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2007

Plumage development and molt in long-tailed manakins (chiroxiphia linearis): variation according to sex and age

Stéphanie M. Doucet University of Windsor

David B. McDonald

Mercedes S. Foster

Rob P. Clay

D. B. Lank

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Recommended Citation Doucet, Stéphanie M.; McDonald, David B.; Foster, Mercedes S.; Clay, Rob P.; and Lank, D. B., "Plumage development and molt in long-tailed manakins (chiroxiphia linearis): variation according to sex and age" (2007). The Auk, 124, 1, 29-43. https://scholar.uwindsor.ca/biologypub/1113

This Article is brought to you for free and open access by the Department of Biological Sciences at Scholarship at UWindsor. It has been accepted for inclusion in Biological Sciences Publications by an authorized administrator of Scholarship at UWindsor. For more information, please contact [email protected]. PLUMAGE DEVELOPMENT AND MOLT IN LONG-TAILED MANAKINS (CHIROXIPHIA LINEARIS): VARIATION ACCORDING TO SEX AND AGE Author(s): Stéphanie M. Doucet, David B. McDonald, Mercedes S. Foster, and Rob P. Clay Source: The Auk, 124(1):29-43. Published By: The American Ornithologists' Union https://doi.org/10.1642/0004-8038(2007)124[29:PDAMIL]2.0.CO;2 URL: http://www.bioone.org/doi/full/10.1642/0004-8038%282007%29124%5B29%3APDAMIL %5D2.0.CO%3B2

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. The Auk 124(1):29–43, 2007 © The American Ornithologists’ Union, 2007. Printed in USA.

PLUMAGE DEVELOPMENT AND MOLT IN LONG-TAILED MANAKINS (CHIROXIPHIA LINEARIS): VARIATION ACCORDING TO SEX AND AGE S M. D,1,5 D B. MD,2 M S. F,3 R P. C4,6 1Department of Biological Sciences, 401 Sunset Avenue, University of Windsor, Windsor, Ontario N9B 3P4, Canada; 2Department of Zoology and Physiology, University of Wyoming, Laramie, Wyoming 80721, USA; 3U.S. Geological Survey Patuxent Wildlife Research Center, National Museum of Natural History, 10th and Constitution Avenue NW, Washington, D.C. 20560, USA; and 4Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, United Kingdom

A.—Lek-mating Long-tailed Manakins (Chiroxiphia linearis) exhibit an unusual pa ern of delayed plumage maturation. Each year, males progress through a series of predefi nitive plumages before a aining defi nitive plumage in their fi h calendar year. Females also exhibit variation in plumage coloration, with some females displaying male-like plumage characteristics. Using data from mist-net captures in northwest Costa Rica (n = 1,315) and museum specimens from throughout the range of Long-tailed Manakins (n = 585), we documented the plumage sequence progression of males, explored variation in female plum- age, and described the timing of molt in this species. Males progressed through a series of age-specifi c predefi nitive plumages, which enabled the accurate aging of predefi nitive-plumaged males in the fi eld; this predefi nitive plumage sequence is the basis for age-related status-signaling in these males. Females tended to acquire red coloration in the crown as they aged. However, colorful plumage in females may be a byproduct of selection on bright male plumage. Females exhibited an early peak of molt activity from February to April, li le molt from May through July, and a second, more pronounced peak of molt activity in October. By contrast, males in older predefi nitive-plumage stages and males in defi nitive plumage exhibited comparable unimodal distributions in molt activity beginning in June and peaking between July and October. Our data are consistent with selective pres- sure to avoid the costs of molt–breeding overlap in females and older males. Our fi ndings have important implications for social organization and signaling in Long- tailed Manakins, and for the evolution of delayed plumage maturation in birds. Received 20 May 2005, accepted 5 January 2006.

Key words: Chiroxiphia linearis, cooperation, delayed plumage maturation, hierarchy, leks, Long-tailed Manakin, plumage coloration.

Desarrollo del Plumaje y Muda en Chiroxiphia linearis: Variación de Acuerdo al Sexo y la Edad

R.—En Chiroxiphia linearis se presenta un patrón inusual de maduración retardada del plumaje. Cada año, los machos pasan por una serie de plumajes predefi nitivos antes de acanzar su plumaje defi nitivo en su quinto año calendario. Las hembras también exhiben variación en la coloración del plumaje: algunas presentan características del plumaje similares a las de los machos. Empleando datos de capturas

5E-mail: [email protected] 6Present address: BirdLife International, Vicente Cárdenas E5-7S y Japón, 3er Piso, C. P. 17-17-717, Quito, Ecuador. 29 30 D . [Auk, Vol. 124

hechas con redes de niebla en el noroeste de Costa Rica (n = 1,315) y especímenes de museo de todo el rango de distribución (n = 585), documentamos la secuencia de plumajes progresivos de los machos, exploramos la variación en el plumaje de las hembras y describimos el momento en que tiene lugar la muda en C. linearis. Los machos progresaron a través de una serie de plumajes pre-defi nitivos específi cos para cada clase de edad, lo que permitió determinar la edad de los machos sin plumaje defi nitivo con exactitud en el campo. Esta secuencia de plumajes predefi nitivos es la base para la señalización del estatus entre los machos, que está relacionada con la edad en esta especie. Las hembras tendieron a adquirir coloración roja en la corona a medida que envejecieron. Sin embargo, el plumaje colorido en las hembras podría ser un subproducto de la selección por plumaje brillante en los machos. Las hembras exhibieron un pico temprano de actividad de muda entre febrero y abril, poca muda entre mayo y julio y un segundo pico más pronunciado de actividad de muda en octubre. En contraste, los machos en estadíos de plumaje predefi nitivo más avanzados y en plumaje defi nitivo exhibieron distribuciones unimodales de actividad de muda comparables comenzando en junio, con un pico entre julio y octubre. Nuestros datos concuerdan con la existencia de una presión selectiva para evitar los costos del sobrelapamiento de la muda de las hembras y de los machos más viejos. Nuestros hallazgos tienen implicaciones importantes relacionadas con la organización social y la señalización entre individuos de C. linearis, y también para la evolución de la maduración retardada del plumaje en las aves.

I , males do not assume defi ni- 1995; VanderWerf 2001; Mulder et al. 2002; tive, adult-like plumage for one or more years DuVal 2005). Investigations of the adaptive sig- a er hatching. In some species, this delay in nifi cance of delayed plumage maturation, and plumage maturation is accompanied by a delay of the signal function of variation in plumage, in sexual maturation (Lawton and Lawton require a thorough understanding of plumage 1986). In many sexually dichromatic, north- development and molt. Here, we investigate temperate passerines, however, males do not age- and sex-related plumage variation in the a ain their defi nitive plumage until a er their Long-tailed Manakin (Chiroxiphia linearis). fi rst potential breeding season, despite having Long-tailed Manakins have a lek-based mating reached sexual maturity (Rohwer et al. 1980, system (Foster 1977; McDonald 1989a, b). Males Lyon and Montgomerie 1986). The adaptive gather at lek sites, where they establish age- signifi cance of this type of delayed plumage graded dominance hierarchies. The two most maturation has been the focus of extensive dominant males at each lek, the alpha and beta research in recent decades (e.g., Rohwer et al. males, perform vocal duets and elaborate, dual- 1980, Lyon and Montgomerie 1986, Hill 1996), male dance displays for females visiting the leks. with most studies investigating the one-year Females usually copulate only with alpha males delays typically exhibited by north-temperate (Foster 1977, McDonald 1989b, McDonald and passerines. However, many tropical passerines Po s 1994). As in other lekking species (Höglund deviate from this pa ern. In some species, such and Alatalo 1995), females are solely responsible as bowerbirds and birds of paradise, males molt for rearing off spring (Foster 1976). into the same predefi nitive plumage for sev- As they grow older, male Long-tailed eral years before assuming defi nitive plumage Manakins progress through a series of tran- (Frith and Beehler 1998, Frith and Frith 2004). In sitional, predefi nitive plumage stages before other species, for example manakins, Darwin’s a aining defi nitive plumage in their fi h fi nches, paradise fl ycatchers, Hawaiian hon- calendar year (Foster 1987; McDonald 1989a, eycreepers, and monarch fl ycatchers, males 1993a). This delay is unusually long for such a progress through a transitional series of dif- small (15–21 g) passerine (Lawton and Lawton ferent predefi nitive plumage stages before 1986). Female Long-tailed Manakins also vary assuming defi nitive plumage (Foster 1987; in plumage color, with some females develop- McDonald 1989a, 1993a; Lepson and Freed ing red or tawny crown feathers, a trait believed January 2007] Plumage and Molt in Long-tailed Manakins 31 to be associated with age (McDonald 1989b). (Stiles and Skutch 1989). All three sites exhibit Such extensive age- and sex-based variation in marked seasonality, with a dry season extend- plumage may present unique signaling oppor- ing from approximately January through April, tunities, particularly in species with complex and a rainy season extending from May through social organization (Lawton and Lawton 1986). December. Male Long-tailed Manakins display In Long-tailed Manakins, for example, a male’s actively from February through September, position within a lek hierarchy may be largely with a pronounced peak in activity from March infl uenced by his age. Thus, transitional plum- through June (Foster 1977; McDonald 1989a, b, ages that reliably signal a male’s age or status 1993b). Active nests have been discovered from in the hierarchy would likely reduce the occur- March to July (Foster 1976; S. M. Doucet unpubl. rence of costly, escalated encounters between data), though the nesting season likely extends males of low and high status (Foster 1987, until September (Foster 1976). McDonald 1993a). We captured 1,315 Long-tailed Manakins Foster (1987) described predefi nitive male using mist nets and fi ed each individual with plumages in Long-tailed Manakins as transition- a unique combination of plastic colored leg ing through several stages along a continuous bands; birds at Monteverde and Santa Rosa spectrum, with second-year males being mostly also carried a numbered aluminum leg band. green with a red crown patch and, occasionally, Of 20 birds banded as nestlings, only 2 were some black on the face, coverts, and body and recaptured or resighted in following years (one fl ight feathers, and third- and fourth-year males male and one female). To determine the plum- having a mixture of red, green, black, and blue age sequence followed by birds as they aged, plumage. McDonald (1989a, 1993a) proposed we recorded detailed descriptions of each bird’s an alternative sequence, whereby males prog- plumage coloration each time it was captured. ress through a transitional series of age-specifi c Whenever possible, we also recorded plumage predefi nitive plumages; in this proposed descriptions of marked individuals seen during sequence, males develop a red crown in their behavioral observations at lek sites or encoun- second year, a black mask in their third year, tered opportunistically at the study sites. Over and a blue mantle in their fourth year. Using the course of the study, R.P.C. and M.S.F. noted recapture and resighting data from three study that second-year birds of both sexes could be populations, together spanning 27 years, we re- identifi ed by the presence of retained juvenal examined the plumage sequences proposed by wing feathers; R.P.C. also discovered that the Foster (1987) and McDonald (1989a, 1993a) to mouth-lining color of second-year birds was determine whether predefi nitive male plumage diagnostic (Clay 2001). Thus, we examined the can reliably signal age in Long-tailed Manakins. mouth-lining color and the amount of wear on Additionally, we investigated pa erns of varia- wing feathers of all green-plumaged birds cap- tion in female plumage and described sex- and tured from 1997 to 1999 and in 2005. Only a sub- age-based variation in the timing of molt. set of the data we present here was described briefl y elsewhere (plumage sequence informa- M tion from 56 males; McDonald 1989a, 1993a). To assess the timing of molt, we examined all We studied Long-tailed Manakins at three birds captured from 1971 to 1977, some birds sites in northwestern Costa Rica: from 1971 to captured in 1986 and 1987, and all birds cap- 1974 and in 1977 at the Enrique Jiménez Nuñez tured since 1995 for signs of molt (i.e., sheathed Experiment Station (10°20’N, 85°8’W); from 1981 feathers), recording whether birds were molting to 1999 in Monteverde (10°18’N, 84°48’W); and at time of capture and noting in which regions from 2003 to 2005, as well as for a few weeks in of which feather tracts they were molting. 1986, in Santa Rosa National Park, Guanacaste Occasionally, we noted extremely asymmetric Conservation Area (10°40’N, 85°30’W). The molt or molt of only a single, isolated feather Monteverde site is located in premontane tropi- on some individuals. We assumed in both cal moist forest (Holdridge 1966), and the Santa instances that the molt was adventitious and Rosa and Jiménez Station sites encompass both did not include these individuals in our calcula- evergreen bo omland moist forest and areas tions of proportions of birds molting (Pyle 1997, of tropical dry forest on surrounding hillsides VanderWerf 2001). Although most birds were 32 D . [Auk, Vol. 124 captured and observed between March and July, R we collected molt information on wild birds in all months except September and February. Molt.—All Long-tailed Manakins underwent To obtain additional molt data spanning the a prebasic (postbreeding) molt each year. The calendar year, we also examined 585 Long- olive-green juvenal plumage grown in the nest tailed Manakin specimens in museum collec- was identical in males and females. The fi rst pre- tions (see Acknowledgments). We recorded basic molt began within four months of fl edging feather regions and tracts with molting feath- and was a partial molt: hatch-year birds of both ers and, if discernible, the plumages from sexes retained some of their juvenal wing feath- which and into which a bird was molting. ers. Thus, second-year birds had two genera- Many museum specimens were also examined tions of wing feathers: retained juvenal remiges for the presence of juvenal remiges and coverts. and distal greater coverts, and new lesser and Taken together, our data from museum speci- median coverts and proximal greater coverts. mens and wild birds spanned the calendar Additionally, the mouth linings of second-year year, though some months are considerably birds were bright orange to orange-yellow, simi- be er represented than others. Molt and plum- lar to those of nestlings (Foster 1976), whereas age terminology follow the Humphrey-Parkes the mouth linings of older birds were paler and (H-P) system (Humphrey and Parkes 1959) as more pinkish in color. All subsequent prebasic summarized in Pyle (1997). A recent review molts were complete. (Howell et al. 2003) recommends modifi cations Male plumage sequence.—Overall, we captured to H-P terminology. The complex nature of and marked 653 individuals in Monteverde, 280 molt in Long-tailed Manakins, however, makes individuals at the Jiménez Station, and 382 indi- it diffi cult to assign consistent molt terminol- viduals in Santa Rosa. Many of these birds were ogy to diff erent sex and age classes under the recaptured or resighted in one or more subse- proposed changes. Thus, for simplicity, we quent years, which allowed us to document 562 opted for traditional H-P terminology. We also plumage transitions from a total of 235 males. Of follow Pyle’s (1997) age terminology. Thus, a these transitions, 343 were successive molts in hatch-year is a bird in its fi rst calendar year defi nitive plumage, whereas 219 were molts from (until 31 December of the year it fl edged), a one predefi nitive plumage to another or from second-year bird is in its second calendar year predefi nitive to defi nitive plumage. Of these (from 1 January to 31 December of the year fol- 219 informative transitions, we have records for lowing fl edging), a third-year bird is a bird in two diff erent plumage stages for 98 males, three its third calendar year, and so on. diff erent plumage stages for 32 males, and four Wild birds in all-green or primarily green diff erent plumage stages for 19 males. One male plumage were identifi ed as females if they had was sighted in all fi ve plumage stages. a vascularized brood patch, were recaptured or Males progressed through the following resighted in green plumage in multiple years, plumage sequence (Fig. 1 and Tables 1 and 2). were aged as a er-second-year birds on the basis They acquired their juvenal plumage in the nest, of the absence of retained juvenal wing feathers which, like the plumage of females, was olive (see above), exhibited female-like behavior dur- green above with a paler wash below. Within ing dance displays by males (McDonald 1989a), four months of fl edging, males initiated their fi rst or were identifi ed as such either by genetic sex- prebasic molt. Males in their fi rst basic plumage, ing (Griffi ths et al. 1998) or by laparotomy. Birds which we term “red-cap plumage,” were olive in green plumage were identifi ed as males if green throughout with a small red crown patch. they were recaptured or resighted in predefi n- The amount of red in the crown was highly itive or defi nitive male plumages in subsequent variable, and males o en had two strips of red years or by laparotomy. For museum specimens, feathers on the outer edges of the crown rather green birds were identifi ed as females or males than a contiguous red crown patch (Fig. 2A). A only if the specimen tag indicated the pres- limited number of males in red-cap plumage also ence of ovaries or testes, respectively. Birds in had some black feathers on the face. These black green plumage that did not meet these criteria feathers, or additional ones, were acquired along were considered of unknown sex and were not with an expanded red crown in some males dur- included in our analyses. ing a partial molt (either a limited prealternate January 2007] Plumage and Molt in Long-tailed Manakins 33

Fl. 1. Typical appearance of birds in different plumage stages: (A) female or male in juvenal plumage, (B) male in red-cap plumage, (C) male in black-face plumage, (D) male in blue-back plumage, and (E) male in definitive plumage. Photograph (E) courtesy of Richard Laval. molt or the early onset of the second prebasic plumage,” were mostly olive-green with a molt; see below) in March and April. In addi- small red crown patch and a black facial mask tion, some males undergoing the fi rst prebasic or hood. In this plumage, the red crown patch molt replaced their central, but no other, rectrices was always contiguous and was larger than that (M. S. Foster unpubl. data). These rectrices were of red-cap males but smaller than that of males darker and longer than those retained from the in defi nitive plumage. The amount of black on juvenal plumage. the face varied from a small black facial mask In the following year, males underwent their to a full black hood. Some black-face males also second prebasic molt. Males in their second had some black in their coverts and fl ight feath- basic plumage, which we term “black-face ers, and a blackish tinge to their body plumage. 34 D . [Auk, Vol. 124

T 1. Plumage development in male Long-tailed Manakins. Plumage descriptions summarize the typical appearance of males in each plumage stage.

Age Plumage Name of range a Age name b stage plumage stage Plumage description 0–4 hatch-year juvenal juvenal Olive green throughout with paler wash below 4–15 second-year fi rst basic red-cap Olive green body and fl ight feathers; partial red crown 15–27 third-year second basic black-face Olive green body and fl ight feathers; small red crown; black face or hood 27–39 fourth-year third basic blue-back Black and green body and fl ight fea- thers; red crown; blue and green mantle ≥39 ≥ fi h-year defi nitive-basic defi nitive Black body and fl ight feathers; red crown; blue mantle a Months since hatching. b Calendar year; age terminology follows Pyle (1997); see text for explanation.

T 2. Summary of sequential plumage tran s i t ions recorded in male Long-tailed Manakins.

Plumage transitions Recorded instances (n) Typical Green to red-cap 1 Red-cap to black-face 60 Black-face to blue-back 60 Blue-back to defi nitive 48 Defi nitive to defi nitive 343 Potential anomalies Green to black-face 2 Red-cap to blue-back 2

Rarely, males in black-face plumage had a lim- ited number of blue feathers on their mantle. Males in their third basic plumage, which we term “blue-back plumage,” had a mixture of green and black body and fl ight feathers, a full red crown patch, and some blue feathers on the mantle. Birds in blue-back plumage exhibited the greatest range of variation in proportions of plumage colors, though all exhibited some blue in the back, and some black ventrally. O en, blue-back males had body feathers that were mostly black with a tinge of olive-green and fl ight feathers that were black with green edg- ing. Some blue-back males had very li le green Fl. 2. (A) A young male Long-tailed Manakin at all in their plumage and might be mistaken in red-cap plumage and (B) a female Long-tailed for defi nitive-plumaged males in the fi eld. Manakin with some partly red crown feathers. Other blue-back males had substantial amounts Note differences in the distribution of red on of green in their black body plumage, giving the crown, the distribution of red on individual them an almost grayish appearance. feathers, and the length of red crown feathers. January 2007] Plumage and Molt in Long-tailed Manakins 35

Finally, males in defi nitive-basic plumage aberrant bird, captured in red-cap plumage and had entirely jet-black body and fl ight feathers, without any black on its body, had a larger red a sky-blue mantle, and a bifi d, red crown patch. crown, a well-developed black hood (but no other A small number of males molting from blue- black body feathers), and a small area of blue black plumage to defi nitive plumage retained feathers on the back the following year. Thus, minimal amounts of green on the rump, fl anks, ≤0.7% of plumage transitions deviated from the or undertail coverts. This green disappeared expected pa ern. Even if we exclude transitions during the following prebasic molt. between defi nitive plumage stages, these anoma- Four lines of evidence allow us to assign ages lies account for only 1.8% of plumage transitions. to these sequences. First, one male banded as a These anomalies invariably involved an acceler- nestling was recaptured or observed in three ated plumage-maturation process, because no subsequent years: in his fi rst prebasic molt, he male ever remained in the same plumage stage acquired the red-cap plumage; in his second for two subsequent years. In 96 instances, more prebasic molt, the black-face plumage; and in than one year elapsed between recaptures or his third prebasic molt, the blue-back plumage. resightings of particular males. Even among (Unfortunately, this male was not resighted these nonsequential transitions, males were again until his sixth calendar year, when he was always in the expected plumage category when in defi nitive plumage.) Second, all red-cap males they were eventually recaptured or resighted, as captured between 1997 and 1999 at Monteverde estimated from the number of years separating (32 individuals) and in 2005 at Santa Rosa (11 recaptures or resightings. individuals) were identifi ed as second-year Female plumage.—Female Long-tailed Man- birds on the basis of retained juvenal remiges akins are typically olive-green above with a and distal greater coverts and mouth lining paler wash below. However, of the 649 con- color. Third, we documented the full, four-year fi rmed females examined (including museum progression of 17 males from red-cap plumage specimens), 145 (23%) had variable amounts of to defi nitive plumage. Finally, all males observed tawny or red feathers on the crown, ranging in red-cap plumage invariably had black feathers from a single feather to a full tawny or red crown. on the face in the following year. Similarly, all The presence of red in the crown of females may males observed in black-face plumage had blue make it diffi cult for inexperienced observers feathers on their mantle the following year. No to diff erentiate them from young males in red- male observed in defi nitive plumage was ever cap plumage. However, the red crown feathers observed to have green feathers in subsequent of females can be distinguished from those of years. Our observations suggest that this plum- males by one or more of the following charac- age sequence is unidirectional, nonreversible, teristics (Fig. 2). First, the red feathers of females and remarkably age-specifi c. o en had a tawny or rusty appearance, a feature Of the 562 plumage transitions we recorded, never observed in males. Second, the red color 465 were sequential (i.e., the males were was o en present on only some of the barbs of recaptured or resighted in the following year). each feather in females, while the remainder of These sequential transitions allowed us to assess the feather remained green, thereby creating a the frequency of unexpected plumage transi- slightly streaked appearance (Fig. 2A). By con- tions. We documented only four unusual plum- trast, the red feathers of young males usually age transitions. Two males were fi rst captured in had red distal barbs, and red, orange, or yellow all-green plumage and both were recaptured in central and proximal barbs, regardless of the black-face plumage the following year (Table 2). number of red feathers on the crown (Fig. 2B). Because these males were captured in March and Third, the red feathers of females were usually April as green males but in the following breed- the same length as the other (green) feathers on ing season as black-face males, it is possible that the crown, whereas the red feathers of males they showed red in the crown during some of the were usually longer than the green feathers and interval between these records. A third otherwise tended to increase in length with age (Fig. 2; S. M. all-green male was molting in a limited black Doucet pers. obs.). Fourth, the distribution of red mask and red crown when it was captured in feathers on the crown diff ered between females April. A year later, a er a single prebasic molt, it and males. In females, red feathers could be was in blue-back plumage. A fourth presumably found in the front, center, or rear of the crown. By 36 D . [Auk, Vol. 124 contrast, among males in red-cap plumage, the distribution of the proportion of birds molting red feathers tended to grow on the outer edges over the course of the year, with an early peak of the crown, o en resulting in a split, rather than of molt activity in March and a second peak in contiguous, red crown (Fig. 2A). October (Fig. 3A). The molt occurring between Development of tawny coloration in the February and April is limited to some head and crown of females appeared to be associated body feathers, whereas the second peak corre- with age. Of the females we were able to age as sponds to the complete prebasic molt. The early second-year or a er-second-year (on the basis peak varies by age. Of the females examined in of plumage and mouth lining color), none of March and April that we were able to age (n = 43 second-year females had any trace of red or 81), 13 of 15 (86%) second-year females showed tawny on the crown, whereas 91 of 189 a er- signs of molt, whereas only 25 of 66 (38%) second-year females had traces of tawny or red a er-second-year females showed signs of molt (Fisher’s exact test, P <0.00001). Of the females (Fisher’s exact test, P = 0.0003). Unfortunately, that exhibited changes in plumage color during our data do not allow us to determine whether the course of the study, nine were observed or this early peak corresponds to a limited preal- recaptured suffi ciently frequently to estimate ternate molt or whether it is an early beginning the minimum amount of time elapsed between to the prebasic molt that is suspended through when the bird was originally captured and the reproductive period. This distinction would when a change in plumage was fi rst noted require confi rmation that newly molted feathers (mean ± SD = 5.1 ± 1.17 years). Two of these were replaced in the subsequent prebasic molt females were fi rst captured as second-year (in the case of a limited pre-alternate molt) or females; one of these developed a tawny crown not replaced in the subsequent molt (in the case in her eighth year, and the other developed red of an early suspended prebasic molt). crown feathers in her ninth year. Some females The molt activity pa erns of males in pre- never developed red or tawny crowns, includ- defi nitive plumage are more complex. We sepa- ing the three oldest, minimum-age females. Two rated males by plumage stage, which generally were recaptured in completely green plumage corresponds to age (see Table 1, and above). As 10 years a er initial capture. A third female, last with females, a large proportion of red-cap (sec- observed 15 years a er her initial capture, had ond-year) males showed signs of molt in March no discernible red or tawny in her crown. and April (Fig. 3B). Among these young males, In rarer instances, females departed from there was a slight decrease in molt activity in the typical olive-green plumage in other ways. May. By July, however, all red-cap males cap- During the course of our study, we captured a tured or examined showed signs of molt. Of the few females with black lores or black forehead, red-cap males showing signs of molt in March cheek, or nape feathers (n = 21); with one or more and April (n = 28), 82% were molting only crown partially or completely black wing or tail feathers or head feathers. Three of these males (11%) (n = 11); or with blue or black wing or tail coverts were molting both head and body feathers, and or blue mantle feathers (n = 5). Apart from crown two others (7%) were molting only body feath- color, none of these patches was extensive enough ers. Many of these red-cap males were molting to be seen easily in the fi eld. Females with some in additional red crown feathers and some were tawny or red coloration in the crown were signifi - molting in black feathers on other parts of the cantly more likely to show these additional male- head. In some cases, however, these males were like plumage tendencies (28 of 147) than females simply molting in green crown or head feath- that were otherwise all green (6 of 504; Fisher’s ers. The peak of molt in June corresponds to exact test, P < 0.00001). Two of the females that the complete fi rst prebasic molt: males were in had black or blue on the body were recaptured in a much heavier molt that o en included fl ight subsequent years and no longer had black or blue feathers. Among black-face (third-year) and in their plumage. By contrast, all females with a blue-back (fourth-year) males, we detected molt red or tawny crown that were recaptured in sub- in only a small percentage of males (13%) in sequent years retained a colored crown. March and April (Fig. 3C, D). As with red-cap Timing of molt.—Long-tailed Manakins fol- males, this early molt in black-face and blue- low a complex pa ern of molt that varies by back males was largely restricted to the crown age and sex. Among females, there is a bimodal and head regions. Black-face and blue-back January 2007] Plumage and Molt in Long-tailed Manakins 37

Fl. 3. Monthly proportions of Long-tailed Manakins showing signs of molt at time of capture for birds in different plumage stages. Data are from mist-net captures in northwestern Costa Rica (n = 867) and museum specimens (n = 585). Data are pooled across years, and numbers above bars indi- cate total number of birds captured in each month. (Although plumage stages are indicated on each graph, letters are included to facilitate referencing in the text and comparisons with Figure 1.) males exhibited a peak of molt activity between documented age- and sex-related variation in June and August, which corresponded to their plumage maturation and molt timing in Long- complete third and fourth prebasic molts, tailed Manakins. Male plumage development respectively. progressed in discrete, age-specifi c categories Males in defi nitive plumage exhibited the from an all-green juvenal plumage, through simplest yearly molt activity pa ern (Fig. 3E). three distinct predefi nitive plumages, to a defi n- Very few (<5%) males showed any signs of molt itive adult plumage in fi h-year and older birds. from March to May. By June, more than one- This represents the longest delay yet reported third of defi nitive-plumaged males examined in any manakin (see Foster 1987, Duval 2005). were molting, and molt activity in these males Although variation in female plumage was peaked in September. more subtle, some females acquired male-like plumage features as they aged. Our fi ndings D have important implications for elucidating the adaptive signifi cance of delayed plumage By examining the plumage characteristics of maturation, and the potential signal function 1,315 color-banded individuals in northwestern of intraspecifi c variation in plumage, in Long- Costa Rica and 585 museum specimens, we tailed Manakins and other species. 38 D . [Auk, Vol. 124

Male plumages.—Male Long-tailed Manakins hatch-year males. Indeed, in a separate analysis, progressed through the following plumage Clay (2001) identifi ed two museum specimens sequence. Hatch-year (juvenal) males were as second-year males with all-green crowns. olive green throughout; second-year (red-cap) Moreover, the males in our study were captured males were olive green with some red on the in March and April, and would have fl edged crown; third-year (black-face) males were olive from exceptionally early nests if they were, in green with a red crown and a black facial mask fact, hatch-year males. Two other males appar- or hood; fourth-year (blue-back) males were a ently molted from a red-cap plumage into a mixture of green and black with a red crown blue-back plumage. If, in fact, these four males and a blue and green mantle; and fi h-year and represent anomalous sequence transitions, older (defi nitive) males were black with a red they correspond to accelerations of the typical crown patch and a blue mantle. This plumage sequence. However, because of the rarity of sequence can be summarized by the following these anomalies (≤1.8% of predefi nitive plum- heuristic: from (1) a green-plumaged bird, (2) age transitions), they probably occur arbitrarily add red, (3) add black, (4) add blue, (5) take rather than as a response to selective pressure away green. Our conclusions are consistent on males to accelerate through the maturation with those of McDonald (1989a, 1993a) but dif- process. Taken together, our fi ndings strongly fer from those of Foster (1987). In Foster’s (1987) suggest that plumage coloration is a highly con- sequence, red-cap and black-face males were sistent signal of age in young males until they included in the same age class, whereas blue- reach their fi h calendar year. This conclusion back males were separated into two age classes. has two important implications. First, our data Diff erences in interpretation of the red-cap confi rm that young males can be aged reliably stage may refl ect the fact that birds in red-cap in the fi eld on the basis of plumage features. plumage occasionally have some black feath- Second, our data support the hypothesis that ers on the face, particularly once they begin to plumage variation can serve as a social signal of molt in the early breeding season. Foster (1987) age in young males (McDonald 1993a). therefore (incorrectly) included black-face birds Social signaling in males.—The complex social in the red-cap plumage stage. The discovery system of Long-tailed Manakins is dependent that second-year birds can be aged on the basis on the development of long-term cooperative of diff erences in wing feathers now makes this alliances between males (Foster 1977; McDonald distinction infallible (see also Ryder and Durães 1989a, b, 1993a). Males must spend several years 2005). Foster’s (1987) diff erentiation of males working their way up the dominance hierarchy with blue, black, and green plumage into two to eventually have the opportunity to display stages likely refl ects a misinterpretation of the for females and, in a minority of males, to copu- extreme variation in the proportions of these late. The social stability of these mating queues colors in the third basic plumage. Nevertheless, appears to be strictly enforced by female mate our data from numerous plumage transitions choice, given that females will o en leave the show that the presence of blue mantle feathers dance perch at the fi rst sign of disruption by and black body feathers (other than those on the males other than the dominant males (Foster head) is a robust criterion for defi ning the third 1987; McDonald 1989a, 1993a). The evolution basic (blue-back) plumage. of predefi nitive male plumages is benefi cial to Although there was considerable variation both subordinate and dominant males in this within plumage stages of male Long-tailed type of social system. For dominant males, Manakins, there was li le overlap between the predefi nitive plumage of young males plumage stages. Two apparent exceptions to the immediately identifi es them as not posing a sequence involved males that were fi rst captured threat to their reproductive success (McDonald in green plumage and recaptured the following 1989b, McDonald and Po s 1994), which likely year in black-face plumage. These birds were reduces the amount of aggression that young captured before it was discovered that green males will receive from older males. Indeed, in birds could be aged on the basis of retained the congeneric Blue Manakin (C. caudata), the juvenal wing feathers, however, and it is likely amount and intensity of aggression shown by that these were second-year males without a red dominant males toward subordinate individu- crown patch, as opposed to juvenal-plumaged als decrease with decreasing age of the target January 2007] Plumage and Molt in Long-tailed Manakins 39 individual (Foster 1987). In addition, the evo- it is maladaptive. Because females are solely lution of age-specifi c plumages can provide responsible for parental care in manakins, they additional information about the status of males should experience strong natural selection for within the dominance hierarchy. In support crypsis (Martin and Badyaev 1996), particularly of this hypothesis, a taxidermy mount experi- given that rates of nest predation are quite high ment revealed that male Long-tailed Manakins in the tropics (Stutchbury and Morton 2001). responded more strongly to males in defi nitive Yet bright female coloration has been reported plumage than to males in predefi nitive plumage in a number of manakin genera (Graves 1981) (McDonald 1993a). Moreover, responses were and, in Long-tailed Manakins, females with red o en initiated by non-alpha males, which sug- crowns were more likely to express other male- gests that the model intruders posed a threat like plumage characteristics. Our documented to established male–male alliances rather than association between ornamental color and age a risk of stolen copulations (McDonald 1993a). in older females could be proximately mediated These observations are paralleled in Blue by age-related hormonal changes (Kimball and Manakins, in which aggression directed toward Ligon 1999). In some cases, male-like plumage a transgressor was o en initiated by males of characteristics other than crown color disap- intermediate rank and directed toward the indi- peared a er the following molt, which suggests viduals nearest them in the hierarchy (Foster that they may have resulted from adventitious 1981). These studies suggest that males are most feather loss and replacement at a time of year likely to challenge males of similar rank in a hier- when environmental cues, such as photoperiod archy and, presumably, against whom they have or daytime light intensity (Gwinner 2003), led to the greatest probability of success. The obverse the growth of more male-like plumage. of this is that males are also most likely to have A less likely possibility is that the develop- to defend their own positions against challenges ment of red crown coloration in older females from members of their own or adjoining age serves a social signaling function. Because of cohorts. A model presentation experiment in its association with age, red crown coloration another species with a graded, multiyear delay could signal a female’s longevity or viability. in plumage maturation, the Hawaiian ‘Elepaio Such a signal may be useful to males, who (Chasiempis sandwichensis), yielded similar fi nd- could optimize their display intensity or sperm ings (VanderWerf and Freed 2003). allocation by investing more in females they Female plumage.—Extreme sexual dichroma- deem to be of high quality (e.g., Amundsen tism is characteristic of the family Pipridae. 2000, Werner and Lotem 2003), a pa ern that Male manakins are usually brightly colored, may explain some of the variation in male whereas females are typically olive green (Prum display intensity in this species. Alternatively, 1997, Doucet et al. 2006). Here, we documented a signal of female age may be useful to young considerable variation in the plumage of female females, whose mate choice decisions could Long-tailed Manakins. Some females developed be infl uenced by those of older, experienced variable amounts of red or tawny coloration females when multiple females observe dis- in the crown, reminiscent of the red crowns playing males together (Dugatkin and Godin of males, and a small proportion of females 1993, Doucet et al. 2004). Comparative analyses developed black feathers on the face, head, of the relationship between male and female wing, or tail. Older females were more likely ornamentation, in combination with intraspe- than young females to develop red or tawny cifi c empirical investigations of the proximate crowns, and, on average, more than fi ve years control and signal function of female traits, elapsed between initial female captures and the will help to identify the relative merit of these appearance of red in their crowns. Female orna- hypotheses in explaining the evolution of bright mentation may have evolved as a byproduct of female plumage in manakins. genetic correlations between male and female Timing of molt.—Long-tailed Manakins un d- traits (Lande 1987, Amundsen 2000). Strong ergo a post-juvenal molt within four months of selection for elaborate ornaments in males, hatching and subsequently undergo a prebasic combined with weaker selection against these molt each year. The fi rst prebasic molt is incom- traits in females, could lead to the expression plete: birds of both sexes retain their juvenal rem- of ornamental coloration in females, even if iges and distal greater coverts. Second-year birds 40 D . [Auk, Vol. 124 also retain the yellow-orange mouth color typical McDonald 1989b, Trainer and McDonald 1993). of nestlings of this species (Foster 1976). A similar By June, there is usually a notable decrease in pa ern of delayed maturation in mouth color has male display activity, especially at the least suc- been reported in one species of bowerbird (Frith cessful leks (S. M. Doucet and D. B. McDonald and Frith 2004). Given the considerable number unpubl. data), which, as we have shown here, of species that show delayed maturation in iris corresponds to a sharp increase in proportion and so -part color (Lawton and Lawton 1986), of males in defi nitive plumage showing signs delayed maturation in mouth color may be rela- of molt. Females, on the other hand, are known tively widespread and should be investigated in to nest until at least July, and probably until other species. September (Foster 1976). Male display activity We found signifi cant age- and sex-based is intrinsically linked to the availability of recep- variation in timing of molt. Females exhibited tive females. A successful copulation, however, an early peak of molt activity in February and marks only the beginning of a female’s parental March. Second-year females were more likely responsibilities. Thus, the reproductive periods to show signs of early molt than older females. of dominant males and females are inherently Nevertheless, fewer than half of females showed staggered, which may explain why the post- signs of early molt activity, and this molt was breeding molt of males in defi nitive plumage limited to some body and head feathers. Molt peaks earlier than that of females. Moreover, activity was low from May through July in many defi nitive-plumaged males occupy subor- females and increased in August to a second dinate ranks at leks. These males are expected to peak, corresponding to the complete prebasic expend much less energy on display than domi- molt, in October. The decrease in molt activity nant males and to curtail their breeding season from April to July may refl ect evolutionary pres- activities sooner. sure to avoid the costs of molt–breeding overlap Over the course of the breeding season, (Foster 1974), because this period corresponds young male Long-tailed Manakins in predefi n- to the peak of female nesting activity (Foster itive plumage form affi liations with other males 1976). Molt and breeding are both energeti- at particular lek sites, o en practicing courtship cally demanding (e.g., Murphy and King 1992, displays on dance perches used by dominant Lindstrom et al. 1993). As such, physiological males. Young males are tolerated at dance and ecological trade-off s are expected to occur perches only in the absence of females, how- between these two life-history traits (Foster ever, because only dominant males display for, 1975a). Theory therefore predicts that molt and and copulate with, females (McDonald 1989a). breeding should be temporally segregated, yet Moreover, young males are resighted at leks molt–breeding overlap has been reported in less frequently than older males (McDonald numerous tropical and temperate passerines 1989a), which suggests that they invest less time (Foster 1975b, Pyle 1997) and, as we have shown and energy in breeding-season activities than here, occurs at the population level in Long-tailed older males. Thus, young males can begin molt- Manakins (Fig. 3). However, our data show that ing earlier in the season than older individuals. in May, June, and July, <15% of females exhibited Correspondingly, blue-back and black-face any signs of molt. Later in the season, females’ males exhibited an earlier peak of molt activity primary resource-consuming activity can switch than males in defi nitive plumage. from breeding to molt (see Foster 1975b), which Early molt in red-cap males is more diffi cult may explain the second, most prominent peak of to interpret. Many males in red-cap plumage female molt activity in October. began to molt in March, at the onset of the Though they provide no parental care, male breeding season. Moreover, this molt was appar- Long-tailed Manakins may expend consider- ently restricted to the crown and head. Indeed, able amounts of energy in breeding-related these males o en molted in additional red activities and are, therefore, also expected crown feathers and black-face feathers, thereby to avoid molt–breeding overlap. Dominant accelerating their transition into black-face (alpha and beta) males perform energetically plumage. Dominance interactions among males demanding dance displays for females and sing of the same age cohort may explain this early duets at high rates to a ract females to their molt. If crown and mask color allow males to leks (≤5,000 vocalizations per day; Foster 1977, assert their dominance over members of their January 2007] Plumage and Molt in Long-tailed Manakins 41 own age cohort, then selection might favor the taxa, particularly species that diff er from the acceleration of such a molt. Males in predefi n- typical north-temperate pa ern, are likely to itive plumages, particularly younger ones, are reveal that the adaptive signifi cance of delayed subject to opposing selective forces: by signal- plumage maturation cannot be encompassed ing their lesser age, the plumages may reduce by a single hypothesis. Moreover, accumulat- the aggression directed toward them by older ing evidence of interspecifi c variation in both males; at the same time, however, it might ben- pa erns and consequences of delayed plumage efi t them to develop, as much as possible, the maturation suggest broader evolutionary impli- traits that signal their prowess to males of the cations than we originally anticipated. same cohort (Foster 1987, McDonald 1993a). This confl ict may explain why some species Ap|l progress through several distinct predefi nitive plumage stages rather than molting into the We are extremely grateful to all our research same predefi nitive plumage for several years, assistants and Earthwatch volunteers for as has been documented in numerous other their help with fi eld data collection and to species (e.g., Frith and Beehler 1998, Frith and D. J. Mennill for help with museum data col- Frith 2004). lection and comments on the manuscript. Implications.—Male Long-tailed Manakins in S.M.D. thanks R. Blanco and the Area de predefi nitive plumage have testes capable of Conservación Guanacaste for permission to producing sperm (Foster 1987). Thus, delayed work in Santa Rosa; D.B.M. thanks A. Hoge plumage maturation in this species represents and J. and J. Stuckey for permission to work an instance of heterochrony and, more spe- on their property; M.S.F. thanks E. Carmona B. cifi cally, of neoteny (i.e., a slowing down of and the Ministerio de Agricultura y Ganadería somatic maturation in relation to sexual matu- of Costa Rica for housing and permission to ration; Lawton and Lawton 1986). Mean testis work at the Jiménez Station. We thank the size among 60 defi nitive-plumaged males was curators at the following institutions for pro- 29.3 ± 16.16 mm3 (Foster 1987). Interestingly, viding access to or loans of the specimens in the testis size of a beta male known to have their research collections: Academy of Natural been in defi nitive plumage for several years Sciences, Philadelphia; American Museum was 75 mm3, nearly three standard deviations of Natural History; California Academy above the mean (D. B. McDonald unpubl. data), of Sciences; Carnegie Museum of Natural which suggests that plumage maturation likely History; Field Museum of Natural History; precedes full testis maturation in this species. Florida Museum of Natural History; Louisiana Long-tailed Manakins may therefore exhibit State University Museum of Natural Science; both neoteny and progenesis (where somatic Moore Laboratory of Zoology, Occidental maturation precedes reproductive matura- College; Museum of Vertebrate Zoology, tion). Lawton and Lawton (1986) proposed that University of California, Berkeley; National heterochronic trends in plumage, iris, and so - Museum of Natural History; Natural History part maturation are associated with complex Museum of Los Angeles County; University social organization within the Corvidae and of Arizona; University of Kansas; University may have played a role in speciation among of California, Los Angeles (including the closely related corvids. As empirical investiga- Donald R. Dickey Collection); and Western tions of delayed plumage maturation become Foundation of Vertebrate Zoology. We thank more widely available, particularly among R. Laval for providing the photo in Figure tropical species, it will be possible to examine 1E. Funding to D.B.M. was provided by the pa erns of heterochrony, and the complex mix- National Geographic Society, the Harry Frank ing of neotenic and progenetic features, in other Guggenheim Foundation, and the Earthwatch groups that vary in degree of social organiza- Institute. Funding to S.M.D. was provided tion, including other manakins (Prum 1997). by the Natural Sciences and Engineering The increasing availability of well-supported Research Council of Canada, Sigma-Xi, the phylogenies will greatly facilitate these com- American Ornithologists’ Union, the Wilson parative investigations. Studies of delayed Ornithological Society, the Explorer’s Club, plumage maturation across a wider variety of the American Museum of Natural History, 42 D . [Auk, Vol. 124

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