The Condor96:6X-630 0 The CooperOrnithological society 1994

TESTIS MASS AND SUBADULT PLUMAGE IN BLACK-HEADED

GEOFFREY E. HILL Department of Zoology and Wildlife Scienceand Alabama Agricultural Experiment Station, FunchessHall 331, Auburn University,Auburn, AL 36849-5414

Abstract. Like males of approximately 30 other speciesof North American , male Black-headedGrosbeaks (Pheucticus melanocephalus) do not attain complete definitive alternate plumage until their second breeding season.I collected yearling and adult male Black-headed Grosbeaks in the Rio Grande valley in central New Mexico to test the hy- pothesisthat delayed plumage maturation in Black-headedGrosbeaks is one manifestation of a general, hormonally-mediated developmental pattern. I compared the mass of testes to the degreeof plumagematuration in eleven yearling males and found a significantpositive correlation. Moreover, the mean testis mass of yearling males was significantly lower than the mean testis mass of older males. In contrast, I found no significantrelationship between plumagebrightness and testis massamong sevenadult males in definitive alternate plumage. These observations support the idea that delayed plumage maturation in Black-headed Grosbeaksis part of a general delay in investment in first-year reproduction. Key Words: Delayedplumage maturation; hormones;life history: plumage color;Pheuc- ticus melanocephalus.

INTRODUCTION season, and, in recent years, a growing number Males of most speciesof temperatepasserine of studies have also begun to focus both on non- attain a definitive alternate plumage in the first breeding functions and constraints to producing spring after their birth and attempt to breed. In ornamental plumage (Rohwer and Butcher 1988, approximately 31 species of sexually dichro- Butcher and Rohwer 1989, Zack and Stutchbury matic North American passerines, however, 1992). Despite the effort that has been devoted males fail to attain a complete definitive alternate to understanding delayed plumage maturation, plumage in their first breeding season and may however, there is still no consensuson why this or may not attempt to breed (Rohwer et al. 1980, developmental pattern evolved and is main- Rohwer and Butcher 1988). In specieswith such tained (Thompson 1991, Zack and Stutchbury delayed plumage maturation, the extent to which 1992) or much data on the proximate factorsthat yearling males develop definitive plumage is determine the extent of plumage development in variable, with some individuals achieving a more yearling males. adult-male-like appearance than others (e.g., Black-headed Grosbeaks (Pheucticusmelano- Flood 1984, Hill 1988a, Enstrom 1992). More- cephalus)are typical of temperate passerinesthat over, whether or not subadult males attempt to show delayed plumage maturation. They are sex- breed is often related to the degree of plumage ually dichromatic with ASY (after second year: maturation that they display-yearlings with a in a second or later breeding season)males dis- more adult-male-like appearance are generally playing a complex, brightly colored nuptial more likely to breed than those with a more fe- plumage and with females having a much drab- male/juvenile appearance (Flood 1984; Hill ber streaked brown plumage (see Hill 1987 for 1988a, 198813;ButcherandRohwer 1989). Thus, a detailed description ofplumage). Yearling male the patterns of reproductive behavior and plum- Black-headed Grosbeaks are intermediate in ap- age development are linked in many species. pearance between females and ASY males but Numerous studies have addressed the adap- highly variable: a few nearly resemble females, tive function of subadult plumage in the breeding showing only a few features of male definitive- alternate plumage; a few look much like ASY males, showing only a few features of female/ juvenile plumage; most show a more balanced ’ ’ Received 10 December 1993. Accepted 7 March mix of ASY male and female/juvenile charac- 1994. teristics(Hill 1988a). Previous researchhas shown

f62f.4 TESTIS MASS 621

0.016’ ’ ’ ’ ’ ’ ’ ’ L 0.044 Yearling Males 0 0 Adult Males

0.012. 0 0.03. 0 0

0 0 0 0 0.02. 0 0.008. 0 0 0 0

0.004- 0 0.01. o 0 0 4 . c 25 30 35 40 45 50 52 54 56 58 60 62 64 female-like _ adult-male-like drab W bright

Plumage Brightness Score

FIGURE 1. The relationshipbetween plumage brightness and testismass corrected for body mass.Plumage brightnessof yearlingmales reflects extent of first prealtematemolt. Plumagebrightness of ASY malesreflects brightnessof orangeand yellowventral plumage.

that most yearling male grosbeaksforego breed- yearling Black-headedGrosbeaks, I compared the ing and that only thoseyearlings with adult-male- plumage scoreand testismass of the 11 SY males. like plumage defend territories and attempt to To correct for the potential confounding effects breed (Hill 1988a, 1988b, 1989). The purpose of of body size, I used testis mass divided by body the present study was to test the idea that degree mass in the comparison. I found a significant of plumage development is related to the degree positive correlation (rs= 0.9 1, n = 11, P = 0.004, of testes development and thus to test the hy- Fig. 1)-yearling males with brighter plumage pothesis that there is a proximate (hormonal) (i.e., more extensive definitive alternate plum- mechanism for the associationbetween breeding age) tended to have larger testes. behavior and plumage coloration in subadult All ASY male Black-headed Grosbeaks dis- males. play definitive alternate plumage and thus show the same pattern of nuptial plumage, but they vary substantially in plumage brightness (inten- METHODS AND RESULTS sity of ventral orange and yellow) (Hill 1987, I collected seven adult and 11 subadult male 1988a). Therefore, I also compared the plumage Black-headed Grosbeaks (Pheucticus melano- brightnessand testismass of adult males. I found cephalus)along the Rio Grande in the vicinity no significant relationship between the plumage of Los Lunas, New Mexico in May and June brightnessofASY males and testis size (rr = 0.40, 1985. For each that I collected, I scoredthe n = 7, P = 0.33, Fig. 1). The small number of plumage brightness as outlined in Hill (1987, males on which this last comparison was based 198 8a). For 16 plumage regionsI assigneda score made the power of the test weak and the chance of 0 (dullest/most female-like) to 3 (brightest/ of detecting a significant relationship low. most adult-male-like). The 16 scoreswere then Grosbeaks were collected over a 32-day inter- summed to give an estimate of overall plumage val during the peak period of nesting. To test for brightness that ranged from 0 to 48 (see Hill the potential effects of season on testis size, I 1987, 1988a for details). Immediately after being compared testis massand collecting date for both collected the birds were weighed to the nearest ASY and yearling males. There was no significant 0.1 g, and within a few hours after they were relationship between collecting date and testis collected, the birds were dissectedand both their size for either ASY (rs= - 0.33, n = 7, P = 0.42) right and left testes were removed and weighed or yearling (rs = 0.02, It = 11, P = 0.93) males. to the nearest 0.01 g. I also compared the testis mass of subadult and To see if there was a relationship between the ASY males, again correcting for body size. Adult plumage development and testis development in males had significantly heavier testesthan year- 628 GEOFFREY E. HILL

.04- % 0

.03-

0 z o- Yearling Males Adult Males

FIGURE2. Testismass of yearling(n = 11)and ASY(n = 7) maleBlack-headed Grosbeaks. Box plots illustrate IOth, 25th, 5Oth,75th and 90th percentileswith horizontallines and showall datapoints outside this range.

lings (U = 67, it = 11, 7, P = 0.01, two-tailed stimulate the development of additional struc- Mann-Whitney U Test; Fig. 2). tures and behaviors related to reproduction (Eis- ner 1960, Murton and Westwood 1977). The en- docrinological control of molt is less clear. In at DISCUSSION least one tropical species,molt is stimulated by This is the first report linking extent of yearling testosterone: subadult male Satin Bowerbirds male plumage development to testis mass in a (Ptilonorhynchusviolaceus) implanted with tes- specieswith delayed plumage maturation. Mol- tosteroneproduced definitive plumage years be- ler and Erritzoe (1988) found a similar positive fore untreated males in the same agecohort (Col- relationship between testis volume and the size lis and Borgia 1992). Yearling male Black-headed of the black throat patch in House Sparrows Grosbeaksderive their female/juvenile plumage (Passerdomesticus), a speciesin which yearling characteristicsfrom the retention of first basic males are on average less well ornamented than feathers,not by molting drab feathersduring their adults but lack a distinctive subadult plumage. first pre-alternate molt (unpubl. data). Thus, it Observations presented in this paper as well as is the extent of the first pre-alternate molt that previously published studies of Black-headed determines the degree to which yearlings attain Grosbeakssupport the idea that delayed plumage definitive plumage. For temperate bird species, maturation is part of a generalreproductive strat- fall molt seems generally to be stimulated by egy in which many features of breeding-testes thyroxin and inhibited by androgenssuch as tes- size, pre-alternate molt, timing of migration, ag- tosterone(Payne 1972). In the spring, androgens gressiveness,song output, etc.-are reduced in likely do not inhibit molt but it is unclear wheth- yearling males (Hill 1988a, 1988b, 1989). Such er or not they might directly or indirectly stim- a simultaneousdepression of multiple traits that ulate molt (Payne 1972). As stressedby Murton function in reproduction suggestssome com- and Westwood (1977:183) “. . . moult requires mon, controlling mechanism that may simulta- synergismand hence appropriate phasingof sev- neously depressall of these morphological and eral hormones.” Thus, although details of the behavioral traits. mechanism remain to be worked out and may Most of the behavioral and morphologicaltraits vary among species,it seems quite reasonable associated with reduced reproductive effort in that through hormone releases yearling males yearling male grosbeaksappear to be under hor- might coordinate expressionof reproductive be- monal control (Murton and Westwood 1977). haviors and structures. In this way, males that Testis growth is primarily under control of go- invest more in first-year reproduction produce nadotropic hormones (Murton and Westwood larger testes,grow more adult-male-like plumage 1977, Payne 1972, Morton et al. 1990). In turn, and are aggressive,while those males that invest Leydig cells of the testis produce androgensthat less produce smaller testes, retain a female-like GROSBEAK TESTIS MASS 629 appearance, and show reduced aggressiveness. adaptive function for subadult plumage per se, Such hormonal control might be simultaneous, the Fickens proposed that it was advantageous so that yearling males arrive on the breeding for yearling males to reduce their overall repro- grounds with an aggression level that matches ductive effort in their first year. The physiological their plumage, or it might be offset. In the latter mechanism by which the birds accomplishedthis case,a bird’s appearancewould affect how other was depression of levels of hormones that si- birds reacted to it, which could affect hormonal multaneously inhibited molt, reduced aggres- release and hence behavior. Either way, hor- siveness, changed migratory patterns, and gen- mones would coordinate behavior and appear- erally reduced the structures and behaviors ance. associatedwith breeding. The Fickens presented This explanation for delayed plumage matu- no data on gonad size in redstarts,but they cited ration provides a mechanism for the cryptic hy- the studiesby Miller and the Wrights, and clearly pothesis(Procter-Gray and Holmes 198 1, Studd they expected reduced testis volume to be one and Robertson 1985), one of the prominent hy- of the effectsof decreasedfirst-year reproductive pothesesthat has been proposed to explain de- investment. Recent papers searchingfor a func- layed plumage maturation. Under the cryptic hy- tional explanation for the delayed plumage mat- pothesis,reproductive opportunities for yearling uration have generally overlooked these early males are assumedto be limited, so yearling males ideas about hormonal control. For instance, Fos- benefit by reducing their investment in first-year ter (1987) reportedreduced testis size of SY males reproduction, thereby increasing their survivor- compared to ASY males in Long-tailed Mana- ship. Here, I emphasize that a common hor- kins (Chiroxiphiu lineuris)but not Swallow-tailed monal mechanism might both depress and co- Manakins (C. caudata), but she did not consider ordinate expression of a number of features that the underlying hormonal mechanisms that might affect the cost of first-year reproduction and that produce such a pattern. However, Foster (1987) subadult plumage is simply the most conspicu- as well as Lawton and Lawton (1986) did discuss ous of these features. This echoesa recent paper the phenomenon of delayed plumage maturation by Ketterson and Nolan (1992) that emphasized in the context of heterochrony, with the clear the controlling and coordinating effects of hor- implication that such a developmental pattern mones on diverse suites of morphological and would be hormonally mediated. behavioral characters. Finally, the cost of bright plumage has long The idea that delayed plumage maturation been assumed to be increased risk of predation might be symptomatic of a more general, hor- (Darwin 187 1, Lack 1954) but there is virtually monally mediated developmental pattern is not no evidence to support this assumption (seeGot- new. Long before the function and evolution of mark 1992 for a review). Recently, another cost delayed plumage maturation became a focal point to displaying bright plumage has been proposed. for behavioral and evolutionary research, three Ligon et al. (1990) and Foldstad and Karter (1992) studies proposeda link between hormone levels pointed out that expressionof many ornamental and plumage development. Wright and Wright traits is closely linked to levels of circulating tes- (1944) found that the testes of subadult Red- tosterone and that elevated levels of testosterone winged Blackbirds (Ageluius phoeniceus) mature are known to suppressimmune responsein ver- later and were only about two-thirds the size of tebrates. They proposed that this link between the testes of ASY males. The Wrights further testosterone,ornament expression,and immune suggestedthat this reduction in testes size was response provides a mechanism by which or- related to the subadult plumage displayed by namental traits signal individual quality. Only yearlings. Miller (1933) suggestedthat the vari- robust, high quality individuals would be able to ability in the plumage of yearling Phainopeplas maintain both their health and the high levels of (Phainopeplunitens) was directly related to vari- testosteroneneeded for maximum ornament ex- ation in circulating testicular hormone during pression.Although the role of testosteronein dis- molt. Finally, Ficken and Ficken (1967) formally play of bright plumage in species such as the developed a hypothesis linking testosterone, Black-headed Grosbeak is still unclear, it is in- plumage development, and reproductive behav- teresting to speculate trade-offs between hor- ior in subadult male American Redstarts (Se- mone levels, immune response, and plumage tophaga ruticilla). Rather than proposing an brightness might affect costs and promote de- 630 GEOFFREY E. HILL

laved investment in revroduction, including de- maturation in male Black-headedGrosbeaks. Auk layed plumage maturaiion. - 105:1-10. HILL, G. E. 1988b. Age, plumagebrightness, territory ACKNOWLEDGMENTS quality, and reproductive successin the Black- headed Grosbeak. Condor 90:379-388. I thank Bill Howe and Eric Breckman for help in col- HILL, G. E. 1989. Late spring arrival and dull nuptial lecting specimens.David Ligon, Lisa Ellis, David En- plumage:aggression avoidance by yearling males? Strom, and an anonymous reviewer provided many Anim. Behav. 371665-673. comments on earlier drafts of the paper. Financial sup- KETTERSON, E. D., AND V. NOLAN, JR. 1992. Hor- port for this project was provided by an E. Alexander mones and life histories:an integrative approach. BergstromAward from the Northeastern Bird-Banding Am. Nat. 14O:S33-S62. Association, a Paul A. Stewart Award from the Wilson LACK, D. 1954. The natural regulation of Omitholoaical Societv.a Frank M. Chanman Research numbers. Clarendon Press, Oxford. Grant from the American Museum of Natural History, LAWTON.M. F.. ANDR. 0. LAWTON. 1986. Heteroch- a grant-in-aid of researchfrom SigmaXi, The Scientific rony, deferred breeding, and avian sociality. Cur- Research Society, a research grant from the Western rent Ornithology 3: 187-2 19. Bird-Banding Association and Grants from the Grad- LIGON,J.D., R. THORNHILL,M. ZUK, ANDK. JOHNSON. uate Student Association and the Department of Bi- 1990. Male-male competition, ornamentationand ology at the University of New Mexico. Collecting for the role of testosteronein sexual selection in Red this study was conductedunder federal (#6809 17) and Jungle Fowl. Anim. Behav. 40~367-373. state (# 1707) permits. MILLER, A. H. 1933. Postiuvenal molt and the an- pearanceof the sexual characteristicsof plumage LITERATURE CITED in Phainopeplanitens. Univ. California Publ. Zool. 381425446. MILLER, A. P., ANDJ. ERRITZ~)E.1988. Badge,body BUTCHER,G. S., AND S. ROHWER. 1989. The evolu- and testes size in House SparrowsPasser domes- tion of conspicuousand distinctive coloration for ticus. Omis Stand. 19~72-73. communication in birds. Current Ornithology MORTON,M. L., L. E. PETERSON,D. M. BURNS,AND 6:5 l-107. N. ALLAN. 1990. Seasonaland age-relatedchanges COLLIS,K., ANDG. BORGIA. 1992. Age-related effects in plasma testosteronelevels in Mountain White- of testosterone,plumage, and experience on ag- crowned Sparrows. Condor 92: 166-173. gression and social dominance in juvenile male MURTON,R. K., ANDN. J. WESTWOOD.1977. Avian Satin Bowerbirds. Auk 109:422434 breeding cycles.Clarendon Press, Oxford. DARWIN,C. 1871. The descentof man and selection PAYNE,R. B. 1972. Mechanisms and control of molt. in relation to sex. John Murray, London. p. 103-155. In D. S. Famer and J. R. King [eds.]; EISNER,E. 1960. The relationship of hormones to Avian biology, vol. 2. Academic Press,New York. reproductivebehavior of birds, referring especially PR~cI~R-GRAY,E., ANDR. T. HOLMES. 1981. Adap- to parental behavior: a review. Anim. Behav. tive significanceof delayed attainment of plumage 8:155-179. in male American Redstarts:tests of two hypoth- ENSTROM,D. A. 1992. Breeding season communi- eses.Evolution 351742-751. cation hypothesesfor delayedplumage maturation ROHWER,S., AND G. S. BUTCHER. 1988. Winter ver- in passerines:tests in the Orchard Oriole, Zcterus sussummer explanationsof delayedplumage mat- spurius.Anim. Behav. 43~463472. uration in temperate birds. Am. Nat. FICKEN,M. S., ANDR. W. FICKEN. 1967. Age-specific 131:556-572. differencesin the breeding behavior and ecology ROHWER,S., F RETWEU,S.D.,ANDNILES,D.M. 1980. of the American Redstart. Wilson Bull. 79:188- Delayed maturation in passerineplumages and the 199. deceptive acquisition of resources.Am. Nat. 13 1: FLOOD,N. 1984. The adaptive significanceof delayed 556-572. plumage maturation in male northern orioles. STUDD, M. V., ANDR. J. ROBERTSON.1985. Life span, Evolution 32~267-279. competition, and delayed maturation in male pas- FOLSTAD,I., ANDI(ARTER, A. J. 1992. Parasites,bright serines: the breeding threshold hypothesis. Am. males,and the immunocompetencehandicap. Am. Nat. 126:101-l 15. Nat. 139:603-622. THOMPSON,C. W. 1991. The sequenceof molts and FOSTER,M. S. 1987. Delayed maturation, neoteny. plumagesin Painted Buntingsand implications for and social system differencesin two manakins of theories of delayed plumage maturation. Condor the aenus Chiroxiohia. Evolution 41:547-558. 931209-235. GZ~TMA&, F. 1992. Anti-predator effect of conspic- WRIGHT, P. L., AND M. H. WRIGHT. 1944. The re- uous plumage in a male bird. Anim. Behav. 44: productive cycle of the male Red-winged Black- 51-55. bird. Condor 46146-59. HILL, G. E. 1987. Aging and sexing Black-headed ZACK, S., AND B. J. STUTCHBURY.1992. Delayed Grosbeaksin alternate plumage.J. Field Omithol. breeding in avian social systems:the role of ter- 58:311-317. ritory quality and “floater” tactics.Behaviour 123: HILL, G. E. 1988a. The function of delayed plumage 194-219.