The Condor93~935-942 0 The CooperOrnithological Society I99 1

HORMONAL CORRELATES OF BOWER DECORATION AND SEXUAL DISPLAY IN THE (PTILONORHYNCHUS VIOLACEUS)’

GERALD BORGIA Department of Zoology, Universityof Maryland, CollegePark, MD 20742

JOHN C. WINGF~ELD Department of Zoology, Universityof Washington,Seattle, WA 98195

Abstract. Male Satin Bowerbirdscourt females with complexdisplays that includestick structuresbuilt adjacentto a decorateddisplay court. Here we reportcirculating levels of testosteroneand corticosteronein a naturalpopulation of SatinBowerbirds and their relation to the developmentof complexmating displays.We found that (1) maleswithout bowers had lowerlevels of testosteronethan bowerholders, (2) testosterone,but not corticosterone, levelswere significantly correlated with male mating success,and (3) levelsof testosterone, but not corticosterone,were consistentlycorrelated with the quality of severalimportant displaycharacters that have been shownto be importantin affectingmale mating success. Theseresults suggest that testosteronelevel is an important componentof male mating success.We considerreasons why variation in testosteronelevels persistsamong mature male bowerbirdsgiven its potentialto affectmale mating success. Key words: Sexual display;Bowerbird; hormone; testosterone; ;Ptilonorhyn- thus violaceus:corticosterone.

INTRODUCTION work has shown that female Satin Bowerbirds Male Satin Bowerbirds (Ptilonorhynchusviola- prefer males with well-constructed and well-dec- ceus),like many species in the family Ptilono- orated bowers (Borgia 1985a), and that male rhynchidae, have developed complicated court- competition by destruction of other male’s bow- ship displays oriented around a bower, a stick ers (Borgia 1985b) and theft of decorations (Bor- structure that they build and decorate (Vellenga gia 1985b) affects display characters important 1970; Donaghey 1981; Borgia 1985a, 1986). in female choice. Young males associate with Courtship displays at the bower involve harsh older males at bowers and may learn some ele- calls, vocal mimicry, and jumping or “dancing” ments of display behavior (Vellenga 1970, Borgia postures(Loffredo and Borgia 1986). Naturalists 1986, Loffredo and Borgia 1986). have long been curious about the peculiar nature There is considerable evidence for the role of of these displays, and recently bowerbirds have the steroid hormone testosterone in regulation attracted the attention of evolutionary biologists of male-aggressivenessand courting behavior in becausethey provide a model system for under- (Balthazart 1983, Harding 1981, Harding standing the of complex symbolic sex- et al. 1988, Hegner and Wingfield 1987, Wing- ual displays. Investigations of the development field 1984) although this has not been true in all of male display behavior have revealed that there cases(e.g., Rohwer and Wingfield 1981; Wing- is age-relatedimprovement in male displays(Lof- field et al. 1982a, 1987). These studies involved fredo and Borgia 1986; Borgia, in preparation) investigations of specieswith relatively sim- and that male dominance may be important in ple courtship displaysand resource-basedmating determining male ability to obtain and hold a systems in which male successin obtaining a display site (Borgia 1985b; Borgia and Gore 1986; mate is primarily dependent on territory quality. Borgia and Loffredo, in preparation). Previous Bowerbirds have a non-resource-based mating system, and female choice appears almost en- tirely dependent on the quality of male display. I Received25 February 1991. Final acceptance30 Investigation of courtship behavior in male Satin May 1991. Bowerbirds is of special interest because the

19351 936 GERALD BORGIA AND JOHN C. WINGFIELD’ unique mating systemallows numerous elements taining matings. We also evaluate the possible of male display to be quantified, and the devel- relationship between hormone levels and male opment of thesedisplay components can be mea- advertising and bower destruction tendencies. sured in relation to hormone levels. Castration of Ptilonorhynchusviolaceus impairs bower METHODS building and displays to females, whereas tes- This study was carried out at Wallaby Creek, in tosterone injections partially restore these be- the Beaury State Forest, 120 km NW of Lismore, haviors (Marshall, 1950), suggestinga major role New South Wales, , and the study site for testosteronein social behavior of this species. has been described elsewhere (Borgia 1985b). Furthermore, becausemale bowerbirds can mate Satin Bowerbirds at Wallaby Creek have been with many different females in a season,there is the subject of an intensive field study from 1980 an opportunity to score the relative quality of to 1987, and general information about the birds male display independently of other factors such was collected over that period. Data for the com- as those found in speciesin which territory qual- parisons reported here were collected from Au- ity affects mating decisions. gust 1984-December 1984. Recent studiesofjuvenile plumage Satin Bow- Birds were captured in baited traps and re- erbirds show that testosteronecan have a critical moved immediately. The birds were color-band- role in determining male successin aggression ed (if not previously captured), scoredfor plum- around feeding sites and in adult male plumage age characters and numbers of ectoparasites, development (Collis and Borgia 1990, 1991). weighed, measured for wing length, and imme- Testosterone-implanted juvenile males showed diately released. Plumage characters and mea- an increased tendency to build bowers, perform surements of wing length allowed sexing and ag- displays and related behaviors, and molt into ing of birds (Vellenga 1970). Individual birds adult plumage, when these birds were compared were banded with unique combinations of col- with a control group. However, the behaviors of ored bands. Our records allowed us to estimate implanted birds were uncoordinated and these the ages of males based on when they obtained birds were not tolerated by bower-holding males. adult plumage. Males exhibit a green female-like These resultssuggest that, although adult-like be- plumage with dark beaks until four years of age, haviors can be induced by testosteroneimplants, at which time the beak begins to gradually turn these birds suffer from an inability to produce completely yellow. At five years, males exhibit fully coordinated behaviors, and, becauseof their a mottled blue and green plumage which, after early attainment of adult plumage, they may be the final molt, becomes entirely blue at seven denied opportunities to observe displays of older years of age. We classified individual males as males. Thus, it is possible that a combination of juveniles if they were less than seven years old. hormonal factors (e.g., testosterone) and hor- Male ranks were establishedby observation of mone independent factors (e.g., experience) may male interactions at trapping sites. We recorded regulate courtship and bower construction in Sat- the identity of birds that were involved in inter- in Bowerbirds. It is also possible that circulating actions, including the band combinations of birds corticosteronelevels may be important since this that initiated and received the attack. Aggres- adrenocortical steroid hormone is known to sup- sivenesswas measured as the ratio of the number pressreproductive behavior either directly or in- of attacks by a bird to the total number of en- directly by inhibiting secretion of reproductive countersby a bird. Encounters are the total num- hormones (e.g., Wingfield and Silverin 1986, ber of times a bird was an attacker plus the num- Wingfield 1988). ber of times it was attacked. This aggressiveness In this study we report levels of testosterone index was used to order males into ranks. Our and corticosterone in individual male birds of aggressivenessindex was highly correlated with different age classesin a wild population. We dominance value (see Collis and Borgia 1990, compare juvenile plumage and adult males and 199 1; Borgia and Loffredo, MS) based on a total assessage-related changes in testosterone and of 2,176 interactions recorded in 1984. corticosterone levels. We test the specific pre- Each permanent bower site was monitored by dictions that circulating concentrations of these a camera controlled by an infrared device that two hormones affect the performance of bower- was triggered when birds entered the bower (see holding males in producing displays and in ob- Borgia 1985a, 1986a). Matings occur in the bow- TESTOSTERONE AND BOWER DECORATION 931 er, and our camera system provided continuous coated charcoal. Standard curves covered the monitoring at bowers through the entire mating range 2-500 pg for testosterone and 7.8-2,000 season. Behavioral observations including be- pg for corticosterone.All sampleswere processed havior around the bower and male advertising within a single assay, and intra-assay variation and display calls were made from hides located was < 10%. For further details of procedure, as- 15 m from the bowers. Male mating success, say validation, and reliability criteria see Wing- number of courtships, and identity of visitors field and Famer (1975); Wingfield et al. (1982b); were determined by review of films (Borgia Ball and Wingfield (1986). 1985a). Females typically mate once per season. STATISTICAL ANALYSIS Rarely females mated twice with a male without moving out of the bower and these were scored Spearman rank correlations (r,), Student’s t-test as a single mating. (t), and combined probability tests (Sokal and Nine categories of decorations were counted Rohlf 1969) were used for statistical compari- and bower quality estimates were made on daily sons. Means are expressed as x & SD except visits to bowers (see Borgia 1985a). These data where noted. One-tailed tests were used for ini- were reduced by taking seasonal means of dec- tial comparisons of testosterone and corticoste- orations counts to representvalues for individual rone levels with male and mating successand for decoration variables. In 1984, one-half of the other tests of a priori predictions. bowers on the study site were regularly destroyed as part of another experiment. Measures of bow- RESULTS er quality are based on mean estimates of bower HORMONE LEVELS AND CLASS quality in the three week period preceding the Differences in testosteronelevels were found be- experimental bower destruction experiment. To tween bower-holding and nonbower-holding test if this experiment affected the results re- males (Fig. la) and these were statistically sig- ported here, we compared treatment and control nificant (t = 2.9, df = 23, P < 0.03). Similar bowers and found no significant difference in tes- trends were found for corticosterone levels be- tosterone levels (t = 1.18, df = 13, P > 0.30). tween bower-holding (Fig. 1b) and nonbower- holding males, but they were not significant (t = HORMONE ANALYSIS 1.43, df = 23, P > 0.10). Blood samples for hormonal analysis were taken as birds were captured at feeding sites in 1984. HORMONE LEVELS AND MATING SUCCESS The birds were captured in cage traps that were We predicted that testosterone levels might be operated by a hidden observer who removed and significantly correlated with male mating success processedthe bird immediately after capture.Two and this result was supported (r, = 0.47, n = 14, to four heparinized capillary tube (75 mm x 1.4 P = 0.023, Fig. 2) however there was no signif- mm i.d.) blood samples were taken from wing icant correlation with corticosterone levels (r, = veins punctured by a 27 gauge hypodermic nee- 0.22, n = 14, P = 0.111, Fig. 3). There was no dle. All of the birds in our sample had been correlation with rank as determined by aggres- captured numerous times before blood samples sive interactions at feeding sites with either tes- were taken. Birds with a previous history of hav- tosterone (Y, = 0.009, n = 14, P > 0.50) or cor- ing been captured tended not to struggle when ticosterone (r, = -0.253, II = 14, P = 0.19) levels, handled, and most returned to the vicinity of the and number of copulations were marginally cor- trap immediately after releasewith no noticeable related with rank (r, = 0.33, n = 14, P = 0.065). effecton their behavior. Blood sampleswere cen- There was no significant correlation between cor- trifuged, and the serum and RBC fractions were ticosterone and testosteronelevels (r, = 0.173, n separated and held on ice until they could be = 14, P > 0.25). frozen. Samples were transported frozen on dry ice to the laboratory for analysis. HORMONE LEVELS AND The steroid hormones testosteroneand corti- DISPLAY CHARACTERS costerone were measured by radioimmunoassy Visitation and courtship at bowers were both after partial purification of steroid fractions on strongly associatedwith hormone levels (Table diatomaceousearthglycol microcolumns. Bound 1). There was a strong positive correlation be- and free moieties were separated by dextran- tween testosteronelevels and visitation at males’ GERALD BORGIA AND JOHN C. WINGFIELD

a 16 6 ” = 15

1 - 6 .

5 6 .

5 z 4 . . . . . 2 . . . . 0 0 2 4 6 0 10 12

Testosterone w/ml 1 BOWER NO BOWER FIGURE 2. Circulating testosteronelevels and male b mating successin 1984. 501 terone and individual decoration variables (Ta- 40 ble 3) were combined. Each decoration type had a positive correlation coefficient, and when com- bined, there was a highly significant association 30 between decorations and testosterone levels (combined probability test x2 = 49.7, df = 18, P 20 -c 0.001). Adjusting for multiple comparisons (by dividing by the number of contrasts) caused 10 these individual comparisons to become nonsig- nificant. None of the nine individual decoration

0 types showed a significant (unadjusted) correla- BOWER NO BOWER tion with corticosterone (Fig. 4) and correlation FIGURE 1. Plasma levels of testosterone(a) and cor- coefficients show no clear pattern (only six of ticosterone (b) in males with and without bowers. nine of these are in the positive direction). Male advertising. Table 4 shows the relation- ship between advertising calls and hormone lev- bowers, the number of courtships by a male and els. Neither the frequency of scratch or whistle courtships without copulations. Negative cor- calls showed significant correlations with testos- relations were found for corticosteronelevels and terone or corticosterone levels. these same variables. Two of four bower quality variables (Table 2) 16- were significantly correlated with testosterone, but none showed correlations with corticoste- 14-- z 12.. rone. The high Pvalues for theseprobability tests .s suggestthat these results are robust even with + 10.. multiple comparisons. A combined probability e . 0 a-- test showedthe overall correlation ofbower vari- % ables and testosteronewas highly significant (x2 j 6-- . E = 26.36, df = 8, P < 0.005). z' 4.. . . . The summary variable for decorations (the to- 2...... tal number of decorations) was positively cor- 07 related with testosterone levels (r, = 0.64, n = 0 10 20 30 40 50 60 70

14, P = 0.01) but not corticosterone (r, = 0.161, Corticosterone N = 14, P = 0.15). This result is also supported w/ml in an analysis in which results from Spearman FIGURE 3. Circulatingcorticosterone levels and male correlations based on contrasts between testos- mating successin 1984. TESTOSTERONE AND BOWER DECORATION 939

TABLE 1. Relationships of plasma testosteroneand corticosteronelevels to behavior at the bower.

Visitors and display Corticosterone Testosterone Spearm(an=cw$ation Spearmancorrelation n P (n = 14) P

Total visitors at bower -0.521 0.013 0.333 0.032 Total courtshipsat bower -0.452 0.023 0.531 0.006 Courtships without copulations -0.531 0.012 0.410 0.017

Bower destruction.Table 5 shows the relation ticosterone were less often significant than those between hormone levels and the frequency that involving testosterone. a male was a victim of bird-caused destructions Display variables that showed significant neg- and the number of times he was a destroyer. ative correlations with corticosterone levels also There was no relationship between corticoste- showedsignificant positive correlations with tes- rone or testosteroneand the number of times a tosterone. Courtship displays of Satin Bower- male was a destruction victim. Male tendency to birds have been suggestedto be energetically de- destroy was negatively correlated (marginally) manding because of the extreme postures taken with corticosterone levels, but showed no rela- by males. These include puffing of feathers, tionship to testosteronelevels. harshness of their calls, and the protrusion of their eyes (Marshall 1954, Vellenga 1970, Lof- fredo and Borgia 1985). However, the observa- DISCUSSION tion that display activity is inversely related to Our results, which show a significant correlation corticosteronelevels suggeststhe possibility that of male mating successwith levels of testoster- active displaying by males is not severely stress- one, are consistent with the hypothesis that tes- ful. This implies that, contrary to earlier sugges- tosteroneaffects male mating success.Additional tions and what is implied from some recent sex- comparisonsshowed that testosteronelevels were ual selection models (Zahavi 1975; Lande 198 1; marginally correlated with rank. There was no see Borgia 199 1 for a full discussion) male Satin significant correlation of testosterone or corti- Bowerbird displays are not costly in terms of costerone with absolute male age, but bower- impairing overall male function or survivorship. holding males (a group that includes the oldest This result is supported by the observation that males) had higher testosterone and corticoste- successfulmale Satin Bowerbirds tend to live rone levels than other males. There were signif- longer and have high quality displays relative to icant positive correlations between testosterone other males (Borgia 199 1). The inverse relation- levels, and male ability to attract females to bow- ship between corticosteroneand male display be- ers for courtship, two measuresof bower quality, havior is also consistent with the hypothesis that and the number of decorations on bowers. This male display itself may lower stressin males (but overall pattern suggestsan important effect of see Marler and Moore 1988; Moore and Marler testosterone on display and mating in the satin 1987, 1988). If so,this may account for the com- bowerbird. In general, contrasts involving cor- mon tendency among male Satin Bowerbirds to

TABLE 2. Relationships of plasma testosteroneand corticosteronelevels to bower quality.

Bowerquality measures* Corticosterone Testosterone Spa-man correlation Spearmancorrelation (n = 14) P (n = 14) P

Bower symmetry -0.039 ns -0.258 0.10 Bower stick size -0.212 ns -0.622 0.012 Bower stick density -0.002 ns -0.505 0.016 Bower quality of construction -0.188 ns -0.261 0.10

*The highestquality bowersreceived the low scoresso a negativecorrelation indicates a positive relationshipbetween hormone level and bower quality. 940 GERALD BORGIA AND JOHN C. WINGFIELD

TABLE 3. Relationships of plasma testosteroneand corticosteroneto bower decorations.

Bowerdecoration Cmticosterone Testosterone Spearman SpeXILUl correlation correlation (n = 14) P (n = 14) P

Yellow leaves 0.129 0.165 0.380 0.045 Yellow straw 0.013 0.24 0.498 0.017 Blue feathers 0.232 0.11 0.140 0.16 Blue blossoms -0.369 0.05 0.084 0.19 Snail shells 0.141 0.16 0.346 0.055 Yellow blossoms 0.123 0.17 0.435 0.03 Man made objects -0.178 0.14 0.326 0.065 Cicadas -0.122 0.17 0.399 0.04 Other natural obiects 0.016 0.25 0.127 0.16 display in bowers with no other birds present. males nor produce high quality displays. Simi- Another possibility is that males who fail to dis- larly in the red-winged blackbird, Aegelanius play do so becausethey are intimidated by other phoeniceus,implants increase the likelihood that males. they would obtain a territory and mates (Beletsky The observed correlations support a model et al., 1990). suggestingthat intrapopulational differences in The tendency for male Satin Bowerbirds to testosteronelevels can account for differencesin frequently practice displays (Loffredo and Borgia male ability to produce display characters and 1986), the long delay in their attainment of sec- ultimately affect male reproductive success.It ondary sexual traits, and the finding that older should be noted, however, that the correlations males produce the highest quality displays (Bor- involving testosterone levels generally failed to gia 1986, Borgia, in preparation) support the hy- explain a large proportion of the total variation pothesis that experience is critical for high male in either male display charactersor mating suc- mating success.High levels of testosteronemight cess.This suggeststhat a simple increase in tes- then only be one of several determinants of male tosterone levels may not be sufficient to cause mating success.Marshall (1950) also showedthat large changesin male reproductive success.Al- testosterone injections only partially restored ternatively, daily cycling in testosteronemay have bower-building behavior, suggestingthat other contributed to variation in measured levels of factors may also be involved. testosteroneand thereby reduced the total level This model may explain why males have not of variation that could be explained in our com- evolved to produce high levels of testosteroneat parisons. a young age. Increasesin testosteroneproduction The experiments described above involving in immature males might be costly in forcing implants of testosteronein juvenile males (Collis them into high risk activities before they have and Borgia 1990, 199 1) showedsignificant effects sufficient experience to produce a display com- on male aggressionagainst other juvenile males. petitive with those of older and more practiced Even so, implanted juvenile males with levels of males (seeCollis and Borgia 1990). The variation circulating testosteronein excessof adult plum- in testosteronelevels explained only a relatively age males could not dominate the adult plumage small part of the total variation in male success

TABLE 4. Relationships of plasma testosteroneand corticosteroneto male advertising behaviors.

Advertking calls Corticosterone Testosterone Spearman Spearman correlation P correlation P

Whistle call frequency 0.270 0.09 0.149 0.24 Scratch call frequency 0.154 ns 0.070 ns TESTOSTERONEAND BOWER DECORATION 941

120- TABLE 5. Relationshipsof plasmatestosterone and 110.. . . corticosteronelevels to bowerdestruction. E lOO-- . .2 go-- Natural bower destructions ao-- e Cortlcosterone TeStOSteIOlK 8 70~. Spearman Spearman d 60 -- z l . correlation P correlation P 2 50..-- . . f 40 Destructionvictim -0.234 ns -0.109 ns z 30.- . -0.405 0.05 -0.252 ns . Destrover 2O . Two-talled tests. lo-- 0.. . Ot 1 0 2 4 6 8 10 12 terone levels and seasonalcycling of testosterone

Testosterone levels with large increases occurring in antici- ns/ml pation of the mating season(see Marshall 1954). FIGURE 4. Circulatingtestosterone levels and the Increases of testosterone in anticipation of the total number of bowerdecorations in 1984. breeding seasoncould be induced by male-male competition over bower sites (see Wingfield and Moore 1987), a point not addressedin this study. (and less than decoration variables, see Borgia 1985a), suggestingthat testosteroneand experi- ACKNOWLEDGMENTS ence may act independently to affect male mating This researchwas supportedby funds to G.B. from success.This view is further supported by pat- the AmericanPhilosophical Society, the Harry Frank terns among variables showing strong correla- GuggenheimFoundation, the National ScienceFoun- tions with testosteronelevels that tended not to dation(BNS 81-13477,BNS 83-08154,BNS-85-10483 and BSR-89114 1 l), the Dean of Life Sciencesand the be those that measure artistic experience. Thus, GraduateSchool of the Universitv of Marvland. and stick density, stick size, and total numbers of the University of MarylandComp;ter ScienceCenter. decorations that show strong correlations with J.C.W.was supported by grantsfrom the National Sci- testosteronelevels, all require that males be very enceFoundation (DCB 83 16155 and DCB 86 16189). active in pursuing specific types of sticks or dec- ChristineLevesque provided expert assistance with the hormoneassays. We areindebted to the many vol- orations, but do not directly reflect male expe- unteerassistants who helpedcollect field data and to rience. By contrast, variables such as quality of the J. and E. Hayes,Mulkay, and Bell families who bower construction show nonsignificant corre- allowedaccess to their propertiesand providedmuch lations with testosteronelevels even though this kind assistance.The New SouthWales Forestry Com- missionallowed access to the BeauryState Forest. M. is one of the best predictors of male reproductive J. Littlejohn, J. Hook, and membersof the Zoology success(Borgia 1985a, in preparation). Departmentof the University of Melbourneprovided Our findings from earlier studies showing an critical support.We thank Ken Collis and Lois Read important role for bower quality, bower deco- for their reviewsof this manuscript. ration and male display affecting male mating success(Borgia 1985, Loffredo and Borgia 1986) LITERATURE CITED and testosterone-implant studies showing an in- BALL, G. F., AND J. C. WINGFIELD. 1987. Changesin creasein theseactivities in juvenile birds suggests plasmalevels of luteinizinghormone and sexste- that testosterone may be part of an enabling roid hormonesin relation to multiple-brooded- nessand nestsite density in male starlings.Phys- mechanism that allows the correct level of ex- iol. Zool. 60:191-199. pression of these traits by males that differ in BALTHAZART, J. 1983. Hormonal correlatesof be- dominance and experience. While it may be pos- havior, p. 221-365. In D. S. Famer, J. R. King, sible that mating experience is the cause of high and K. C. Parkesleds.1, Avian biology,-. Vol. 7. testosterone-levels (e.g., Wingfield and Moore Academic Press, New York. BELETSKY. L.. G. H. ORIANS. AND J. C. WINGFIELD. 1987) that hypothesis would less adequately ex- 1990: Elects of exogeno;s androgenand antian- plain both increasesin display behavior by im- drogenon territorial and non-territorial red-winged planted juvenile males (Collis and Borgia 1990) blackbirds (Aves:Zcterinae). Etholoav 85:58-72. and changes in male mating successat bowers BORGIA, G. 1985a. Bower quality, number of deco- rations and mating successof male Satin Bower- where decorations have been manipulated (e.g., birds (Ptilonorhynchusvioluceus): an experimental Borgia 1985, Borgia in preparation). Moreover, analysis. Anim. Behav. 33~266-271. it leaves unresolved the function of high testos- BORGIA, G. 1985b. Bower destruction and sexual 942 GERALD BORGIA AND JOHN C. WINGFIELD

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