00

'Q;Co 1.50CII...

:§ 1.00>0)

"iij 0.50E0)

LL. 0.00

YearFig. 3 Decline in female visitation at perch-zone Z after the replace-

ment of the beta male in year 2

song, about 300 Hz higher in frequency than that ofany other male sampled. Not only was the degree offrequency matching in the songs of the new teamextremely low, songs were not as loud and were deliv-ered from perches closer to the ground. Because the

The measure of song performance that most directlyaccounted for the harmonious sound of well-coordi-nated manakin song \,!,as frequency matching. Songswith extremely poorly matched frequency not onlysound dissonant to human ears, but sound unsyn-chronized as well. The apparent lack of synchrony wasnot due to unusually long intervals between the onsetsof the two males' song contributions; onset intervalswere similar in harmonious and unharmonious songs.Rather, the frequency mismatch renders the temporaloffset between the two males' contributions more per-ceptible, making the song sound less synchronous.Likewise, the amount of variability in the singing ofalpha and beta males was not related to the degree offrequency matching. All males in this sample weredefinitive (at least 4 years old) and sang quite con-sistently. Frequency matching appears to be the bestmeasure of how harmonious and coordinated manakinsongs sound to the human ear.

Teams of long-tailed manakins with songs that werewell matched in terms of frequency attracted more

1011,21

119102127

134

(6)(5)(3)(4)(7)(2)(1)

(1)(2)(3)(4)(6)(5)(7)

253

propagate would be less than this for two reasons. First,temporal overlap of matched frequencies is not perfect,so the intensity of a dual-male song is probably notdoubled at the source. Second, sound intensity atten-uates considerably in a dense forest (Wiley andRichards 1978), and this excess attenuation is linearwith distance. Thus, the increased distance of audibil-ity of a dual song would be somewhat less than thetheoretical maximum of 1.41 times as far. Therefore, iffemale visitation preferences were based solely on audi-bility, a male with a partner might potentially attractmore females than a solitary male, but the benefit islikely to be considerably less than a twofold increasein visitation. Solitary songs are rare, however, and ourinterest is in whether duet songs with close frequencymatching may propagate further than poorly matchedsongs. It seems unlikely that a small difference in fre-quency matching would increase the area of audibilityenough to impact the rate of female visitation, espe-cially since temporal overlap of the two males' songcontributions is imperfect in both well and poorlymatched songs. It is more likely that active choice byfemales explains the higher visitation at perch-zoneswhere well matched songs are heard.

Frequency matching may provide females with anunambiguous ideal against which dual-male perfor-mance can be judged. Like the morphological charac-ters assessed under fluctuating asymmetry arguments(Watson and Thornhill 1994), frequency matching hasa clear maximum of perfect matching. Thus, dual-maleperformances provide females with the opportunity forenhanced discrimination among potential mates.Furthermore, such performances may provide femaleswith a criterion useful in assessing the quality of poten-tial mates.

The expression of frequency matching may be re-lated to the cooperative abilities of the participatingmales. The partnership between an alpha and beta maledevelops over several years. Young, predefinitive malesinitially participate in several partnerships, fluidly mov-ing among perch-zones (McDonald 1989a). In this way,they become established in a dominance system inwhich status increases with age. As males grow olderand their status relationships become better defined,they spend more time displaying at fewer perch-zones.The dominance hierarchy at a perch-zone appears tofunction as a queue of variously aged males awaitingopportunities to move into beta and alpha positions(McDonald 1993a). By the age of about 8 years, malestend to be established in stable, long-term partnershipsas beta males. As long as these queues remain orderly,little overt aggression is observed. The orderliness ofqueues may be reinforced by female choice, sincefemales seldom remain in a perch-zone while chasingamong males occurs. Opportunities for males to movebetween queues, however, appears to be limited byaggression, particularly among the younger males(McDonald 1993a). We have some evidence to suggest

females. Neither the degree of synchrony nor the con-sistency with which team members sang was related tothe ability to attract females. Although a significantrelationship between visitation rate and frequencymatching is suggestive, it is insufficient to allow us toconclude that well matched singing per se causes highvisitation by females. Females may have been respond-ing to other correlated behavioral cues. For example,teams of males that sang more persistently attractedmore females (McDonald 1989b), and this may havebeen the primary basis for females' choice of perch-zone. Characteristics of the duet song, includingamount of output, appear to be important in deter-mining which perch-zones a female will visit. Once shearrives in the display area, characteristics of the dance,including a "butterfly" display, appear to determinewhether or not she will choose to mate with the alphamale (McDonald 1989b). Nevertheless, our results sug-gest that females may have a preference for songs witha high degree of frequency matching.

Song quality in long-tailed manakins is a functionof the behavior of two males. Mate choice based on adual-male phenotype is an intriguing possibility, espe-cially since one of the males does not mate. The suc-cess of the alpha male may depend on the ability ofhis partner to sing in a coordinated fashion. The effectof the non-mating partner on courtship success wasillustrated the year that the beta partner disappearedfrom team Z, the most successful partnership in thestudy area. Visitation and copulation rates declinedwhen the alpha male established a partnership with amale whose song was abnormal. The individual phe-notype of the formerly extremely successful alpha maledid not change, yet females ceased responding to hiscourtship. The change in the dual-male phenotype,therefore, is most likely to explain this decline incourtship success.

The above observations raise questions about theevolution of mate choice based on a dual-male pheno-typic character. How does a dual-male character suchas frequency matching help a female find or select amate? We consider two possibilities, which are notmutually exclusive: frequency matched songs are moreaudible than unmatched songs, or frequency matchingprovides females with a criterion useful in assessing thequality of potential mates.

By matching sound frequencies, two males may pro-duce a song with up to 2 times the intensity of thatsung by a single male (a fourfold increase in intensitytheoretically is possible if coherent sound waves areproduced by two closely spaced sources; however, thedistance between manakin singers, 10-15 cm, is toolarge for such near-field interference to occur). A dualsong with twice the source intensity would be audiblefrom a maximum of 1.41 times as far (sound intensitydecreases in proportion with the square of the dis-tance), and would be audible over twice the area. Inreality, the additional distance a manakin song could

254

that frequency matching may be related to the dura-tion of a partnership. First, frequency matching in-creases with age of the younger partner. Second, songsof established teams of males have better frequencymatching than songs resulting from randomly com-bining the measurements of individual males' song por-tions to form artificial teams (J.M. Trainer andD.B. McDonald, unpublished work). Because partnersare not genetically related (McDonald and Potts 1994),frequency matching is very unlikely to result fromgenetic similarity. These observations suggest that jointsongs of established teams become better matched asthe partnership develops.

Thus, females may be able to acquire informationabout the duration and stability of an alpha male's part-nership from the degree of frequency matching in hisjoint songs. A male whose songs have a higher degreeof frequency matching has demonstrated that he hassurvived eight or more years, acquired sufficient statusto be a member of an established team, has the abilityto perform highly coordinated courtship display, andexhibits the tolerance of other adult males necessaryto form a stable partnership. To the extent that thesequalities are heritable, females may benefit from choos-ing males with a high degree of frequency matching.Our studies of the long-tailed manakin help us under-stand how mate choice based on dual-male phenotypemight have evolved.

Acknowledgments This project was funded by NSF grant BNS-8814038 to J.M.T., a Jessie Smith Noyes Foundation grant fromthe Organization for Tropical Studies, the Frank M. Chapman fundof the American Museum of Natural History and the AmericanPhilosophical Society. D.B.M. is grateful to the Harry FrankGuggenheim Foundation, the Organization for Tropical Studiesand the National Geographic Society for support. Joe and JeanStuckey graciously permitted the use of their farm as a study site.Members of the Monteverde community have helped in many ways.Personnel in the offices of Vida Silvestre were remarkably courte-ous, prompt and helpful in securing necessary permits. We thankPeter Hoekje for discussions of acoustics.

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