PLUMAGE COLORATION AND MORPHOLOGY IN CHIROXIPHIA MANAKINS:
INTERACTING EFFECTS OF NATURAL AND SEXUAL SELECTION
Except where reference is made to the work of others, the work described in this
dissertation is my own or was done in collaboration with my advisory committee. This
dissertation does not include proprietary or classified information.
_________________________________________
St?phanie M. Doucet
Certificate of Approval:
__________________________________________
F. Stephen Dobson Geoffrey E. Hill, Chair
Professor Schamagel Professor
Biological SciencesBiological Sciences
____________________________________________
Craig Guyer Stephen L. McFarland
Professor Acting Dean
Biological Sciences Graduate School
PLUMAGE COLORATION AND MORPHOLOGY IN CHIROXIPHIA MANAKINS:
INTERACTING EFFECTS OF NATURAL AND SEXUAL SELECTION
St?phanie M. Doucet
A Dissertation
Submitted to
the Graduate Faculty of
Auburn University
in Partial Fulfillment of the
Requirements for the
Degree of
Doctor of Philosophy
Auburn, Alabama
May 11, 2006
iii
PLUMAGE COLORATION AND MORPHOLOGY IN CHIROXIPHIA MANAKINS:
INTERACTING EFFECTS OF NATURAL AND SEXUAL SELECTION
St?phanie M. Doucet
Permission is granted to Auburn University to make copies of this dissertation at
its discretion, upon request of individuals or institutions and at their expense.
The author reserves all publication rights.
____________________________________
Signature of Author
____________________________________
Date of Graduation
iv
DISSERTATION ABSTRACT
PLUMAGE COLORATION AND MORPHOLOGY IN CHIROXIPHIA MANAKINS:
INTERACTING EFFECTS OF NATURAL AND SEXUAL SELECTION
St?phanie M. Doucet
Doctor of Philosophy, May 11, 2006
(M.S. Queen?s University, 2002)
(B.S. Queen?s University, 2000)
231 Typed Pages
Directed by Dr. Geoffrey E. Hill
I examined how natural and sexual selection may have influenced the morphology
and coloration of Chiroxiphia manakins (Aves: Pipridae). In the first chapter, I
investigated age? and sex?related patterns of plumage coloration and molt timing in
long?tailed manakins, C. linearis. I examined how plumage coloration changed with age
in males and females based on 1315 mist net captures in northwestern Costa Rica and
examined molt patterns in an additional 585 museum specimens. Males followed a
remarkably age?specific pattern of plumage maturation before attaining definitive adult
plumage in their fifth year. Some females developed male?like plumage characteristics as
they aged, but not reliably so. Although molt?breeding overlap occurred at the population
level, few individuals molted while breeding. In the second chapter, I examined the
explanatory power of natural and sexual selection hypotheses in explaining patterns of
v
sexual dimorphism in Chiroxphia manakins. I measured six morphological traits in 361
wild C. linearis and a subset of these traits in 872 museum specimens of Chiroxphia
manakins. My findings were consistent with both sexual selection and natural selection
hypotheses, suggesting that both mechanisms have strongly influenced the evolution of
sexual dimorphism in this group. In the third chapter, I investigated how the perceptual
environment influences the conspicuousness of plumage displays in long?tailed
manakins. I measured the reflectance of 62 males and 59 females, the reflectance of the
background vegetation, and the irradiance of light at display perches. Male manakins
were highly conspicuous against the visual background, whereas females were relatively
cryptic. Males did not appear to adjust the location or timing of their displays to take
advantage of particular light conditions but rather displayed in the most common light
environment of forest shade. Displays performed in forest shade may optimize the
short?distance conspicuousness of male plumage ornaments while minimizing the
long?distance conspicuousness of male ornaments and the short? and long?distance
conspicuousness of female plumage patterns. In the fourth chapter, I evaluated the degree
to which the color of study skins is representative of coloration in wild birds. I measured
the plumage reflectance of 58 wild and 55 museum specimens of long?tailed manakins. I
found significant differences in color between museum specimens and wild birds, and the
degree of difference depended on the coloration mechanism. Potential sources of these
differences include the specimen preparation process, the age of specimens, and
geographic variation. Although caution is warranted for some types of studies, most
differences were relatively subtle, justifying the use of museum specimens to assess color
in many instances.
vi
ACKNOWLEDGEMENTS
I must first acknowledge the contributions of my co?authors for the various
chapters of this dissertation. Order of authorship is as follows: Chapter 1:  S. M. Doucet,
D. B. McDonald, M. S. Foster, and R. P. Clay; Chapter 2: S. M. Doucet, F. Hertel, and G.
E. Hill, Chapter 3: S. M. Doucet and G. E. Hill; Chapter 4; S. M. Doucet and G. E. Hill. I
thank all of these colleagues for their direct contributions to particular chapters and for
indirect contributions in the form of advice, observations, support, and encouragement.
The contributions of many other individuals, institutions, and funding agencies are
acknowledged in each chapter.
Dr. Geoffrey Hill has been an outstanding advisor and mentor. I am grateful for
the academic freedom he provided. He taught me much about the ins and outs of
academia. His drive, boundless enthusiasm, and ability to expertly juggle his academic
and personal lives are admirable. He leads by example and leaves most of us panting in
his wake. I am also grateful to the members of my advisory committee, Dr. Steve Dobson
and Dr. Craig Guyer, for their guidance, editorial suggestions, statistical advice, and
encouragement. My external reader, Dr. Henry Fadamiro, provided helpful feedback and
suggestions on the dissertation.
I also benefited greatly from the advice and support of other colleagues, most
notably Dr. Herman Mays, Dr. Dan Mennill, Dr. Bob Montgomerie, Dr. Laurene
vii
Ratcliffe, and Dr. Matthew Shawkey. My many labmates over the years were a constant
source of ideas, support, amusement, and friendship, and I offer my sincerest thanks.
My friends and family have contributed more to this dissertation than they could
possibly imagine. My extended family cheered me on. My friends were a most welcome
diversion, commiserating or celebrating as warranted by the occasion. Sandi, Paul, and
Sally were tremendous sources of encouragement and inspiration. My brother Vernon
was understanding and supportive. My mother and father, Mercia and Conrad, long ago
presented the world as a place full of opportunities for me. They glossed over my
mistakes and sang my praises. They made sacrifices so that I could achieve what hadn?t
been a possibility for them. I will be forever grateful.
I owe my greatest debt of gratitude to my husband, Dan. His contributions are
more numerous and of greater importance than can be conveyed here. He has been
involved with my dissertation project from the very beginning, first serving as a sounding
board for my ideas, then helping with many parts of data collection, and finally reading
several manuscript drafts. His hard work, dedication, and many successes were a daily
source of inspiration. He, too, made some sacrifices and compromises which enabled me
to pursue my work. I am so very thankful for all of these things. I am most grateful,
however, for his unwavering love and support. His encouragement and ability to convey
the bigger picture helped me through the rough spots, and he was always my biggest fan
when things were going well. I don?t know how I would have managed without him.
viii
Style manual of journal used: The American Naturalist
Computer Software Used: Microsoft Word, Microsoft Exel, JMP, EndNote
ix
TABLE OF CONTENTS
LIST OF TABLES.....................................................xi
LIST OF FIGURES...................................................xiii
CHAPTER 1. PLUMAGE DEVELOPMENT AND MOLT IN LONG?TAILED
MANAKINS: VARIATION ACCORDING TO SEX AND AGE..................1
Abstract............................................................2
Introduction.........................................................3
Methods...........................................................5
Results............................................................8
Discussion.........................................................16
Acknowledgements..................................................26
Literature Cited.....................................................28
Figure Captions.....................................................35
CHAPTER 2. COMPLEX PATTERNS OF SEXUAL DIMORPHISM IN
CHIROXPHIA MANAKINS: INTERACTING EFFECTS OF NATURAL AND
SEXUAL SELECTION?................................................39
Abstract...........................................................40
Introduction........................................................42
Methods..........................................................50
Results...........................................................54
Discussion.........................................................60
Acknowledgements..................................................73
Literature Cited.....................................................75
Figure Captions.....................................................88
CHAPTER 3. LEKS, LIGHT, AND LOOKS: DOES THE VISUAL
ENVIRONMENT INFLUENCE DISPLAY CONSPICUOUSNESS IN
LONG?TAILED MANAKINS?..........................................98
Abstract...........................................................99
Introduction.......................................................101
Methods.........................................................106
Results..........................................................117
Discussion........................................................125
x
Acknowledgements.................................................136
Literature cited....................................................138
Figure Captions....................................................153
CHAPTER 4. CAROTENOID, MELANIN, AND STRUCTURAL PLUMAGE
COLOR OF AVIAN STUDY SKINS: EFFECTS OF SPECIMEN AGE AND
GEOGRAPHIC VARIATION..........................................168
Abstract..........................................................169
Introduction.......................................................171
Methods.........................................................174
Results..........................................................178
Discussion........................................................182
Acknowledgements.................................................191
Literature Cited....................................................193
Figure Captions....................................................208
CONCLUSIONS.....................................................215
xi
LIST OF TABLES
CHAPTER 1
Table 1. Summary of plumage development in male long?tailed manakins????..
33
Table 2. Summary of sequential plumage transitions recorded in male long?tailed
manakins. ????????????.?????????????????..
34
CHAPTER 2
Table 1. Predicted direction of dimorphism for morphological traits in long?tailed
manakins based four non?mutually exclusive hypotheses??????????.?
85
Table 2. Flight parameters, their associated measures of performance, and the sizes
or magnitudes of four morphological traits that should enhance performance for each
specific flight parameter?????????????????????.???
86
Table 3. Means ? standard deviations of morphological traits in museum specimens
of male and female Chiroxiphia manakins????????????????.?
87
CHAPTER 3
Table 1. The influence of sex, body region, and sex by body interactions on
chromatic plumage contrast against the background in long?tailed manakins for two
different backgrounds and three different light environments??????????
146
Table 2. The influence of sex, body region, and sex by body interactions on
achromatic plumage contrast against the background in long?tailed manakins for two
different backgrounds and three different light environments??????????
147
Table 3. Sex difference in chromatic and achromatic contrast between body regions
in long?tailed manakins for three different light environments????????.?
148
Table 4. Paired comparisons of chromatic and achromatic plumage contrast against
the background for long?tailed manakins in different light environments?????.
149
Table 5. Paired comparisons of chromatic and achromatic plumage contrast against
the background for long?tailed manakins in viewed against different backgrounds.?
150
Table 6. Paired comparisons of chromatic and achromatic plumage contrast between
body regions for long?tailed manakins in different light environments??????.
151
Table 7. Paired comparisons of irradiance PC scores at primary display perches of
long?tailed manakins versus secondary display perches, nearby control perches not
used for display, and an arbitrary location 10 m from the primary display perch??..
152
xii
CHAPTER 4
Table 1. Comparison of plumage reflectance between museum skins and live?caught
male long?tailed manakins in definitive adult plumage????????????.
203
Table 2. Relationship between plumage color variables and specimen age among
male long?tailed manakins in definitive adult plumage????????????
204
Table 3. Relationship between plumage color variables and geographic location
among male long?tailed manakins in definitive adult plumage?????????.
205
Table 4. Multiple regression of plumage color variables on specimen age and
sampling location among male long?tailed manakins in definitive adult plumage?...
206
Table 5. Multiple regression of plumage chroma variables on specimen age and
sampling location among male long?tailed manakins in definitive adult plumage?...
207
xiii
LIST OF FIGURES
CHAPTER 1
Figure 1. Photographs showing typical appearance of long?tailed manakins in
different plumage stages???????????????????????...
36
Figure 2. Monthly proportions of long?tailed manakins showing signs of molt at
time of capture for birds in different plumage stages????????????...
37
Figure 3. Photographs showing the crowns of a young male long?tailed manakin in
red?cap plumage and a female with reddish crown feathers??????????
38
CHAPTER 2
Figure 1. Schematic diagram illustrating aspects of wing morphology
measurements in the long?tailed manakin????????????????..
90
Figure 2. Box plots showing differences in morphological traits among male
long?tailed manakins in different age classes???????????????..
91
Figure 3. Box plots showing sex differences in morphological traits in long?tailed
manakins?????????????????????????????..
92
Figure 4. Scatterplot of canonical axes 1 and 2 of a Discriminant Function Analysis
in long?tailed manakins????????????????????????
93
Figure 5. Box plots showing differences wing in morphology among male
long?tailed manakins in different age classes???????????????..
94
Figure 6. Box plots showing sex differences in wing morphology in long?tailed
manakins?????????????????????????????...
95
Figure 7. Three?dimensional morphospace of wing size and shape, bill size and
shape, and body mass in male and female long-tailed manakins????????.
96
Figure 8. Sexual dimorphism indexes for three morphological traits based on
measurements from museum specimens of Chiroxiphia manakins???????.
97
xiv
CHAPTER 3
Figure 1. Mean reflectance spectra of adult male and female long?tailed manakins...
156
Figure 2.  Mean reflectance spectra of long-tailed manakin display perches, of the
green leaves of saplings and the bark of trees surrounding display perches, and of
the leaf litter beneath display perches??????????????????...
157
Figure 3. Component loadings for the first three principal components of a principal
components analysis of reflectance spectra from plumage patches of male and
female long?tailed manakins and of the bark and leaves constituting the visual
background of long?tailed manakin display sites??????????????.
158
Figure 4. Scatterplots of reflectance principal component scores representing the
color space of male and female manakin plumage coloration and components of the
visual background??????????????????????????.
159
Figure 5. Mean irradiance spectra of forest shade, small gaps, and cloudy light
environments collected at primary display perches of long?tailed manakins???..
160
Figure 6. Long?distance conspicuousness as measured by and achromatic contrast
against the background for different body regions of male and female long?tailed
manakins in a forest shade light environment and against a background of green
leaves???????????????????????????????
161
Figure 7. Short?distance conspicuousness as measured by chromatic and
achromatic contrast between body regions for male and female long?tailed
manakins in three different light environments???????????????
162
Figure 8. Mean chromatic contrast against the background for male and female
long?tailed manakins for a background composed of green leaves or brownish bark
in three different light environments???????????????????
163
Figure 9. Mean achromatic contrast against the background for male and female
long?tailed manakins for a background composed of green leaves or brownish bark
in three different light environments???????????????????
164
Figure 10. Component loadings for the first three principal of a principal
components analysis of irradiance spectra from three different light environments
measured at primary display perches of long?tailed manakins?????????
165
Figure 11. Irradiance principal component scores from spectra collected in forest
shade and small gap light environments at primary, secondary, control, and
arbitrary display perches of long?tailed manakins?????????????...
166
Figure 12. Comparison of physical characteristics of primary, secondary, and
control perches of long?tailed manakins?????????????????..
167
xv
CHAPTER 4
Figure 1. Map of Central America showing geographic distribution of long?tailed
manakins, Chiroxiphia linearis?????????????????????
210
Figure 2. Average reflectance spectra for the red crown, blue mantle, and black
body among male long?tailed manakins in definitive adult plumage??????..
211
Figure 3. Box plots showing differences in plumage color variables between
live?caught male long?tailed manakins in definitive adult plumage and study skins..
212
Figure 4. Scatterplots showing relationship between plumage color variables and
residual specimen age among male long?tailed manakins in definitive adult
plumage??????????????????????????????
213
Figure 5. Scatterplots showing relationship between plumage color variables and
residual geographic location among male long?tailed manakins in definitive adult
plumage??????????????????????????????
214
1
CHAPTER 1. PLUMAGE DEVELOPMENT AND MOLT IN LONG?TAILED
MANAKINS: VARIATION ACCORDING TO SEX AND AGE
2
ABSTRACT
Lek?mating long?tailed manakins (Chiroxiphia linearis) exhibit an unusual pattern of
delayed plumage maturation. Each year, males progress through a series of predefinitive
plumages before attaining definitive plumage in their fifth calendar year. Females also
exhibit variation in plumage coloration, with some females displaying male?like plumage
characteristics. Using data from mist net captures in northwestern Costa Rica (n = 1,315)
and museum specimens from throughout the range of long?tailed manakins (n = 585), we
document the plumage sequence progression of males, explore variation in female
plumage, and describe the timing of molt in this species. Males progressed through a
series of age?specific predefinitive plumages, enabling the accurate aging of
predefinitive?plumaged males in the field and providing 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 result as a by?product of selection on
bright male plumage. Females exhibited an early peak of molt activity from February to
April, little molt from May through July, and a second, more pronounced peak of molt
activity in October. By contrast, males in older predefinitive plumage stages and males in
definitive plumage exhibited comparable, unimodal peaks in molt activity beginning in
June and peaking between July and October. Our data are consistent with selective
pressure to avoid the costs of molt/breeding overlap in females and older males. Our
findings have important implications for social organization and signaling in long?tailed
manakins, and the evolution of delayed plumage maturation in birds.
3
INTRODUCTION
In many birds, males delay assuming definitive, adult?like plumage for one or more years
after hatching. In some species, this delay in plumage maturation is accompanied by a
delay in sexual maturation (Lawton and Lawton 1986). In many sexually dichromatic,
north?temperate passerines, however, males delay attaining their definitive plumage until
after their first potential breeding season, despite having reached sexual maturity
(Rohwer et al. 1980; Lyon and Montgomerie 1986). The adaptive significance of this
type of delayed plumage maturation has been the focus of extensive research in recent
decades (e.g., Rohwer et al. 1980; Lyon and Montgomerie 1986; Hill 1996), with most
studies investigating one?year delays typically exhibited by north?temperate passerines.
However, many tropical passerines deviate from this pattern. In some species, such as
bowerbirds and birds of paradise, males molt into the same predefinitive plumage for
several years before assuming definitive plumage (Frith and Beehler 1998; Frith and Frith
2004). In other species, for example Chiroxiphia manakins, Geospiza Darwin?s finches,
paradise flycatchers, Hawaiian honeycreepers, and monarch flycatchers, males progress
through a transitional series of different predefinitive plumage stages before assuming
definitive plumage (Foster 1987; McDonald 1989a; McDonald 1993a; Lepson and Freed
1995; Vanderwerf 2001; Mulder et al. 2002). Investigations of the adaptive significance
of delayed plumage maturation, and of the signal function of variation in plumage,
require a thorough understanding of plumage development and molt. Here, we investigate
age? and sex?related plumage variation in the long?tailed manakin (Chiroxiphia
linearis).
4
Long?tailed manakins have a lek?based mating system (Foster 1977; McDonald
1989a; McDonald 1989b). Males gather at lek sites where they establish age?graded
dominance hierarchies. The two most dominant males at each lek, the alpha and beta
males, perform vocal duets and elaborate, dual?male dance displays for females visiting
the leks. Females usually copulate only with alpha males (Foster 1977; McDonald 1989b;
McDonald and Potts 1994). As in other lekking species (H?glund and Alatalo 1995),
females are solely responsible for rearing offspring (Foster 1976).
As they grow older, male long?tailed manakins progress through a series of
transitional, predefinitive plumage stages before attaining definitive plumage in their fifth
calendar year (Foster 1987; McDonald 1989a; McDonald 1993a). This delay is unusually
long for such a small (15?21 g) passerine (Lawton and Lawton 1986). Female long?tailed
manakins also vary in plumage color, with some females developing red or tawny crown
feathers, a trait thought to be associated with age (McDonald 1989b). Such extensive
age? and sex?based variation in plumage may present unique signaling opportunities,
particularly in species with complex social organization (Lawton and Lawton 1986). In
long?tailed manakins, for example, a male?s position within a lek hierarchy may be
largely influenced by his age. Thus, transitional plumages that reliably signal a male?s
age and/or status in the hierarchy would likely reduce the occurrence of costly, escalated
encounters between males of low and high status (Foster 1987; McDonald 1993a).
Foster (1987) described predefinitive male plumages in long?tailed manakins as
transitioning through several stages along a continuous spectrum, with second?year
males being mostly green with a red crown patch and, occasionally, some black on the
face, coverts, and body and flight feathers, and third? and fourth?year males having a
5
mixture of red, green, black, and blue plumage. McDonald (1989a; 1993a) proposed an
alternative sequence, whereby males progress through a transitional series of age?specific
predefinitive plumages. In his proposed sequence, males develop a red crown in their
second year, a black mask in their third year, and a blue mantle in their fourth year. Using
recapture and resighting data from three study populations, together spanning 27 years,
we reexamine the plumage sequences proposed by Foster (1987) and McDonald (1989a;
1993a) to determine whether predefinitive male plumage can reliably signal age in
long?tailed manakins. Additionally, we investigate patterns of variation in female
plumage, and describe sex? and age?based variation in the timing of molt.
METHODS
We studied long?tailed manakins at three sites in northwestern Costa Rica: from 1971 to
1974 and 1977 at the Enrique Jim?nez Nu?ez Experiment Station (10? 20? N, 85? 8? W),
from 1981 to 1999 in Monteverde (10? 18? N, 84? 48? W), and from 2003 to 2005, as well
as for a few weeks in 1986, in Santa Rosa National Park, Guanacaste Conservation Area
(10? 40? N, 85? 30? W). The Monteverde site is located in premontane tropical moist
forest (Holdridge 1966) and the Santa Rosa and Jim?nez Station sites encompass both
evergreen bottomland moist forest and areas of tropical dry forest on surrounding
hillsides (Stiles and Skutch 1989). All three sites exhibit marked seasonality, with a dry
season extending from approximately January through April, and a rainy season
extending from May through December. Male long?tailed manakins display actively
from February through September, with a pronounced peak in activity from March
through June (Foster 1977; McDonald 1989a; McDonald 1989b; McDonald 1993b).
6
Active nests have been discovered from March to July (Foster 1976; SMD, unpubl. data),
although the nesting season likely extends until September (Foster 1976).
We captured 1,315 long?tailed manakins using mist nets and fitted each
individual with a unique combination of plastic colored leg bands; birds at Monteverde
and Santa Rosa also carried a numbered aluminum leg band. Of 20 birds banded as
nestlings, only two were recaptured or resighted in following years (one male and one
female). To determine the plumage sequence followed by birds as they aged, we recorded
detailed descriptions of each bird?s plumage coloration each time it was captured.
Whenever possible, we also recorded plumage descriptions of marked individuals seen
during behavioral observations at lek sites or encountered opportunistically at the study
sites. Over the course of the study, R. P. Clay and M. S. Foster noted that second?year
birds of both sexes could be identified by the presence of retained juvenal wing feathers;
R. P. Clay also discovered that the mouth?lining color of second?year birds was
diagnostic (Clay 2001). Thus, we examined the mouth?lining color and the amount of
wear on wing feathers of all green?plumaged birds captured between from 1997 to 1999,
and in 2005. Only a subset of the data we present in this study were described briefly
elsewhere (plumage sequence information from 56 males, McDonald 1989a; McDonald
1993a).
To assess the timing of molt, we examined all birds captured from 1971 to 1977,
some birds captured in 1986 and 1987, and all birds captured since 1995 for signs of molt
(i.e., sheathed feathers), recording whether birds were molting at time of capture and
noting in which regions of which feather tracts they were molting. Occasionally, we
noted extremely asymmetric molt or molt of only a single, isolated feather on some
7
individuals. We assumed in both instances that the molt was adventitious and did not
include these individuals in our calculations of proportions of birds molting (Pyle 1997;
Vanderwerf 2001). Although most birds were captured and observed between March and
July, we collected molt information on wild birds in all months except September and
February.
To obtain additional molt data spanning the calendar year, we also examined 585
long?tailed manakin specimens in the collections of museums listed in the
Acknowledgements. We recorded feather regions and tracts with molting feathers and, if
discernible, the plumages from which and into which a bird was molting. A large number
of the museum specimens were also examined for the presence of juvenal remiges and
coverts. Taken together, our data from museum specimens and wild birds spanned the
entire calendar year, although some months are considerably better represented than
others. Molt and plumage terminology follow the Humphrey?Parkes (H?P) system
(Humphrey and Parkes 1959) as summarized in Pyle (1997). A recent review (Howell et
al. 2003) recommends modifications to H?P terminology. The complex nature of molt in
manakins, however, makes it difficult to assign consistent molt terminology to different
sex and age classes under the proposed changes. Thus, for simplicity, we opted for
traditional H?P terminology. We also follow Pyle?s (1997) age terminology. Thus, a
hatch?year is a bird in its first calendar year (until 31 December of the year it fledged), a
second?year bird is in its second calendar year (from January 1 to December 31 of the
year following fledging), a third?year bird is a bird in its third calendar year, and so on.
Wild birds in all?green or primarily green plumage were identified as females if
they had a vascularized brood patch, were recaptured or resighted in green plumage in
8
multiple years, were aged as after?second year birds based on the absence of retained
juvenal wing feathers (see above), exhibited female?like behavior during dance displays
by males (McDonald 1989a), or were identified as such either by genetic sexing
(Griffiths et al. 1998) or by laparotomy. Birds in green plumage were identified as males
if they were recaptured or resighted in predefinitive or definitive male plumages in
subsequent years or by laparotomy. For museum specimens, green birds were identified
as females or males only if the specimen tag indicated the presence of ovaries or testes,
respectively. Birds in green plumage that did not meet these criteria were considered of
unknown sex and were not included in our analyses.
RESULTS
Molt
All Long?tailed Manakins underwent a prebasic (postbreeding) molt each year. The
olive?green juvenal plumage grown in the nest was identical in males and females. The
first prebasic molt began within four months of fledging and was a partial molt, as
hatch?year birds of both sexes retained some of their juvenal wing feathers. Thus,
second?year birds had two generations of wing feathers: retained juvenal remiges and
distal greater coverts and new lesser and median coverts and proximal greater coverts.
Additionally, the mouth linings of second?year birds were bright orange to
orange?yellow, similar to those of nestlings (Foster 1976), whereas the mouth linings of
older birds were paler and more pinkish in color. All subsequent prebasic molts were
complete.
9
Male plumage sequence
Overall, we captured and marked 653 individuals in Monteverde, 280 individuals
at the Jim?nez Station and 382 individuals in Santa Rosa. Many of these birds were
recaptured or resighted in one or more subsequent years, allowing us to document 562
plumage transitions from a total of 235 males. Of these transitions, 343 were successive
molts in definitive plumage, while 219 consisted of molts from one predefinitive plumage
to another or from predefinitive to definitive plumage. Of these 219 informative
transitions, we have records for two different plumage stages for 98 males, three different
plumage stages for 32 males, and four different plumage stages for 19 males. One male
was sighted in all five plumage stages.
Males progressed through the following plumage sequence (Fig. 1; Tables 1, 2).
They acquired their juvenal plumage in the nest, which, like the plumage of females, was
olive green above with a paler wash below. Within four months of fledging, males
initiated their first prebasic molt. Males in their first?basic plumage, which we term
?red?cap plumage?, were olive green throughout with a small red crown patch. The
amount of red in the crown was highly variable, and males often had two strips of red
feathers on the outer edges of the crown rather than a contiguous red crown patch (Fig.
3A). A limited number of males in red?cap plumage also had some black feathers on the
face. These black feathers, or additional ones, were acquired along with an expanded red
crown in some males during a partial molt (either a limited prealternate molt or the early
onset of the second prebasic molt; see Timing of Molt) in March and April. In addition,
some males undergoing their first prebasic molt replaced their central, but no other,
10
rectrices (MSF, unpubl. data). These rectrices were darker and longer than those retained
from the juvenal plumage.
The following year, males underwent their second prebasic molt. Males in their
second?basic plumage, which we term ?black?face plumage?, were mostly olive?green
with a small red crown patch and a black facial mask or hood. In this plumage, the red
crown patch was always contiguous and was larger than that of red?cap males but smaller
than that of males in definitive plumage. The amount of black on the face varied from a
small black facial mask to a full black hood. Some black?face males also had some black
in their coverts and flight feathers, and a blackish tinge to their body plumage. Rarely,
males in black?face plumage had a limited 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 flight 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, although all exhibited some blue in the back,
and some black ventrally. Often, blue?back males had body feathers that were mostly
black with a tinge of olive?green and flight feathers that were black with green edging.
Some blue?back males had very little green at all in their plumage and might be mistaken
for definitive?plumaged males in the field. Other blue?back males had so much green in
their body plumage that they had an almost grayish appearance. Finally, males in
definitive?basic plumage had entirely jet?black body and flight feathers, a sky?blue
mantle, and a bifid, red crown patch. A small number of males molting from blue?black
plumage to definitive plumage retained minimal amounts of green on the rump, flanks, or
undertail coverts. This green disappeared during the following prebasic molt.
11
Four lines of evidence allow us to assign ages to these sequences. First, one male
banded as a nestling was recaptured or observed in three subsequent years: in his first
prebasic molt he acquired the red?cap plumage, in his second prebasic molt, the
black?face plumage, and in his third prebasic molt, the blue?back plumage.
(Unfortunately, this male was not resighted again until his sixth calendar year, when he
was in definitive plumage). Second, all red?cap males captured between 1997 and 1999
at Monteverde (32 individuals) and in 2005 at Santa Rosa (11 individuals) were identified
as second?year birds on the basis of retained juvenal remiges and distal greater coverts
and mouth lining color. Third, we documented the full, four?year progression of 17 males
from red?cap plumage to definitive plumage. Finally, all males observed in red?cap
plumage invariably had black feathers on the face the following year. Similarly, all males
observed in black?face plumage had blue feathers on their mantle the following year. No
male observed in definitive plumage was ever observed to have green feathers in
subsequent years. Our observations suggest that this plumage sequence is unidirectional,
non?reversible, and remarkably age?specific.
Of the 562 plumage transitions we recorded, 465 were sequential (i.e., the males
were recaptured or resighted the following year). These sequential transitions allowed us
to assess the frequency of unexpected plumage transitions. We documented only four
unusual plumage transitions. Two males were first captured in all green plumage and
both were recaptured in black?face plumage the following year (Table 2). Because these
males were captured in March and April as green males but the following breeding
season as black?face males, it is possible that they showed red in the crown during some
of the interval between these records. A third otherwise all?green male was molting in a
12
limited black mask and red crown when it was captured in April. A year later, after a
single prebasic molt, it was in blue?back plumage. A fourth presumably aberrant bird,
captured in red?cap plumage and without any black on its body, had a larger red crown, a
well developed black hood (but no other black body feathers), and a small area of blue
feathers on the back the following year. Thus, at most 0.7 % of plumage transitions
deviated from the expected pattern. Even if we exclude transitions between definitive
plumage stages, these anomalies account for only 1.8 % of plumage transitions. These
anomalies invariably involved an accelerated plumage maturation process, as no male
ever remained in the same plumage stage for two subsequent years. In 96 instances, more
than one year elapsed between recaptures or resightings of particular males. Even among
these non?sequential transitions, males were always in the expected plumage category
when they were eventually recaptured or resighted, as estimated from the number of
years separating recaptures or resightings.
Female plumage
Female Long?tailed Manakins are typically olive?green above with a paler wash
below. However, of the 649 confirmed females examined (including museum
specimens), 145 (23 %) had variable amounts of tawny or red feathers on the crown,
ranging from a single feather to a full tawny or red crown. The presence of red in the
crown of females may make it difficult for inexperienced observers to differentiate them
from young males in red?cap plumage. However, the red crown feathers of females can
be distinguished from those of males by one or more of the following characteristics (Fig.
3). First, the red feathers of females often had a tawny or rusty appearance, a feature
13
never observed in males. Second, the red color was often present on only some of the
barbs of each feather in females, while the remainder of the feather remained green,
thereby creating a slightly streaked appearance (Fig. 3A). By contrast, the red feathers of
young males usually had red distal barbs, and red, orange, or yellow central and proximal
barbs, regardless of the number of red feathers on the crown (Fig. 3B). Third, the red
feathers of females were usually the same length as the other (green) feathers on the
crown, whereas the red feathers of males were usually longer than the green feathers and
tended to increase in length with age (Fig. 3; S. M. Doucet, pers. obs.). Fourth, the
distribution of red feathers on the crown differed between females and males. In females,
red feathers could be found in the front, center, or rear of the crown. By contrast, among
males in red?cap plumage, the red feathers tended to grow on the outer edges of the
crown, often resulting in a split, rather than contiguous, red crown (Fig. 3A).
The development of tawny coloration in the crown of females appeared to be
associated with age. Of the females we were able to age as second?year or after?second
year (on the basis of plumage and mouth lining color), none of 43 second?year females
had any trace of red or tawny on the crown, while 91 of 189 after?second?year females
had traces of tawny or red (Fisher?s Exact Test, P < 0.00001). Of the females that
exhibited changes in plumage color during the course of the study, nine were observed or
recaptured sufficiently frequently to estimate the minimum amount of time elapsed
between when the bird was originally captured and when a change in plumage was first
noted (5.1 ? 1.17 years; mean ? SD). Two of these females were first captured as
second?year females ? one of these developed a tawny crown in her eighth year while the
other developed red crown feathers in her ninth year. Some females never developed red
14
or tawny crowns, including the three oldest, minimum?age females in this study. Two
were recaptured in completely green plumage 10 years after initial capture. A third
female, last observed 15 years after her initial capture, had no discernible red or tawny in
her crown.
In rarer instances, females departed from the typical olive?green plumage in other
ways. During the course of our study, we captured a few females with black lores or
black forehead, cheek, or nape feathers (n = 21); with one or more partially or completely
black wing or tail feathers (n = 11); or with blue or black wing or tail coverts or blue
mantle feathers (n = 5). Apart from crown color, none of these patches was extensive
enough to be easily seen in the field. Females with some tawny or red coloration in the
crown were significantly more likely to show these additional male?like plumage
tendencies (28 of 147) than females that were otherwise all green (6 of 504; Fisher?s
Exact test, P < 0.00001). Two of the females that had black or blue on the body were
recaptured in subsequent years and no longer had black or blue in their plumage. By
contrast, all females with a red or tawny crown that were recaptured in subsequent years
retained a colored crown.
Timing of molt
Long?tailed manakins follow a complex pattern of molt that varies by age and
sex. Among females, there is a bimodal distribution of proportion of birds molting over
the course of the year, with an early peak of molt activity in March and a second peak in
October (Fig. 2A). The molt occurring between February and April is limited to some
head and body feathers, while the second peak corresponds to the complete, prebasic
15
molt. The early peak varies by age. Of the females examined in March and April that we
were able to age (n = 81), 13 of 15 (86%) second?year females showed signs of molt,
while only 25 of 66 (38%) after?second?year females showed signs of molt (Fisher?s
Exact Test, P = 0.0003). Unfortunately, our data do not allow us to determine whether
this early peak corresponds to a limited prealternate molt, or whether it is an early
beginning to the prebasic molt that is suspended through the reproductive period. This
distinction would require confirmation that newly molted feathers were replaced in the
subsequent prebasic molt (in the case of a limited pre?alternate molt) or not replaced in
the subsequent molt (in the case of an early suspended prebasic molt).
The molt activity patterns of males in predefinitive plumage are rather more
complex. We separated males by plumage stage, which generally corresponds to age (see
Table 1 and Male plumage sequence above). As in females, a large proportion of red?cap
(second?year) males showed signs of molt in March and April (Fig. 2B). Among these
young males, there was a slight decrease in molt activity in May. By June, however, all
red?cap males captured or examined showed signs of molt. Of the red?cap males
showing signs of molt in March and April (n=19), 84% were molting only crown or head
feathers. Two of these males (10%) were molting both head and body feathers, and two
others (10%) were molting only body feathers. Many of these red?cap males were
molting in additional red crown feathers and some were molting in black feathers on the
face. In some cases, however, these males were simply molting in green crown or face
feathers. The peak of molt in June corresponds to the complete, first?prebasic molt, as
males were in a much heavier molt that often included flight feathers. Among black?face
(third?year) and blue?back (fourth?year) males, we detected molt in only a small
16
percentage of males (13%) in March and April (Fig. 2 C, D). As with red?cap males, this
early molt in black?face and blue?back males was largely restricted to crown and head
regions. Black?face and blue?back males exhibited a peak of molt activity between June
and August, which corresponded to their complete, third? and fourth?prebasic molts,
respectively.
Males in definitive plumage exhibited the simplest yearly molt activity pattern
(Fig. 2E). Very few (<5%) males showed any signs of molt from March to May. By June,
more than one?third of definitive?plumaged males examined were molting, and molt
activity in these males peaked in September.
DISCUSSION
By examining the plumage characteristics of 1,315 color?banded individuals in
northwestern Costa Rica and 585 museum specimens, we documented age? and
sex?related variation in plumage maturation and molt timing in Long?tailed Manakins.
Male plumage development progressed in discrete, age?specific categories from an
all?green juvenal plumage, through three distinct predefinitive plumages, to a definitive
adult plumage in fifth?year and older birds. Although variation in female plumage was
more subtle, some females acquired male?like plumage features as they aged. Our
findings have important implications for elucidating the adaptive significance of delayed
plumage maturation, and the potential signal function of intraspecific variation in
plumage, in Long?tailed Manakins and other species.
17
Male plumages
Male Long?tailed Manakins progressed through the following plumage sequence.
Hatch?year (juvenal) males were olive green throughout; second?year (red?cap) males
were olive green with some red on the crown; third?year (black?face) males were olive
green with a red crown and a black facial mask or hood; fourth?year (blue?back) males
were a mixture of green and black with a red crown and a blue and green mantle; and
fifth?year and older (definitive) males were black with a red crown patch and a blue
mantle. This plumage sequence can be summarized by the following heuristic: from (1) a
green?plumaged bird, (2) add red; (3) add black; (4) add blue; (5) take away green. Our
conclusions are consistent with those of McDonald (1989a; 1993a) but differ from those
of Foster (1987). In Foster?s (1987) sequence, red?cap and black?face males are included
in the same age class, whereas blue?back males are separated into two age classes.
Differences in the interpretation of the red?cap stage may reflect the fact that birds in
red?cap plumage occasionally have some black feathers on the face, particularly once
they begin to molt in the early breeding season. Foster (1987) therefore (incorrectly)
included black?face birds in the red?cap plumage stage. The discovery that second?year
birds can be aged on the basis of differences in wing feathers now makes this distinction
infallible. Foster?s (1987) differentiation of males with blue, black and green plumage
into two stages likely reflects a misinterpretation of the extreme variation in the
proportions of these colors in the third?basic plumage. Nevertheless, our data from
numerous plumage transitions show that the presence of blue mantle feathers and black
body feathers (other than those on the head) is a robust criterion for defining the
third?basic (blue?back) plumage.
18
Although there was considerable variation within plumage stages of male
Long?tailed Manakins, there was little overlap between plumage stages. Two apparent
exceptions to the sequence involved males that were first captured in green plumage and
recaptured the following year in black?face plumage. These birds were captured before it
was discovered that green birds could be aged on the basis of retained juvenal wing
feathers, however, and it is likely that these were second?year males without a red crown
patch, as opposed to juvenal?plumaged hatch?year males. Indeed, in a separate analysis,
Clay (2001) identified two museum specimens as second?year males with all?green
crowns. Moreover, the males in our study were captured in March and April, and would
have fledged from exceptionally early nests if they were in fact hatch?year males. Two
other males apparently molted from a red?cap plumage into a blue?back plumage. If
these four males do, in fact, represent anomalous sequence transitions, they correspond to
accelerations relative to the typical sequence. However, due to the rarity of these
anomalies (at most 1.8 % of predefinitive plumage transitions), they probably occur
arbitrarily rather than as a response to selective pressure on males to accelerate through
the maturation process. Taken together, our findings strongly suggest that plumage
coloration is a highly consistent signal of age in young males until they reach their fifth
calendar year. This conclusion has two important implications. First, our data confirm
that young males can be aged reliably in the field based on plumage features. Second, our
data support the hypothesis that plumage variation can serve as a social signal of age in
young males (McDonald 1993a).
19
Social signaling in males
The complex social system of Long?tailed Manakins is dependent upon the
development of long?term cooperative alliances between males (Foster 1977; McDonald
1989a; McDonald 1989b; McDonald 1993a). Males must spend several years working
their way up the dominance hierarchy to eventually to have the opportunity to display for
females, and, in a minority of males, to copulate. The social stability of these mating
queues appears to be strictly enforced by female mate choice, as females will often leave
the dance perch at the first sign of disruption by males other than the dominant males
(Foster 1987; McDonald 1989a; McDonald 1993a). The evolution of predefinitive male
plumages is beneficial to both subordinate and dominant males in this type of social
system. For dominant males, the predefinitive plumage of young males immediately
identifies them as not posing a threat to their reproductive success (McDonald 1989b;
McDonald and Potts 1994), which likely reduces the amount of aggression that young
males will receive from older males. Indeed, in the congeneric Blue Manakin
(Chiroxiphia caudata), the amount and intensity of aggression shown by dominant males
toward subordinate individuals decrease with decreasing age of the target individual
(Foster 1987). Moreover, the evolution of age?specific plumages can provide additional
information about the status of males within the dominance hierarchy. In support of this
hypothesis, a taxidermy mount experiment revealed that male Long?tailed Manakins
responded more strongly to males in definitive plumage than to males in predefinitive
plumage (McDonald 1993a). Moreover, responses were often initiated by non?alpha
males, suggesting that the model intruders posed a threat to established male?male
alliances rather than a risk of stolen copulations (McDonald 1993a). These observations
20
are paralleled in Blue Manakins, where aggression directed toward a transgressor was
often initiated by males of intermediate rank, and directed toward the individuals nearest
them in the hierarchy (Foster 1981). These studies suggest that males are most likely to
challenge males of similar rank in a hierarchy and, presumably, against whom they have
the greatest probability of success. The obverse of this is that males are also most likely
to have to defend their own positions against challenges from members of their own or
adjoining age cohorts. A model presentation experiment in another species with a graded,
multi?year delay in plumage maturation, the Hawaiian 'Elepaio (Chasiempis
sandwichensis), yielded similar findings (VanderWerf and Freed 2003).
Female plumage
Extreme sexual dichromatism is characteristic of the family Pipridae. Male
manakins are usually brightly colored, while females are typically olive green (Prum
1997; Doucet et al. 2006). In this study, we document considerable variation in the
plumage of female Long?tailed Manakins. Some females developed variable amounts of
red or tawny coloration in the crown, reminiscent of the red crowns of males, and a small
proportion of females developed black feathers on the face, head, wing, or tail. Older
females were more likely to develop red or tawny crowns than were young females, and,
on average, more than five years elapsed between initial female captures and the
appearance of red in their crowns. Female ornamentation may have evolved as a
by?product of genetic correlations between male and female traits (Lande 1987;
Amundsen 2000). Strong selection for elaborate ornaments in males, combined with
weaker selection against these traits in females, could lead to the expression of
21
ornamental coloration in females, even if it is maladaptive. Because females are solely
responsible for parental care in manakins, they should experience strong natural selection
for crypsis (Martin and Badyaev 1996), particularly since rates of nest predation are so
high in the tropics (Stutchbury and Morton 2001). Yet bright female coloration has been
reported in a number of manakin genera (Graves 1981), and, in Long?tailed Manakins,
females with red crowns were more likely to express other male?like plumage
characteristics. Our documented association between ornamental color and age in older
females could be proximately mediated by age?related hormonal changes (Kimball and
Ligon 1999). In some cases, male?like plumage characteristics other than crown color
disappeared after the following molt, suggesting that they may have resulted from
adventitious feather loss and replacement at a time of year when environmental cues,
such as photoperiod or daytime light intensity (Gwinner 2003), led to the growth of more
male?like plumage.
A less likely possibility is that the development of red crown coloration in older
females serves a social signaling function. Because of its association with age, red crown
coloration could signal a female?s longevity or viability. Such a signal might be useful to
males, who could optimize their display intensity or sperm allocation by investing more
in females they deem to be of high quality (e.g., Amundsen 2000; Werner and Lotem
2003), a pattern which may explain some of the variation in male display intensity in this
species. Alternatively, a signal of female age might be useful to young females, whose
mate choice decisions could be influenced by those of older, experienced females when
multiple females observe displaying males together (Dugatkin and Godin 1993; Doucet et
al. 2004). Comparative analyses of the relationship between male and female
22
ornamentation, in combination with intraspecific empirical investigations of the
proximate control and signal function of female traits, will help to identify the relative
merit of these hypotheses in explaining the evolution of bright female plumage in
manakins.
Timing of molt
Long?tailed manakins undergo a post?juvenal molt within four months of
hatching and subsequently undergo a prebasic molt each year. The first?prebasic molt is
incomplete, as birds of both sexes retain their juvenal remiges and distal greater coverts.
Second?year birds also retain the yellow?orange mouth color typical of nestlings of this
species (Foster 1976). A similar pattern of delayed maturation in mouth color has been
reported in one species of bowerbird (Frith and Frith 2004). Given the considerable
number of species that show delayed maturation in iris and soft?part color (Lawton and
Lawton 1986), delayed maturation in mouth color may be relatively widespread and
should be investigated in other species.
We found significant age? and sex?based variation in timing of molt. Females
exhibited an early peak of molt activity in February and March. Second?year females
were more likely to show signs of early molt than older females. Nevertheless, fewer than
half of females showed signs of early molt activity, and this molt was limited to some
body and head feathers. Molt activity was low from May through July in females, and
increased in August to a second peak, corresponding to the complete prebasic molt, in
October. The decrease in molt activity from April to July may reflect evolutionary
pressure to avoid the costs of molt?breeding overlap (Foster 1974), as this period
23
corresponds to the peak of female nesting activity (Foster 1976). Molt and breeding are
both energetically demanding (e.g., Murphy and King 1992; Lindstrom et al. 1993). As
such, physiological and ecological trade?offs are expected to occur between these two
life?history traits (Foster 1975b). Theory therefore predicts that molt and breeding should
be temporally segregated, yet molt?breeding overlap has been reported in a number of
tropical and temperate passerines (Foster 1975a; Pyle 1997) and, as we have shown here,
occurs at the population level in Long?tailed Manakins (Fig. 2). However, our data show
that in May, June, and July, fewer than 15% of females exhibited any signs of molt. Later
in the season, females? primary resource consuming activity can switch from breeding to
molt (see Foster 1975a), which may explain the second, most prominent peak of female
molt activity in October.
Though they provide no parental care, male Long?tailed Manakins may expend
considerable amounts of energy in breeding?related activities and are, therefore, also
expected to avoid molt?breeding overlap. Dominant (alpha and beta) males perform
energetically demanding dance displays for females and sing duets at high rates to attract
females to their leks (up to 5000 vocalizations/day, Foster 1977; McDonald 1989b;
Trainer and McDonald 1993). By June, there is usually a notable decrease in male display
activity, especially at the least successful leks (S. M. Doucet and D. B. McDonald,
unpubl. data), which, as we have shown here, corresponds to a sharp increase in
proportion of males in definitive plumage showing signs of molt. Females, on the other
hand, are known to nest until at least July, and probably until September (Foster 1976).
Male display activity is intrinsically linked to the availability of receptive females. A
successful copulation, however, marks only the beginning of a female?s parental
24
responsibilities. Thus, the reproductive periods of dominant males and females are
inherently staggered, which may explain why the post?breeding molt of males in
definitive plumage peaks earlier than that of females. Moreover, many
definitive?plumaged males occupy subordinate ranks at leks. These males are expected to
expend much less energy on display than dominant males, and to curtail their breeding
season activities sooner.
Over the course of the breeding season, young male Long?tailed Manakins in
predefinitive plumage form affiliations with other males at particular lek sites, often
practicing courtship displays on dance perches used by dominant males. Young males are
tolerated at dance perches only in the absence of females, however, as only dominant
males display for, and copulate with, females (McDonald 1989a). Moreover, young
males are resighted at leks less frequently than older males (McDonald 1989a),
suggesting that they invest less time and energy in breeding?season activities than do
older males. Thus, young males can begin molting earlier in the season than older
individuals. Correspondingly, blue?back and black?face males exhibit an earlier peak of
molt activity than males in definitive plumage.
Early molt in red?cap males is more difficult to interpret. Many males in red?cap
plumage begin to molt in March, at the onset of the breeding season. Moreover, this molt
is apparently restricted to the crown and head. Indeed, these males often molt in
additional red crown feathers and black face feathers, thereby accelerating their transition
into black?face plumage. Dominance interactions among males of the same age cohort
may explain this early molt. If crown and mask color allow males to assert their
dominance over members of their own age cohort, then selection might favor the
25
acceleration of such a molt. Males in predefinitive plumages, particularly younger ones,
are subject to opposing selective forces: by signaling their lesser age, they may reduce the
aggression directed toward them by older males; at the same time, however, it might
benefit them to develop, as much as possible, the traits that signal their prowess to males
of the same cohort (Foster 1987; McDonald 1993a). This conflict may explain why some
species progress through several distinct predefinitive plumage stages rather than molting
into the same predefinitive plumage for several years, as has been shown in a number of
other species (Frith and Beehler 1998; Frith and Frith 2004).
Implications
Male Long?tailed Manakins in predefinitive plumage have testes capable of
producing sperm (Foster 1987). Thus, delayed plumage maturation in this species
represents an instance of heterochrony, and, more specifically, of neoteny; that is, a
slowing down of somatic maturation relative to sexual maturation (Lawton and Lawton
1986). Mean testis size among 60 definitive plumaged males was 29.3 ? 16.16 mm
3
(Foster 1987). Interestingly, the testis size of a beta male, known to have been in
definitive plumage for several years, was 75 mm
3
, nearly three standard deviations above
the mean (D. B. McDonald, unpubl. data), suggesting that plumage maturation likely
precedes full testis maturation in this species. Long?tailed manakins may, therefore,
exhibit both neoteny and progenesis (where somatic maturation precedes reproductive
maturation). Lawton and Lawton (1986) proposed that heterochronic trends in plumage,
iris, and soft?part maturation are associated with complex social organization within the
Corvidae and may have played a role in speciation among closely related corvids. As
26
empirical investigations of delayed plumage maturation become more widely available,
particularly among tropical species, it will be possible to examine patterns of
heterochrony, and the complex mixing of neotenic and progenetic features, in other
groups that vary in degree of social organization, including other manakins (Prum 1997).
The increasing availability of well?supported phylogenies will greatly facilitate these
comparative investigations. Studies of delayed plumage maturation across a wider variety
of taxa, particularly species that differ from the typical north?temperate pattern, are likely
to reveal that the adaptive significance of delayed plumage maturation cannot be
encompassed by a single hypothesis. Moreover, accumulating evidence of interspecific
variation in both patterns and consequences of delayed plumage maturation suggest
broader evolutionary implications than originally anticipated.
ACKNOWLEDGEMENTS
We are extremely grateful to all of our research assistants and Earthwatch volunteers for
their help with field data collection and to D. Mennill for help with museum data
collection and comments on the manuscript. S. Doucet thanks R. Blanco and the ?rea de
Conservaci?n Guanacaste for permission to work in Santa Rosa; D. McDonald thanks A.
Hoge and J. and J. Stuckey for permission to work on their property; M. Foster thanks E.
Carmona B. and the Ministerio de Agricultura y Ganader?a of Costa Rica for housing and
permission to work at the Jim?nez Station. We thank the curators at the following
institutions for providing access to or loans of the specimens in their research collections:
Academy of Natural Sciences, Philadelphia; American Museum of Natural History;
California Academy of Sciences; Carnegie Museum of Natural History; Field Museum of
27
Natural History; Florida Museum of Natural History; Louisiana State University Museum
of Natural Science; Moore Laboratory of Zoology, Occidental College; Museum of
Vertebrate Zoology, University of California, Berkeley; National Museum of Natural
History; Natural History Museum of Los Angeles County; University of Arizona;
University of Kansas; University of California, Los Angeles (including the Donald R.
Dickey Collection); and Western Foundation of Vertebrate Zoology. We thank Richard
Laval for providing the photo in Figure 1E. Funding to D. McDonald was provided by
the National Geographic Society, the Harry Frank Guggenheim Foundation, and the
Earthwatch Institute. Funding to S. Doucet was provided by the Natural Sciences and
Engineering Research Council of Canada, Sigma?Xi, the American Ornithologists?
Union, the Wilson Ornithological Society, the Explorer?s Club, the American Museum of
Natural History, Auburn University, and NSF grant 420647 (to G. E. Hill). Work by M.
Foster was supported in part by a National Science Foundation Fellowship, the American
Museum of Natural History, Sigma Xi, and the U.S. Fish and Wildlife Service.
28
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Table 1. Summary of plumage development in male long?tailed manakins. Plumage descriptions summarize the typical
appearance of males in each plumage stage.
Age range
(months since
hatching)
Age name
 a
(calendar year)
Plumage stageName of
plumage stage
Plumage description
0?4 hatch?yearjuvenaljuvenalOlive green throughout with paler wash below
4?15 second?yearfirst?basicred?capOlive green body and flight feathers; partial red crown
15?27third?yearsecond?basicblack?faceOlive green body and flight feathers; small red crown; black face or hood
27?39fourth?yearthird?basicblue?backBlack and green body and flight feathers; red crown; blue and green mantle
? 39 ? fifth?yeardefinitive?basicdefinitiveBlack body and flight feathers; red crown; blue mantle
a
Age terminology follows (Pyle 1997); see Methods for explanation.
33
34
Table 2. Summary of sequential plumage transitions recorded in male long?tailed
manakins.
Plumage transitionsNumber of recorded instances
Typical
Green to red-cap1
Red?cap to black?face60
Black?face to blue?back60
Blue?back to definitive48
Definitive to definitive343
Potential anomalies
Green to black?face2
Red?cap to blue?back2
35
FIGURE CAPTIONS
Figure 1. Photographs showing typical appearance of long?tailed manakins 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, (E) male in definitive
plumage. Photo in (E) by Richard Laval.
Figure 2. 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 indicate the 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.
Figure 3. Photographs showing the crowns of: (A) a young male long?tailed manakin in
red?cap plumage and (B) a female long?tailed manakin with some red crown feathers.
Note differences in the distribution of red on the crown, the distribution of red on
individual feathers, and the length of red crown feathers.
36
Figure 1.
A
c
E
D
B
C
37
Figure 2.
Proportion 
of  
birds 
molting
0
0.2
0.4
0.6
0.8
1.0
JFMAMJJASOND
Month
0
0.2
0.4
0.6
0.8
1.0
0
0.2
0.4
0.6
0.8
1.0
0
0.2
0.4
0.6
0.8
1.0
0
0.2
0.4
0.6
0.8
1.0
10
4
65
112
157
53
23
5
3
14
10
10
62
13
4256
20
2
6
0
13
5
5
4
19
26
47
22
9
5
2
1362
6
9
20
34
10
5
5
11
2
2
10
22
61
171
124
62
42
39
3
16
13
20
23
A - Females
E - Males in definitive plumage
B - Red-cap males
C - Black-face males
D - Blue-back males
38
A
B
Figure 3
39
CHAPTER 2. COMPLEX PATTERNS OF SEXUAL DIMORPHISM IN
CHIROXPHIA MANAKINS: INTERACTING EFFECTS OF NATURAL AND
SEXUAL SELECTION?
40
ABSTRACT
Sexual size dimorphism is a widespread biological phenomenon. In birds, males are most
often the larger sex, although there exists extensive variation in both the direction and
magnitude of dimorphism across species. Several hypotheses have been proposed to
explain the evolution of sexual size dimorphism, and these can be classified into two
categories: ecological hypotheses and sexual selection hypothesis. In this study, we
investigate the explanatory power of these hypotheses in elucidating patterns of sexual
size dimorphism in Chiroxiphia manakins, with particular emphasis on the long?tailed
manakin, C. linearis. We captured 361 wild long?tailed manakins and measured variation
in six morphological traits: wing size and shape, body mass, bill size and shape, the
length of elongated central rectrices (tail plumes), tail length, and tarsus length. We
measured a subset of these traits in 872 museum specimens distributed among all five
species in the genus Chiroxiphia. Male long?tailed manakins has longer, broader wing
that bore less weight per unit area than females; they also had longer tarsi and tail plumes
than females. Females weighed more, had longer, wider bills and longer tails than males.
Patterns of sexual dimorphism in bill length, tarsus length, and body mass were generally
similar among other Chiroxiphia manakins. Our findings were consistent with the
predictions of three hypotheses. First, compared with females, the body mass and wing
shape of males should enhance flight maneuverability during courtship displays, as
predicted by the Acrobatic Displays Hypothesis. Second, males and females diverged in
bill size and shape in a direction opposite to that predicted from differences in tarsus
length, as predicted by the Intersexual Competition Hypothesis. Finally, the higher body
mass, higher wing loading, higher wing aspect ratio, and larger bills of females should
41
enhance their capacity to catch flying insects, carry more weight, lay larger eggs, and
forage more efficiently, as predicted by the Reproductive Role Division Hypothesis. Our
findings suggest that both natural and sexual selection have had an important influence
on the evolution of complex patterns of sexual dimorphism in Chiroxphia manakins,
although further research is needed to confirm the relative influence of each selection
mechanism on particular morphological traits within this group. Our study identifies a
promising approach for comparative investigations of sexual dimorphism in other avian
groups exhibiting similar life?history traits.
42
INTRODUCTION
Systematic differences in body size between the sexes of a species is a widespread
biological phenomenon (Darwin 1871; Ralls 1976; 1989; Shine 1989; Andersson 1994a;
Fairbairn 1997). Among invertebrates and poikilothermic vertebrates, females are most
often the larger sex, whereas in mammals and birds, males are usually the larger sex
(Shine 1989; Andersson 1994a; Fairbairn 1997). Ever since the publication of Darwin?s
treatise on sexual selection (Darwin 1871), such sexual dimorphism has been of broad
interest to evolutionary biologists, and several hypotheses have been proposed to explain
the evolution and maintenance of size?dimorphic traits. These hypotheses can be
classified into two categories: ?Sexual Selection Hypotheses? and ?Ecological
Hypotheses?. It is important to recognize that although some of these hypotheses focus on
the selective advantage of a particular body size in one sex, the evolution of sexual size
dimorphism ultimately results from sex?specific patterns of selection on body size.
Differences in the sum of all natural and sexual selection pressures can lead to the
evolution of different size optima for different traits in males and females (Price 1984;
Hedrick and Temeles 1989; Andersson 1994a; Badyaev et al. 2000). Because of strong
genetic correlations between the sexes (Lande 1980), dimorphism evolves only when
selection for a particular trait in one sex is counterbalanced by opposing selection in the
other sex. Thus, depending on the strength and direction of selection, the sum of selection
pressures in males and females can either reinforce or constrain the evolution of
dimorphism (Price 1984; Schluter et al. 1991; Meril? et al. 1997; Badyaev et al. 2000;
Badyaev 2002).
43
According to sexual selection hypotheses, size?dimorphic traits evolve because
they directly (via female choice) or indirectly (via male?male competition) enhance
mating opportunities (Darwin 1871; Andersson 1994a). In particular, the ?Direct
Competition Hypothesis? proposes that male?biased size dimorphism evolves because
larger body size in males is favored in competitions over mates or resources (Table 1,
Darwin 1871; Andersson 1994a). In elephant seals, Mirounga angustirostris, for
example, males engage in physical contests over access to reproductive females; larger
males are more successful in these contests and experience greater reproductive success
(Le Boeuf and Reiter 1988). Indeed, in many species, larger males are more successful
than smaller males at monopolizing access to females, high?quality territories, or other
resources (Andersson 1994a).
Sexual selection can also favor the evolution of the reverse pattern of size
dimorphism, with females being larger than males. Occasionally, reversed sexual
dimorphism accompanies a near complete reversal of sex roles, where females become
the competitive sex. This pattern, also consistent with the Direct Competition Hypothesis,
is well?documented in avian groups such as jacanas and coucals (e.g., Andersson 1995;
Emlen and Wrege 2004; Goymann et al. 2004; Andersson 2005) as well as in sex?role
reversed seahorses and pipefish (Jones and Avise 2001). Alternatively, in birds, small
male body size may be favored by sexual selection in species wherein males perform
acrobatic aerial sexual displays (Payne 1984; Jehl and Murray 1986; Hedenstr?m and
M?ller 1992; Blomqvist et al. 1997). This ?Acrobatic Displays Hypothesis? proposes that
small body size enhances a male?s ability to perform acrobatic displays requiring a high
degree of agility and coordination (Table 1). Comparative studies suggest that sexual
44
selection for male display agility may be responsible for the evolution of small male body
size in shorebirds and waders (e.g., Figuerola 1999; Szekely et al. 2000).
Two primary ecological hypotheses have been proposed to explain the evolution
of sexual size dimorphism: the ?Intersexual Competition Hypothesis? and the
?Reproductive Role Division Hypothesis? (Table 1). The Intersexual Competition
Hypothesis proposes that sexual size dimorphism evolves to reduce intersexual
competition for food resources (Darwin 1871; Selander 1966; Selander 1972; Hedrick
and Temeles 1989; Shine 1989). The reasoning is that sexual dimorphism in body size,
particularly for feeding?related traits, allows the sexes to exploit different ecological
niches and thereby reduces intersexual competition for food (Darwin 1871; Selander
1966; Selander 1972; Hedrick and Temeles 1989; Shine 1989). Testing this hypothesis
poses several difficult challenges, and conclusive supporting evidence remains relatively
sparse (Hedrick and Temeles 1989; Shine 1989). Striking examples exist nonetheless,
including mosquitoes, where female mouth parts are adapted for sucking blood whereas
male mouthparts are adapted for ingesting nectar (Darwin 1871; Proctor et al. 1996), and
the extinct New Zealand huia, Neomorpha acutirostris, where remarkable sexual
differences in bill size and shape presumably allowed males and females to forage on
different prey types (Darwin 1871; Andersson 1994a). Recently, Temeles and colleagues
(Temeles et al. 2000; Temeles and Kress 2003) provided compelling evidence that
pronounced bill length dimorphism in the purple?throated carib hummingbird, Eulampis
jugularis, is associated with specialization in each sex for feeding on a different species
of Heliconia.
45
A second ecological hypothesis, the ?Reproductive Role Division? hypothesis
(Table 1), proposes that sexual dimorphism evolves as a consequence of the different
reproductive roles of males and females (Darwin 1871; Ralls 1976; Hedrick and Temeles
1989; Shine 1989; Andersson 1994a; Fairbairn 1997). In many animals, the size of
gametes differs between males and females (anisogamy) and the sexes invest
differentially in various aspects of reproduction (e.g., incubation, brooding, nest defense,
offspring provisioning). Such differences may lead to the evolution of different optimal
body sizes for males and females. In vespertilionid bats, for example, large female body
size may have evolved to facilitate the female?s task of carrying young offspring (Myers
1978). Selection based on reproductive role division can result in either male?biased size
dimorphism or female?biased size dimorphism (Andersson 1994a), and the outcome will
largely depend on the degree of anisogamy, the mating system, and the division of
parental care.
Ecological and sexual selection hypotheses are commonly presented as alternative
explanations for the evolution of sexual size dimorphism and are often studied
independently (Hedrick and Temeles 1989). As we have emphasized, however, natural
and sexual selection may interact to lead to the evolution of different size optima in males
and females (Price 1984; Hedrick and Temeles 1989; Andersson 1994a; Badyaev et al.
2000). Thus, studies that adopt an integrative approach considering both ecological and
natural hypotheses should provide a clearer picture of the selective forces shaping sexual
dimorphism.
In this study, we evaluate the explanatory power of the Direct Competition,
Acrobatic Displays, Intersexual Competition and Reproductive Role Division hypotheses
46
in elucidating patterns of sexual size dimorphism in Chiroxphia manakins, with particular
emphasis on the long?tailed manakin, C. linearis. Manakins (Aves: Pipridae) are small,
largely frugivorous, suboscine passerines distributed throughout the Neotropics. Most
manakins follow a lek?based mating system wherein assemblages of displaying males
compete for copulations with females (Snow 2004). Males typically perform complex,
acrobatic courtship displays to attract females (Prum 1994; Prum 1997; Snow 2004). This
mating system leads to extreme female choosiness and high variance in male mating
success (McDonald 1989b; McDonald 1993; Shorey 2002; Snow 2004). Consequently,
the intensity of sexual selection is thought to be particularly high among manakins in
general (Prum 1997; Snow 2004), and Chiroxiphia manakins in particular (Foster 1981;
McDonald 1993). Females, on the other hand, do not appear to compete for copulations
(Snow 2004). Moreover, as in all lek?mating species (H?glund and Alatalo 1995), female
manakins are entirely responsible for all aspects of parental care, from building the nest,
to incubating the eggs, to caring for nestlings and fledglings (Snow 2004). The sexes also
differ in the sizes of their home ranges, with females and young males having home
ranges several times as large as those of adult males (Graves et al. 1983; McDonald
1989a; McDonald 1989b; Th?ry 1992; Snow 2004). And, in long?tailed manakins at
least, the sexes exhibit a remarkable divergence in demographic variables, including age
at first reproduction, age?specific fecundities, and age?specific survival probabilities
(McDonald 1993). Together, these observations suggest that the selection pressures
shaping morphology may be remarkably divergent in male and female manakins.
Chiroxiphia manakins differ from other manakins in two important ways. First,
they exhibit extended delays in plumage maturation (Foster 1987a; Snow 2004; DuVal
47
2005), with long?tailed manakins, C. linearis exhibiting the longest recorded delay of
four years (Doucet et al. 2006). This delayed plumage maturation parallels a delay in
behavioral maturation, as immature males usually do not compete for copulations with
females (e.g., Foster 1981; McDonald 1989a; McDonald 1989b). The morphology of
young males may therefore be particularly informative, as it should reflect an increasing
influence of sexual selection with age. Second, males cooperate to perform displays for
females (Snow 2004). Although manakins in other genera also perform joint displays,
obligate cooperative display is apparently restricted to Chiroxiphia (Snow 2004). In
long?tailed manakins, males establish age?structured dominance hierarchies at leks. The
two most dominant males at each lek perform complex, dual?male displays for females
(Foster 1977; McDonald 1989a; McDonald 1989b). These displays involve alternating
backward leapfrog displays, where each male alternately jumps over the other male while
hovering briefly at the apex of the jump, and butterfly displays, where males alternately
or simultaneously perform slow, labored butterfly flights and rapid dives between the
display perch and branches and vines up to 20 m away (McDonald 1989b). Displays in
other Chiroxiphia manakins are similar (Snow 2004), although in C. caudata they
frequently involve more than two males (Foster 1981).
Predictions: Sexual Selection Hypotheses
We investigated sexual dimorphism and ontogenetic variation in six
morphological traits of long?tailed manakins (Table 1): (1) wing size and shape; (2) body
mass; (3) bill size and shape; (4) tail plume length; (5) tail length; and (6) tarsus length.
We also measured a subset of these traits among museum specimens of all five species in
48
the genus Chiroxiphia. According to the Direct Competition Hypothesis, male?male
competition should favor larger overall body size in males (Table 1) (Darwin 1871;
Andersson 1994a). According to the Acrobatic Displays Hypothesis, selection should
favor male morphology that enhances the efficiency of male displays (Table 1) (Jehl and
Murray 1986). Based on flight aerodynamic theory, selection for flight endurance as well
as maneuvering and hovering and ability should favor a combination of low body mass
and long, broad wings among adult males (details in methods) (Jehl and Murray 1986;
Rayner 1988; Pennycuick 1989; Norberg 1990; Hedenstr?m and M?ller 1992). In
addition, longer tails should be favored to improve lift and maneuverability whereas
shorter tail plumes (elongated central rectrices) should be favored to decrease drag
(Balmford et al. 1993; Thomas 1993; Norberg 1995).
Predictions: Ecological Hypotheses
According to the Intersexual Competition Hypothesis, the sexes should exhibit
morphological divergence in traits relating to feeding, although the direction of
dimorphism cannot be predicted (Selander 1966; Selander 1972; Hedrick and Temeles
1989; Shine 1989). Manakins are gape?size limited frugivores; that is, they swallow most
fruits whole (Pratt and Stiles 1985; Wheelwright 1985; Foster 1987b; Snow 2004). This
method of feeding imposes constraints on both the maximum size of fruits that can be
eaten and the optimal size for minimizing handling time (Wheelwright 1985; Foster
1987b; Levey 1987). This hypothesis therefore predicts that males and females should
particularly diverge in bill size and shape. According to the Reproductive Role Division
Hypothesis, divergence in the reproductive roles of male and female manakins should
49
result in morphological divergence between the sexes (Darwin 1871; Ralls 1976; Shine
1989). Both male?biased and female?biased size dimorphism can evolve through this
mechanism, although most hypotheses ascribed to this category predict that large body
size should be favored in females (Darwin 1871; Ralls 1976; Shine 1989; Andersson
1994a). Larger females may benefit from increased fecundity, improved nest defense, and
a greater energy storage capacity (Andersson 1994a). Reproductive Role Division
Hypotheses predicting smaller body size in females (e.g., rapid onset of breeding in
fluctuating environments or early maturation) (Andersson 1994a) do not apply to the
breeding system of manakins. In addition to larger female body mass, flight aerodynamic
theory predicts that Reproductive Role Division should favor the evolution of long,
narrow wings in females, which would provide greater load?lifting capacity and higher
potential flight speeds during foraging flights (details in methods) (Jehl and Murray 1986;
Rayner 1988; Pennycuick 1989; Norberg 1990; Hedenstr?m and M?ller 1992). Because
manakins are gape?size limited frugivores (Wheelwright 1985; Foster 1987b) and
females are solely responsible for feeding offspring, large, wide bills may also be favored
in females. Gape size in frugivores is positively correlated with the mean and maximum
(but not minimum) size of fruits eaten (Pratt and Stiles 1985; Wheelwright 1985) and in
long?tailed manakins, there is a close correspondence between gape size and both the
size distribution of fruit species eaten and the size distribution of individual fruits eaten
(Wheelwright 1985). Larger bills would therefore allow females to access a broader
range of fruit species and fruit sizes, as might be favored by the demands of uniparental
care.
50
Predictions: predefinitive males
To have any chance of reproducing, male long?tailed manakins must first survive
for at least eight years (McDonald 1993). Thus, early male ontogeny should favor traits
that enhance survival. As they age, however, young males should face increasingly
intense selection to adopt the morphology most beneficial to survival and reproduction
among older males (Badyaev 2002). If female morphology more closely approaches
optimal body size, and sexual selection drives older males away from this optimum (Price
1984), we predict that young males should exhibit intermediate trait morphology between
females and older males.
METHODS
Wild birds
We studied long?tailed manakins from March to July, 2003?2005 in Santa Rosa National
Park, Guanacaste, Costa Rica (10? 40? N, 85? 30 W). We captured 361 long?tailed
manakins using mist nets. We fitted each individual with a unique combination of up to
three colored leg bands and one numbered aluminum leg band. Females are usually
entirely olive?green, whereas males show age?specific variation in plumage coloration
(Doucet et al. 2006). We aged male birds in predefinitive plumage as second?year,
third?year, or fourth?year males based on plumage characters as described in Doucet et
al. (2006). Males in definitive adult plumage, hereafter adult males, were assumed to be
in their fifth calendar year or older (Doucet et al. 2006). Genetic sexing of all birds
captured in 2003 (n = 145) using sex?specific genetic primers (Griffiths et al. 1998)
confirmed that these criteria are sufficient to accurately sex birds during the breeding
51
season. Additionally, we confirmed the sex and/or age assignments of many individuals
by the presence of a brood patch, sex?specific behavior exhibited during behavioral
observations at leks, as well as stasis (females) or changes (males in predefinitive
plumage) in plumage coloration in subsequent years (Doucet et al. 2006).
Morphometry
We measured the right tarsus length and bill length (from the anterior edge of the
nare to the tip of the upper mandible) of each bird to the nearest 0.1 mm and the
unflattened wing chord and tail length of each bird to the nearest 0.5 mm. Long?tailed
manakins have a pair of elongated central rectrices (tail plumes). We measured the length
of both the left and right tail plume of each bird and used the mean of these two
measurements in our analyses. We weighed each bird to the nearest 0.25 g. The mass of
females can be artificially inflated if they are carrying eggs, and indeed, females with
brood patches were significantly heavier than females without brood patches (t = ?3.21, n
= 34, 146, P = 0.001). However, this pattern could be caused by any combination of
follicular growth (Kullberg et al. 2002a; Guillemette and Ouellet 2005), increased energy
reserves during incubation (Kullberg et al. 2002b), and/or an association between body
size and the likelihood of reproducing in females. Most importantly for the purposes of
this study, the sex differences in body mass reported below remain highly significant
even when only females without brood patches are considered (P <0.0001).
To obtain more detailed information about bill and wing shape, we collected
additional measurements of individuals captured in 2005. We measured the total length
of the bill from the tip of the upper mandible to the nasofrontal ridge, as well as the width
52
and depth of the bill at the nares (to the nearest 0.1 mm). We collected wing size and
shape measurements following the methods outlined by Pennycuick (1989) and Hertel
and Ballance (1999). We measured total wing length as the distance from the sternum to
the tip of the outstretched wing along the ventral surface of the bird; wingspan was thus
twice the total wing length (Fig. 1). To calculate wing area, we traced the fully
outstretched wing with the wing positioned ventral side down. We digitized this tracing
and used the program Image J 1.3 (National Institutes of Health, USA) to determine its
area. The tracing was shorter than the wing length because of the body area between the
proximal edge of the wing and the sternum, known as the root box (Pennycuick 1989).
This rectangular area was quantified by multiplying the width of the wing where it meets
the body with the difference between the total wing length and the length of the wing
tracing (Fig. 1). The root box was added to the partial wing area and the total area was
therefore twice this value (Fig. 1). We used these data to calculate aspect ratio and wing
loading (Rayner 1988; Norberg 1990; Hertel and Ballance 1999). We calculated aspect
ratio as wing span
2
/wing area. Higher values for this index indicate a comparatively
narrow wing and lower values a comparatively broad wing. We calculated wing loading
as body mass X gravitational acceleration constant (a)/ wing area. Wing loading
describes the weight (force) that is borne per unit area of the wings in Newtons/m
2
.
We used aerodynamic theory to evaluate how variation in these traits would
influence flight performance in manakins (Andersson and Norberg 1981; Rayner 1988;
Pennycuick 1989; Norberg 1990). We focused on 10 flight parameters as outlined in
Hedenstr?m and M?ller (1992)(Table 2). (1) Minimum turning radius and (2) roll
acceleration influence the ability to make tight turns and are therefore measures of
53
maneuverability. (3) Minimum gliding speed influences the ability to make accurate
landings. (4) Minimum sink speed in gliding flight, (5) mimimum power in hovering
flight, and (6) power in flapping flight all influence endurance. (7) Best glide ratio is
proportional to the maximum lift?to?drag ratio and is associated with generally efficient
flight performance. (8) Terminal speed in gliding dive and (9) maximum linear
acceleration are speed parameters usually thought to influence hunting capacity. (10)
Climb rate in flapping flight influences load?lifting capacity (Hedenstr?m and M?ller
1992). We followed the predictions outlined by Hedenstr?m and M?ller (1992) to
determine how variation in body mass, wing span, wing area, aspect ratio, and wing
loading would influence these different flight parameters and determined which sex
would be expected to show better performance for each parameter based on phenotypic
differences.
Museum data
We measured specimens from each of the five species in the genus Chiroxiphia,
totaling 872 specimens, at the Louisiana State University Museum of Natural Science and
the American Museum of Natural History (Table 3). We measured the tarsus length and
bill length of each specimen as described above for wild birds. We noted the mass of
birds from specimen tags when available. Birds in entirely green plumage were identified
as males or females as indicated on specimen tags. Birds of unknown sex were excluded
from our analyses.
54
Statistical analyses
We used Shapiro?Wilk tests to determine whether variables were normally
distributed and used non?parametric tests when variables departed significantly from
normality. Small variations in sample size occur because not all information was
available for all birds. We did not measure traits that appeared anomalous (e.g., bill
deformities, broken feathers, growing feathers).
RESULTS
Ontogeny of male morphology
There were significant differences in wing length (ANOVA, F = 10.64, df = 3, 171, P <
0.0001), tail length (ANOVA, F = 37. 31, df = 3, 168, P < 0.0001), tail plume length
(ANOVA, F = 227.46, df = 3, 164, P < 0.0001), and mass (ANOVA, F = 8.43, df = 3,
169, P < 0.0001) among male long?tailed manakins of different age classes (Fig. 2A?D).
Tail length (r
s
 = ?0.66, n = 172, P < 0.0001) and mass (r
s
 = ?0.22, n = 173, P = 0.003)
were significantly negatively correlated with age class, whereas tail plume length was
significantly positively correlated with age class (r
s
 = 0.85, n = 168, P < 0.0001). Wing
length was also significantly positively correlated with age class (r
s
 = 0.24, n = 172, P <
0.0001), but this pattern was driven by the significantly shorter wings of second?year
males (Tukey?Kramer test, P < 0.05). By contrast, there were no significant differences
in bill length (ANOVA, F = 1.80, df = 3, 168, P = 0.15) or tarsus length (ANOVA, F =
0.95, df = 3, 165, P = 0.41) among males of different age classes (Fig. 2E, F). Thus, to
maximize our sample sizes in comparisons with females, we pooled males of all age
classes for analyses of bill and tarsus length, pooled after?second?year males for analyses
55
of wing length, and included only males in definitive plumage for analyses of the
remaining morphological traits.
Sexual dimorphism in long?tailed manakins
Male long?tailed manakins had significantly longer wings (Fig. 3A; t = ?8.97, n =
298, P < 0.0001), tail plumes (Fig. 3C; t = ?59.40, n = 143, 59, P < 0.0001), and tarsi
(Fig. 3F; t = ?15.17, n = 346, P < 0.0001) than females. By contrast, females had
significantly longer tails (Fig. 3B; t = 6.73, n = 238, P < 0.0001) and bills (Fig. 3E; t =
12.71, n = 175, 170, P < 0.0001), and weighed significantly more (Fig. 3D; t = 11.58, n =
242, P < 0.0001), than males.
Sex differences in individual traits can result from overall differences in body
size. We verified that sex differences in morphological traits were not simply an
allometric consequence overall differences in body size by regressing Log
10
?transformed
morphological traits on Log
10 
of tarsus length and comparing the residuals of these
regressions between males and females. We used tarsus length as an index of structural
body size as it is not influenced by short?term variation in nutritional condition and does
not change with age (Rising and Somers 1989; Freeman and Jackson 1990; Webster
1997). Even when controlling for tarsus length, males had significantly longer tail plumes
(t = ?16.16, n = 226, P < 0.0001) and wings (t = ?2.56, n = 234, P = 0.01) than females.
Female?biased dimorphism in bill length, tail length, and mass cannot be simple
by?products of differences in structural body size, as females had shorter tarsi than
males. Indeed, dimorphism in these traits increases when controlling for tarsus length (all
P < 0.0001).
56
Morphological predictors of sex and age classes
We used discriminant function analysis (DFA) to determine whether the six
morphological traits we measured could accurately differentiate birds in different age and
sex classes. We entered tarsus length, bill length, wing length, tail length, tail plume
length, and mass into the DFA as measurement variables and age/sex class as
classification variables.  We found significant morphological differentiation according to
age and sex class (Fig. 4; F
 
= 503.8, df  = 6, 322, P <0.0001). The first and second
canonical axes explained 90.2% and 8.9% of age? and sex?related variation in
morphology, respectively, and the discriminant analysis predicted sex and/or age class
with 84% accuracy. Most errors in classification involved the misclassification of females
as second?year males and vice?versa (20% of errors), or the misclassification of males
into an age class adjacent to the one they belonged in (72% of errors). No classification
errors involved the misclassification of females as males in definitive adult plumage or
vice versa.
Sexual dimorphism in bill size and shape
All three components of bill size were sexually dimorphic in long?tailed
manakins. Females had significantly longer (t = 6.6, n = 21, 28, P <0.0001), wider (t =
4.0, n = 21, 27, P = 0.0002) and deeper (t = 3.53, n = 21, 28, P = 0.0008) bills than males.
However, both bill depth (r = 0.47, n = 49, P = 0.0007) and width (r = 0.30, n = 49, P =
0.04) were positively correlated with bill length. We therefore used the residuals of
regressions of bill width and depth on bill length to investigate dimorphism in bill shape.
Residual bill width (t = 2.24, n = 21, 27, P = 0.03) but not depth (t = 1.03, n = 21, 28, P =
57
0.30) was significantly higher in females than males, indicating that the bills of females
were significantly wider than predicted from increases in length alone.
Ontogeny of male wing size and shape
There were significant differences in wing area (Fig. 5A; F = 6.85, df = 3, 24, P =
0.002), aspect ratio (Fig. 5B; F = 6.76, df = 3, 24, P = 0.002), and wing loading (Fig. 5C;
F = 3.29, df = 3, 24, P = 0.004), but not wing span (Fig. 5D; F = 0.82, df = 3, 24, P =
0.49) among males in different age classes. Wing area increased significantly with age (r
s
= 0.68, n = 27, P < 0.0001) whereas aspect ratio decreased significantly with age (r
s
 =
?0.65, n = 27, P = 0.0001). Wing loading was not linearly related to age, as it was
intermediate among second? and third?year males, highest among fourth?year males, and
lowest among definitive plumaged males (Fig. 5C). We therefore pooled males of all age
classes for analyses of sex differences in wingspan, but restricted our analyses to males in
definitive plumage analyses of sexual differences in wing area, aspect ratio, and wing
loading.
Sexual dimorphism in wing size and shape
Male long?tailed manakins had significantly larger wing areas (Fig. 6A; t = ?7.66,
n = 21, 7, P <0.0001) and longer wing spans (Fig. 6D; t = ?6.23, n = 21, 28, P <0.0001)
than females, whereas females had significantly higher wing loading (Fig. 6C; t = 6.62, n
= 21, 7, P <0.0001) and aspect ratios (Fig. 6B; t = 2.70, n = 21, 7, P = 0.01) than males.
Based on aerodynamic theory, we were able to determine how changes in body mass and
these four measures of wing size and shape would influence 10 different flight
58
parameters (Norberg 1990; Hedenstr?m and M?ller 1992), which then allowed us to
predict which sex would show better performance for each flight parameter (Table 2).
Based on their morphology, males are predicted to outperform females in
maneuverability, landing accuracy, flight endurance, and general flight efficiency (Table
2). By contrast, females are predicted to outperform males in load?lifting capacity and
some components of flight speed (Table 2).
We used measures of wing size and shape, bill size and shape, and body mass to
construct a three?dimensional morphospace, which provided a graphical representation of
relationships between individuals of each sex. We used principal components analysis
(PCA) to calculate a single variable that could summarize variation for each of bill
morphology and wing morphology. We performed a first PCA on bill width, depth, and
length. All three measures had high positive loadings on the first PC axis, which
explained 54% of the variation in bill morphology. We performed a second PCA on
wingspan, wing area, and aspect ratio. Wing area and wingspan had high positive
loadings on the first PC axis whereas aspect ratio had a moderate negative loading on this
axis, which explained 58% of the variation in wing morphology. We standardized body
mass, bill PC1, and wing PC1 to a mean of zero and a standard deviation of one and
plotted these values in a three?dimensional morphospace (Fig. 7). Male and female
long?tailed manakins occupied substantially different regions of the morphospace with
relatively little overlap. Males had a small body mass, long, broad wings, and short,
narrow bills. By contrast, females had a larger body mass, short, narrow wings, and long,
broad bills (Fig. 7).
59
Sexual dimorphism in Chiroxiphia manakins
Museum specimens of long?tailed manakins exhibited similar patterns of
dimorphism to those we documented in wild?caught birds. Males had significantly longer
tarsi (t = ?7.1, n = 119, P < 0.0001) than females, whereas females had significantly
longer bills (t = 4.5, n = 120, P < 0.0001) than males (Table 3). Although females
weighed more, on average, than males, this difference was not statistically significant (t =
1.46, n = 16, P < 0.16).  Other manakins in the genus Chiroxiphia showed similar
patterns of sexual dimorphism. There was no significant difference in morphology
between males in predefinitive plumage and males in definitive plumage (all P > 0.10),
thus we pooled all males in the following analyses (Table 3). Males had significantly
longer tarsi than females in blue manakins, Chiroxiphia caudata (t = ?9.2, n = 223, P <
0.0001), blue?backed manakins, Chiroxiphia pareola (t = ?4.4, n = 213, P < 0.0001),
lance?tailed manakins, Chiroxiphia lanceolata (t = ?6.9, n = 156, P < 0.0001), and
Yungas manakins, Chiroxiphia boliviana (t = ?4.5, n = 102, P = 0.001). By contrast,
females had significantly longer bills than males in blue manakins (t = 3.7, n = 101, P =
0.0003), blue?backed manakins (t = 6.6, n = 220, P < 0.0001), lance?tailed manakins (t =
2.2, n = 164, P = 0.03), and Yungas manakins (t = 3.8, n = 101, P = 0.0002). Females also
weighed significantly more than males in blue?backed manakins (t = 2.4, n = 56, P =
0.02), lance?tailed manakins (t = 3.2, n = 9, P = 0.01), but not in Yungas manakins (t =
0.85, n = 75, P < 0.40). We could not assess sex differences in mass among blue
manakins, as too few of the specimens that we examined had mass information available
on specimen tags. Instead, we report data from Foster (1987b).
60
To compare the degree of dimorphism in different morphological traits across
Chiroxiphia manakins, we calculated a dimorphism index (Greenwood 2003) for each
trait as log
10
(mean male value/mean female value). This dimorphism index results in
positive values when males are the larger sex and negative values when females are the
larger sex (Fig. 8). The degree of male?biased dimorphism in tarsus length was highly
conserved among Chiroxiphia manakins (Fig. 8). By contrast, there was considerable
interspecific variation in the degree of female?biased dimorphism in bill length and body
mass (Fig. 8).
DISCUSSION
Our investigation of morphological variation in a marked population of long?tailed
manakins revealed complex patterns of sexual dimorphism in body size and body shape.
In particular, adult males had significantly longer tarsi, wings, and elongated tail plumes
than females. By contrast, females had significantly longer tails and bills, and weighed
significantly more than males. In most cases, young males exhibited trait values
intermediate to those of females and adult males. These patterns of dimorphism are
unusual in that the identity of the larger sex depends on the trait being considered. In
most species, the larger sex is usually larger for all traits considered, even among
taxonomic groups where both normal and reverse sexual size dimorphism are common
(e.g., Andersson and Norberg 1981; Szekely et al. 2000). Such intraspecific variation in
the degree and direction of dimorphism is unexpected, as morphological traits are usually
strongly genetically correlated (e.g., Badyaev and Hill 2000; Via and Hawthorne 2005).
61
These unusual patterns of dimorphism suggest that there has been strong selection for
morphological differentiation among male and female long?tailed manakins.
The Direct Competition Hypothesis predicts that selection should favor overall
larger body size in males (Table 1). Our findings did not support these predictions, as
males were smaller than females for most traits measured, and the few traits in which
males were larger than females, namely wing length and tail plume length, are unlikely to
be used in agonistic intrasexual interactions. Levels of male?male aggression are
relatively low at long?tailed manakin leks, and orderly male queues thought to be
reinforced by female preference for low levels of disruption (Foster 1983; Foster 1987a;
McDonald 1993).
The Acrobatic Displays Hypothesis predicts that selection should favor long,
narrow wings and a small body mass in males (Table 1). Aerodynamic flight efficiency
should also favor shorter tail plumes and longer tails (Table 1). Some of our findings are
consistent with the Acrobatic Displays Hypothesis. In particular, males had significantly
larger wing areas and significantly longer wingspans than females, whereas females had
significantly higher wing loading and aspect ratios than males. Thus, relative to females,
males have larger, longer, and broader wings that bear less weight per unit area.
According to flight aerodynamic theory, this morphology confers males with high flight
maneuverability by allowing them to make tight turns and accurate landings (Norberg
1990; Hedenstr?m and M?ller 1992). In addition, this phenotype would provide males
with high endurance in both hovering and flapping flight (Norberg 1990; Hedenstr?m and
M?ller 1992). Endurance in hovering flight would benefit males during the performance
of dual?male leapfrog displays. Because hovering flight is energetically expensive
62
(Norberg 1990), the morphology of adult males should allow them to perform these
displays at a reduced energetic cost and could thereby enable them to perform higher
quality displays, to spend more time displaying, and/or to devote more energy to other
important aspects of courtship (McDonald 1989b). Endurance in flapping flight and the
ability to make tight turns would benefit males during butterfly displays, which involve
both slow labored flights and fast dives to and from the dance perch through flight paths
often obstructed by vegetation. Finally, increased ability to make accurate landings would
benefit both components of courtship displays. Our findings therefore suggest that sexual
selection may have favored the evolution of morphological traits that increase the
efficiency of courtship displays in adult male long?tailed manakins. Indeed, one study
documented a significant, positive association between the duration of the butterfly
display and mating success in long?tailed manakins (McDonald 1989b), suggesting an
influence of sexual selection. The number of leapfrog displays showed a similar pattern,
although the relationship was not significant (McDonald 1989b). Further analyses of the
relationship between flight performance and wing morphology in particular individuals
(e.g., Blomqvist et al. 1997) or experimental manipulations of wing shape or wing
loading (e.g., Evans and Thomas 1992) would be particularly informative. Sex
differences in wing morphology may be paralleled by additional differences in anatomy
and physiology. In golden?collared manakins, Manacus vitellineus, for example, the
wing muscles of males show morphological adaptations to rapid and forceful contractions
(Schlinger et al. 2001; Schultz et al. 2001) and wing contractions appear to be modulated
in part by sexually dimorphic patterns of sensitivity to sex steroids in spinal cord neural
63
circuits (Schultz and Schlinger 1999). Such physiological and anatomical adaptations to
display behavior remain to be investigated in other manakins.
As documented in other populations (Foster 1977; McDonald 1989a; McDonald
1989b; Arevalo and Heeb 2005), the length of elongated tail plumes increased with male
age and was highly sexually dimorphic. By contrast, the length of regular tail feathers
decreased with age. These patterns are inconsistent with the Acrobatic Displays
Hypothesis, as longer tail plumes increase drag and shorter tails reduce lift (Balmford et
al. 1993; Thomas 1993; Norberg 1995). A more likely explanation is that elongated tail
plumes in males evolved by sexual selection through female preference for long tails
(Prum 1997). Whether tail plume length remains a current target of sexual selection is
unclear, although McDonald (1989b) found no evidence of an association between tail
plume length and reproductive success in long?tailed manakins. Our finding that, in
males, tail length decreases with age whereas tail plume length increases with age is
particularly puzzling. Because variation in the size of these traits is likely to be regulated
by hormonal changes (Kimball and Ligon 1999; Badyaev 2002), it is difficult to envision
how the same hormonal environment could cause a simultaneous increase and decrease in
the size of different components of the same trait. Males have been captured with their
central rectrices (tail plumes) in various stages of replacement without any signs of molt
among other tail feathers (Doucet et al. 2006), and this temporal segregation of molt may
enable a divergent pattern of growth for the tail plumes and regular tail feathers. The
adaptive significance, if any, of this divergent pattern remains unclear. Limiting resources
may result in an energetic trade?off in length between the different types of tail feathers.
Contrary to the predictions of such a hypothesis, however, there was a significant positive
64
relationship between tail length and tail plume length in second?year males (r = 0.29, n =
54, P = 0.03) and no significant relationship between these two traits among males in
other age classes (all P >0.1). Another possibility is that shorter tail feathers serve as a
signal amplifier by enhancing the appearance of length in the elongated tail plumes
(Hasson 1990; Hasson 1991; Arevalo and Heeb 2005). Finally, it is possible that females
prefer shorter tails and longer tail plumes in males precisely because these traits impose
aerodynamic costs. Thus, short tails and long tail plumes in adult males may serve as
sexually?selected handicaps (Zahavi 1975; Zahavi 1977).
Some of our findings were also consistent with ecological hypotheses. The
Intersexual Competition Hypothesis predicts that males and females should diverge in
traits related to feeding (Table 1). We discovered that females had longer, deeper, and
wider bills than males, as well as bills that were wider than predicted by differences in
length alone. These differences are even more pronounced when variation in structural
body size is taken into account, as females have shorter tarsi than males. Indeed, these
differences in bill morphology meet Selander?s (1966; 1972) conservative criteria that the
only reliable evidence for intersexual niche competition is a sex difference in a trait
related to foraging that is both in a direction opposite to that predicted by sexual selection
and of a larger magnitude than that predicted by differences in body size alone. The
reasoning behind Selander?s (1966; 1972) criteria is that sex differences in foraging
ecology may be a simple consequence of sexual dimorphism that has evolved through
another mechanism, such as sexual selection for large body size in males (e.g., Webster
1997). Further research is needed to determine whether sex differences in bill
morphology are accompanied by sex differences in foraging ecology in long?tailed
65
manakins. Intriguingly, sex differences in foraging ecology have been documented in a
closely?related manakin (Marini 1992).
The Reproductive Role Division hypothesis predicts that sexual dimorphism
evolves as a consequence of the divergent reproductive roles of males and females (Table
1). This hypothesis makes no general prediction about the direction of dimorphism, but a
number of sub?hypotheses have been proposed based on life history characteristics in
particular groups (see Andersson 1994a for specific examples). Because females do not
perform acrobatic displays and are solely responsible for offspring care, we predicted that
reproductive role division would favor large body mass, long, narrow wings, and large,
wide bills in females. Our findings supported all of these predictions. First, females
weighed significantly more than adult males. Larger female body size may be beneficial
in its own right, as it may allow females to defend nests more successfully (Andersson
and Norberg 1981), although this interpretation is doubtful for such a small species.
Larger female body size may also confer greater fecundity by either of two routes: larger
size can allow for the production of larger eggs because it provides more internal space
for eggs or because the energy storage capacity required for producing eggs increases
more rapidly with body size than do metabolic costs (Downhower 1976; Andersson
1994a). Indeed, female manakins in general (Snow 2004), and long?tailed manakins in
particular (Foster 1976b), lay relatively large eggs for such small birds (approximately
15% of their body mass). This egg size is 17% larger than that predicted for a passerine
bird and 15% larger than that predicted for a Tyrannid (Rahn et al. 1975).
As further support of the Reproductive Role Division Hypothesis, compared with
males, females have shorter, narrower wings that bear more weight per unit area. This
66
morphology would result in higher load lifting capacity and higher acceleration capacity
in flapping flight and terminal speed in gliding dives (Norberg 1990; Hedenstr?m and
M?ller 1992). In addition to compensating for their higher body mass, high load?lifting
capacity could be beneficial to female long?tailed manakins in two ways. First, females
must carry the eggs. A 15 % increase in body mass, even if it must be borne only for a
short time, will place high energetic demands on flight, and the increased load?carrying
capacity of females should partially compensate for this. Similarly, the increased
load?carrying capacity of females should facilitate their task of carrying food to the nest.
Acceleration capacity in flapping flight and terminal flight speed in gliding dives are
typically thought to benefit aerial predators (Andersson and Norberg 1981; Hedenstr?m
and M?ller 1992). These same flight parameters may increase female efficiency at
capturing insects in flight. Although most manakins are largely frugivorous, females
supplement their own diets with insects to a larger extent than do males, and they feed
their offspring an even larger proportion of insects than they ingest themselves (Snow
2004).
That females had longer, wider bills than males may also support the
Reproductive Role Division hypothesis. Manakins, like many frugivorous birds, are
gape?size limited (Wheelwright 1985; Levey 1987; Snow 2004). Accordingly, there is a
close correspondence between gape size and both the mean and maximum diameter of
fruits eaten (Wheelwright 1985; Snow 2004). When feeding offspring, females either
carry fruit in their bills or regurgitate previously ingested items (Foster 1976b; Snow
2004). A larger gape would allow females to ingest larger fruits or to carry more fruit in
their bills than males. Because take?off and landing are costly for birds with high wing
67
loading, females should select the largest fruits available to maximize energy gain
(Norberg 1990), and this would apply both to ingesting food for themselves and to
feeding offspring. Moreover, having larger bills provides females with a greater potential
resource base, as it allows them to eat larger fruits without compromising their ability to
eat small fruits (Wheelwright 1985; Levey 1987; Avery et al. 1993; Rey et al. 1997), and
should also allow them to capture flying insects more effectively (e.g., Keast et al. 1995).
Hence females, and, indirectly, their offspring, may be better equipped to deal with
periods of food scarcity caused by stochastic events (Foster 1976a). Finally, compelling
recent studies suggest that predation intensity has had a important influence on life
history evolution in birds (Martin et al. 2000; Martin 2002). In particular, these studies
suggest that higher predation pressure in the tropics constrain the rate at which parents
can deliver food to their young (Martin et al. 2000; Martin 2002). Larger bills should
reduce the number of foraging trips required to deliver food to offspring, thereby
reducing the exposure of females and nestlings to potential predators. Because sexual
dimorphism in bill length remains highly significant even when controlling for body mass
(t = 6.33, n = 175, 170, P < 0.0001), our data suggest that large bill size in females is not
simply a consequence of the energetic demands of higher body mass in females.
Taken together, our findings suggest that both ecological and sexual selection
pressures may be responsible for the evolution of sexual dimorphism in long?tailed
manakins. In particular, our findings were consistent with some predictions of the
Acrobatic Displays, Intersexual Competition, and Reproductive Role Division
hypotheses. Our data do not allow us to directly attribute patterns of dimorphism to a
particular mechanism, as further investigation of natural and sexual selection pressures on
68
morphological traits in each sex will be required to confirm our interpretations (e.g., Price
1984). Nonetheless, our data identify likely hypotheses that clearly warrant further
investigation. Moreover, our findings highlight the importance of considering both
ecological and sexual selection hypotheses in investigations of sexual dimorphism. Many
studies focus on only one or the other of these mechanisms (Hedrick and Temeles 1989),
and in a lek?mating group like manakins, sexual selection might be favored as the key
driving force behind the evolution of dimorphism. Our findings suggest, however, that
ecological mechanisms, including Intersexual Competition and Reproductive Role
Division, may be equally important. Indeed, sexual selection and ecological selection
may reinforce each other. For example, whereas the Acrobatic Displays Hypothesis
predicts small body size and long, narrow wings in males, the Reproductive Role
Division hypothesis predicts a nearly opposite pattern in females. Similarly divergent
influences of sexual and ecological selection might be expected in other lek?mating
species, as the reproductive roles of males and females differ strongly by definition in
this type of mating system (Bradbury 1981; H?glund and Alatalo 1995). Such opposing
selection pressures are consistent with the idea that patterns of dimorphism reflect the
sum of natural and sexual selection pressures acting separately on males and females
(Price 1984; Schluter et al. 1991; Meril? et al. 1997; Badyaev et al. 2000; Badyaev 2002),
and may in fact be a necessary precursor to the evolution of dimorphism.
Males in predefinitive plumage generally exhibited trait values intermediate to
those of females and males in definitive plumage. Indeed, morphological variation alone
was sufficient to categorize most (84%) individuals into appropriate sex and/or age
categories. For all feather traits and body mass, younger males were more similar to
69
females than to older males. Thus, dimorphism in these traits increases with male age.
Because morphological changes in young males were paralleled by striking changes in
plumage coloration and behavior converging on that exhibited by adult males (Doucet et
al. 2006), we propose that ontogenetic changes in male body mass and wing morphology
reflect the increasing influence of sexual selection for courtship display efficiency.
Sexual dimorphism in wing shape and body mass may reflect a compromise between
different flight characteristics in manakins. Flight endurance and maneuverability will
provide the greatest benefit to those few males that invest the most in, and stand to gain
the greatest benefits from, courtship displays. Yet, this morphology may be costly among
males who do not hold dominant status at leks and cannot therefore display for females
and compete for copulations. Similarly, load?lifting capacity and flight speed may benefit
some components of female fitness at the expense of others. Their higher wing loading,
for example, likely makes them more vulnerable to predation due to slower take?off
speeds (Kullberg et al. 2002a; Kullberg et al. 2002b; Kullberg et al. 2005). Such
trade?offs may in part explain why the phenotype of young males is intermediate to that
of females and adult males.
Alternative explanations have been proposed to explain patterns of dimorphism
similar to those we documented. For example, some studies suggest that smaller bill size
can enhance vocal performance in male birds by allowing them to sing trilled songs at a
faster rate or higher bandwidth (Podos et al. 2004a; Podos and Nowicki 2004). This
mechanisms is unlikely to be important in manakins, however, as males dot no typically
sing trilled vocalizations (Trainer and McDonald 1993; Snow 2004). Further research is
needed to determine whether other types of vocalizations are subject to similar
70
performance constraints (Podos et al. 2004b). If so, sexual selection for vocal
performance and, indirectly, small bill size in males, may serve as an additional
reinforcing mechanism explaining the patterns of dimorphism documented in this study.
A second alternative explanation is that the lower body mass of adult males is not an
adaptive response to selection for display efficiency, but rather reflects the costs of sexual
advertisement and display (McDonald 1989a). McDonald (1989a) documented similar
patterns of dimorphism and age?graded changes in body mass in another population of
long?tailed manakins. In that population, however, older males gained weight during the
non?breeding season, such that they did not weigh significantly less than females. Such a
breeding?season induced weight reduction in males could reflect the energetic costs of
extended periods of advertisement and display (McDonald 1989a; McDonald 1989b;
Andersson 1994b). Although this alternative hypothesis deserves further investigation, it
does not necessarily preclude an adaptive advantage of low body mass as predicted by the
Acrobatic Displays Hypothesis.
Many of the patterns of sexual dimorphism that we documented in long?tailed
manakins were paralleled in other Chiroxiphia manakins. In particular, males had
significantly longer tarsi whereas females had significantly longer bills in all four species.
Females also weighed significantly more in two of the three species for which these data
were available, but not in Yungas manakins or blue manakins (Foster 1987b). We did not
measure the wing lengths of museum specimens. However, Payne (1984) reports
male?biased dimorphism in wing length four species of Chiroxiphia manakins. In our
wild?caught long?tailed manakins, wing length was positively correlated with wing area
(r = 0.36, n = 49, P = 0.009), and this likely applies to other Chiroxiphia manakins. Given
71
that females generally weigh more than males, their wing loading will probably be
greater than that of males. Such similarities in patterns of dimorphism are interesting in
light of the fact that Chiroxiphia manakins also share many similarities in life history
traits. Four of the species are known to exhibit a lek?based mating system with
cooperative male displays, female?only parental care, and delayed male plumage
maturation (Foster 1977; Foster 1987a; Snow 2004). Further investigation of possible
associations between the degree of wing?length, bill?length, and body mass dimorphism
and interspecific variation in courtship displays and feeding ecology would be
particularly informative, both within Chiroxiphia and among the Pipridae. In C. caudata,
for example, intrasexual male aggression at display perches is more common (Foster
1981; Foster 1983) and selection for competitive ability may drive male body size away
from that optimal for display efficiency. These opposing selection pressures may explain
the absence of sexual dimorphism in body mass for C. caudata (Foster 1987a).
Payne (1984) first suggested that reversed sexual size dimorphism may have
evolved to facilitate aerial displays in manakins. Our findings within long?tailed
manakins and among Chiroxiphia manakins offer partial support for this hypothesis.
Payne (1984) also suggested that reversed size dimorphism was more common among
smaller manakin species. However, Chiroxiphia manakins, all of which show clear
patterns of reversed dimorphism in some traits, are among the largest in the family (Snow
2004). No study has considered the adaptive significance of sexual dimorphism in bill
size and shape among the Pipridae. If, as suggested by our findings in Chiroxiphia
manakins, gape?size limited frugivory and female?only parental care favor larger bill
dimensions in females, other species that share these life history traits should exhibit
72
similar patterns of dimorphism in bill size. Our hypothesis receives anecdotal support in
at least one group of birds. Among the bowerbirds (Ptilonorhynchidae), a predominantly
frugiviorous family, females have relatively larger bills in polygynous species with
female?only parental care than in monogamous species with bi?parental care (Frith and
Frith 2004). As partly frugivorous birds exhibiting variation in mating systems, the
bowerbirds, birds of paradise, tyrannid flycatchers, manakins, and cotingas offer several
opportunities for comparative tests of this hypothesis.
We have documented unusually complex, age?specific patterns of male?biased
and female?biased sexual size dimorphism in long?tailed manakins and other members
of the genus Chiroxiphia. Overall body size and wing shape are likely to be constrained
by features common to all of these species. Manakins are primarily forest?dwelling birds
(Snow 2004), and flying in environments cluttered with vegetation favors the evolution
of relatively short wings, regardless of taxonomic affiliations (Norberg 1990). Similarly,
manakins forage primarily by sallying for fruits (Snow 2004). This foraging behavior,
along with a disproportionately wide gape, allows manakins to exploit fruits to a greater
extent than larger but less specialized frugivores such as tanagers (Snow 2004). However,
aerial sallies are energetically expensive and make particular demands on body size and
wing morphology (Norberg 1990). Our findings suggest that, despite these general
constraints on body morphology, differing and often opposing selective forces driven by
sexual divergence in life history traits has led to the evolution of complex, age?related
patterns of sexual dimorphism in long?tailed manakins. Moreover, our data are consistent
with predictions of both Sexual Selection Hypotheses and Ecological Hypotheses. Our
findings suggest that both sexual selection and ecological selection have played an
73
important role in shaping the sexually divergent morphologies of manakins. The
evolution of dimorphism in manakins has likely been strongly influenced by their
lek?based mating system. Such a mating system places intense sexual selection pressure
on males while simultaneously segregating the reproductive roles of males and females.
The subsequent evolution of striking sex differences in life history traits may then favor
morphological divergence through differences in the relative influence of natural and
sexual selection on male and female morphologies.
ACKNOWLEDGEMENTS
We thank A. Lindo, L. Baril, V. Connolly, J. Marko, and D. Mennill for field assistance
and the Guanacaste Conservation Area and R. Blanco for logistical support in Costa Rica.
We are grateful to the curators and collection managers at the American Museum of
Natural History and the Natural History Museum of Louisiana State University for
providing access to specimens under their care and for logistical support and to D.
Mennill for help with museum data collection. We thank H. Fadamiro, C. Guyer, and F.
S. Dobson for comments on this manuscript, J. Podos for discussion, and J. Podos and S.
Huber for providing access to a manuscript in press. Funding was provided by a
Collections Study Grant and the Frank M. Chapman Memorial Fund from the American
Museum of Natural History, a Wetmore Research Award from the American
Ornithologists? Union, a Sigma?Xi Grant?in?Aid of Research, the Exploration Fund of
the Explorer?s Club, the Louis Agassiz Fuertes Research Award from the Wilson
Ornithological Society, two Auburn University Graduate Research Awards, and a Natural
Sciences and Engineering Research Council of Canada Post Graduate Scholarship to S.
74
Doucet, a Research and Sponsored Projects Grant from California State University
Northridge to F. Hertel, and NSF grant IBN0235778 to G. Hill.
75
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Table 1. Predicted direction of dimorphism for morphological traits in long?tailed manakins based four non?mutually exclusive
hypotheses. See text for explanations and sources of hypotheses.
Sexual Selection HypothesesEcological Hypotheses
Direct CompetitionAcrobatic DisplaysIntersexual CompetitionReproductive Role Division
Overall influenceFavors overall large body
size in males
Favors small body size and
long, broad wings in males
Favors divergence between
the sexes for
feeding?related traits
Consequence of different
reproductive roles of males
and females
Predictions
Wing size and shapeLarge male wingsLong, broad male wingsEquivocalLong, narrow female wings
Body massLarge male body massSmall male body massEquivocalLarge female body mass
Bill size and shapeLarge male billsEquivocalMales ? femalesLarge, broad female bills
Tail plume lengthLong male plumesShort male plumesEquivocalEquivocal
Tail lengthLong male tailsLong male tailsEquivocalEquivocal
Tarsus lengthLong male tarsiEquivocalEquivocalEquivocal
Table 2. Flight parameters, their associated measures of performance, and the sizes or magnitudes of four morphological traits
that should enhance performance for each specific flight parameter (see Hedenstr?m and M?ller 1992). The final column
indicates which sex is predicted to show higher performance for each parameter based on the morphological variation
documented in this study.
Flight parameterPerformanceMassWingspanWing areaAspect ratioWing loadingSex
1. Min turning radiusManeuverabilityLowNo effectSmallLowLowMales
2. Roll accelerationManeuverabilityHighLongLargeUnknownHighEquivocal
3. Min gliding speedLanding accuracyLowNo effectLargeLowLowMales
4. Min sink speed in gliding flightEnduranceLowLongLargeUnknownHighMales
5. Min power in hovering flightEnduranceLowShortNo effectLowLowMales
6. Power in flapping flightEnduranceLowShortNo effectLowLowMales
7. Best glide ratioEfficient flightNo effectLongLargeHighHighEquivocal
8. Terminal speed in gliding diveSpeed HighLongNo effectHighHighFemales
9. Max linear accel. in flapping flightSpeed HighLongNo effectHighHighFemales
10. Climb rate in flapping flightLoad?lifting capacityHighLongNo effectHighHighFemales
Table 3. Means ? standard deviations of morphological traits in museum specimens of male and female Chiroxiphia manakins.
SpeciesSpecimens Measured
?
Tarsus length (mm)Bill length (mm)Mass (g)
MaleFemaleMalesFemalesMalesFemalesMalesFemales
blue manakin
(C. caudata)
14288 21.12 ? 0.8920.04 ? 0.78*6.66 ? 0.326.83 ? 0.35*22.60 ? 1.1522.65 ? 1.61
blue?backed manakin
(C. pareola)
17251 19.12 ? 0.9418.42 ? 1.05*6.28 ? 0.416.72 ? 0.43*16.91 ? 1.8118.17 ? 2.01*
long?tailed manakin
(C. linearis)
96 26 18.78 ? 0.5717.87 ? 0.58*5.81 ? 0.356.15 ? 0.31*18.33 ? 1.9719.72 ? 0.98*
lance?tailed manakin
(C. lanceolata)
13630 18.95 ? 0.6118.04 ? 0.78*6.44 ? 0.346.59 ? 0.38*17.17 ? 0.3220.60 ? 2.09*
Yungas manakin
(C. boliviana)
93 12 18.86 ? 0.6518.05 ? 0.73*5.83 ? 0.336.22 ? 0.30*17.81 ? 1.3818.21 ? 1.34
?
Sample sizes differ for different morphological measurements (see text for details).
* Identifies statistically significant (P < 0.05) differences between males and females (see text for details).
88
FIGURE CAPTIONS
Figure 1. Schematic diagram illustrating aspects of wing morphology measurements in
the long?tailed manakin. The fully outstretched wing was traced with the wing positioned
ventral side down. The tracing was shorter than the wing length because of the body area
between the proximal edge of the wing and the sternum, known as the root box (dashed
line). This rectangular area was quantified by multiplying the width of the wing where it
meets the body by the difference between total wing length and the length of the wing
tracing. The root box area was then added to the traced wing area, resulting in one half of
the wing area (shaded in grey). The total wing area was thus twice this value.
Figure 2. Box plots showing differences in morphological traits among male long?tailed
manakins in different age classes. Horizontal lines in box plots show 10
th
, 25
th
, 50
th
, 75
th
,
and 90
th
 percentiles. With the exception of tarsus and bill length, all traits vary
significantly with male age (see text for statistical details).
Figure 3. Box plots showing sex differences in morphological traits in long?tailed
manakins. Horizontal lines in box plots show 10
th
, 25
th
, 50
th
, 75
th
, and 90
th
 percentiles. All
traits are significantly different between sexes (see text for statistical details).
Figure 4. Scatterplot of canonical axes 1 and 2 of a Discriminant Function Analysis in
long?tailed manakins where sex and age categories were the classification variables and
six morphological variables (wing length, tarsus length, bill length, tail length, tail plume
length, and mass) were the measurement variables. Shown are females (open circles),
89
second?year males (light grey circles), third?year males (medium grey circles),
fourth?year males (dark grey circles), and fifth?year or older males (black circles).
Figure 5. Box plots showing differences wing in morphology among male long?tailed
manakins in different age classes. Horizontal lines in box plots show 10
th
, 25
th
, 50
th
, 75
th
,
and 90
th
 percentiles. All traits vary significantly with male age (see text for statistical
details).
Figure 6. Box plots showing sex differences in wing morphology in long?tailed
manakins. Horizontal lines in box plots show 10
th
, 25
th
, 50
th
, 75
th
, and 90
th
 percentiles. All
traits are significantly different between sexes (see text for statistical details).
Figure 7. Three?dimensional morphospace of wing size and shape, bill size and shape,
and body mass showing how males (filled circles) and females (open circles) occupy
different areas of the morphospace (see text for details of PC axes).
Figure 8. Sexual dimorphism indexes for three morphological traits based on
measurements from museum specimens of Chiroxiphia manakins. Positive values are
obtained for traits where males are larger than females and negative values are obtained
for traits where females are larger than males (see text for details of calculations). Mass
data for C. caudata from (Foster 1987b).
90
Figure 1.
root box
wing span
91
Figure 2.
wing 
length 
(mm) 
67
69
71
73
75
tail 
length 
(mm) 
26
28
30
32
34
36
38
plume 
length 
(mm)
50
90
130
170
mass 
(g)
15
16
17
18
19
20
bill length
 
(mm)
4.5
5.0
5.5
6.0
6.5
7.0
age class
A B
C
D
E F
tarsus 
(mm) 
18
19
20
21
22
2
nd
 year3
rd
 year4
th
 year?5
th
 year
age class
2
nd
 year3
rd
 year4
th
 year?5
th
 year
92
Figure 3
tarsus 
length  
(mm) 
18
19
20
21
22
bill length (mm)
4.0
4.5
5.0
5.5
6.0
6.5
7.0
wing 
length 
(mm) 
67
69
71
73
75
tail 
length 
(mm) 
26
28
30
32
34
36
38
plume 
length 
(mm)
30
50
70
90
110
130
150
170
mass 
(g)
16
18
20
22
24
A B
C D
E
F
female               male
female               male
sex sex
93
Figure 4
-28
-27
-26
-25
-24
-23
-22
-21
-20
canonical 2
02468101214
canonical 1
94
Figure 5
wing area (cm
2
)
90
95
100
105
110
115
120
125
130
wing 
aspect 
ratio
4.2
4.4
4.6
4.8
5.0
5.2
5.4
5.6
wing 
loading 
(N/m
2
)
20
25
30
35
wing 
span 
(mm)
210
215
220
225
230
235
240
245
A
B
C
D
age class
2
nd
 year3
rd
 year4
th
 year?5
th
 year
age class
2
nd
 year3
rd
 year4
th
 year?5
th
 year
95
Figure 6
wing 
span 
(mm)
210
215
220
225
230
235
240
245
wing 
aspect 
ratio
4.2
4.4
4.6
4.8
5.0
5.2
5.4
5.6
20
25
30
35
wing area (cm
2
)
90
95
100
105
110
115
120
125
130
A B
C D
wing 
loading 
(N/m
2
)
female               male
sex
female               male
sex
96
Figure 7
z
2
1
0
-1
-2
mass
light                            
 
      
heavy
bill
short
narrow
long
wide
2
1
0
-1
-2
3
wings
short
narrow
long
wide
-2
-1
0
1
2
3
97
Figure 8
0.02
0
-0.02
-0.04
-0.08
tarsusmassbill
 
sexual 
dimorphism 
index
C. boliviana
C. linearis
C. lanceolata
C. pareola
C. caudata
98
CHAPTER 3. LEKS, LIGHT, AND LOOKS: DOES THE VISUAL
ENVIRONMENT INFLUENCE DISPLAY CONSPICUOUSNESS IN
LONG?TAILED MANAKINS?
99
ABSTRACT
The conspicuousness of a visual signal depends in part upon the environment in which it
is perceived. In this study, we examined the influence of light environment and visual
background on the conspicuousness of male and female plumage coloration in
long?tailed manakins. We also investigated whether males adjusted the location or timing
of their displays to take advantage of particular light environments. We used reflectance
spectrometry to quantify the plumage coloration of males (n = 62) and females (n = 59)
as well as the coloration of the vegetation comprising the visual background at display
sites. We used irradiance spectrometry to measure light environments at display perches
and at nearby control sites in the forest understory. We analyzed coloration data using
both principal components analysis and an avian visual color space model. Both methods
revealed striking differences in the conspicuousness of males and females. PCA revealed
that the olive?green coloration of females represents a subset of the colors comprising the
visual background of the forest understory, whereas the red, blue, and black coloration of
males occupies a larger portion of the PCA color space and contains unique elements that
are not found in the visual background. The color space model further revealed that
females exhibit low levels of contrast against the background and low levels or contrast
between plumage regions. Males, on the other hand, exhibit high levels of contrast
against the background and contrast between plumage regions. Variation in both the
visual background and the light environment had a pronounced influence on the
conspicuousness of male and female plumage patterns. Male manakins did not, however,
adjust the location or timing of their displays to take advantage of particular light
environments. Instead, they performed the majority of their displays in forest shade, the
100
most common light environment. Our findings suggest that by displaying in forest shade,
long?tailed manakins may optimize the short?distance conspicuousness of male plumage
ornaments while minimizing the long?distance conspicuousness of male ornaments and
the short? and long?distance conspicuousness of female plumage patterns. By so doing,
male manakins can present colorful displays to nearby females while minimizing their
risk of predation from distant predators. Our findings contribute to a growing body of
evidence suggesting that the perceptual environment has an important influence on the
evolution of visual signals used in social communication.
101
INTRODUCTION
In many animals, the coloration or patterning of the skin, fur, feathers, or scales serve as
visual communication signals. The perception of a visual signal by potential receivers
will be influenced by the structural or biochemical properties of the signal, the light
environment in which it is transmitted, the background against which it is viewed, the
visual capabilities of the signal receiver, and further psychophysical processing of the
signal that occurs once it has been detected (Lythgoe 1979; Endler 1990; Guilford and
Dawkins 1991; Endler and Basolo 1998; 1998; Vorobyev et al. 2001; Th?ry 2006).
Whether or not a signal is conspicuous or cryptic depends on the surrounding light
environment and the background against which the signal is viewed (Endler 1990).
Consequently, even the most colorful signals, though undoubtedly conspicuous in some
situations, can appear remarkably cryptic at other times. This concept will be familiar to
anyone who has watched a flock of colorful parrots all but disappear as they alight in a
rainforest canopy. 
Important developments in signal design theory (e.g., Endler 1992; Endler
1993b), visual modeling (e.g., Vorobyev and Osorio 1998; Vorobyev et al. 1998), and
spectrometric measurement and analysis (Endler 1990; Andersson and Prager 2006;
Montgomerie 2006) have motivated new studies in the role of the perceptual environment
in shaping the evolution of colorful signals. In polymorphic bluefin killifish (Lucania
goodei), for example, variation in light environment predicts the relative abundance of
different color morphs, suggesting that selection for efficient communication drives the
evolution of different color morphs in different light environments (Fuller 2002). In a
comparative analysis of Australian birds, differences in color between closely?related
102
pairs of species were associated with differences in habitat (open versus closed) but not
differences in distribution (sympatric versus allopatric), suggesting that variation in the
light environment has a greater influence on plumage color evolution than selection for
species recognition (McNaught and Owens 2002). Among agamid lizards, males were
more conspicuously colored than females in closed habitats, suggesting that coloration
may have been molded by sexual selection, but when coloration and environment were
examined separately for each sex, coloration was associated with habitat openness,
suggesting that natural selection also played an important role (Stuart?Fox and Ord
2004). Light environment also varies along a vertical gradient in forests (Endler 1993a;
Heindl and Winkler 2003b), and a comparative investigation of an avian rainforest
community revealed that patterns of plumage coloration differed across vegetation strata
from the understory to the canopy (Gomez and Th?ry 2004). In particular, male plumage
was more conspicuous than female plumage at each height, and some components of
color appeared to be under natural selection for crypsis, whereas other components
appeared to be under sexual selection for conspicuousness (Gomez and Th?ry 2004).
Finally, a recent comparative study revealed that among Neotropical manakins,
increasing sexual dichromatism was positively associated with plumage contrast against
the background in males but not females, suggesting that sexual selection favors the
evolution of conspicuous male coloration that diverges from background coloration
(Doucet et al. 2006b).
While the studies outlined above clearly suggest that the perceptual environment
has an important influence on the evolution of visual signals, they also highlight two
potential sources of conflict in the evolution of signal design. First, selection for
103
detectability and assessment by conspecifics should favor the evolution of conspicuous
signals, whereas predation pressure should favor the evolution of cryptic signals (Endler
1978; Endler 1991). Second, if the visual signal evolved by sexual selection and if such
selection acts more strongly on males than on females then males should experience
selection for conspicuous coloration, whereas females should experience selection for
cryptic plumage (Endler and Th?ry 1996; G?tmark et al. 1997). Potential resolutions to
these conflicts include the evolution of ornaments that can be displayed facultatively,
such as expandable dewlaps in anoles (e.g., Macedonia et al. 2000), concealable crests in
birds (e.g., Graves 1990), and motile pigment cells in fishes (Fujii 2000) and squids (e.g.,
Hanlon et al. 1994), or the evolution of ornaments that are relatively inconspicuous to
predators because of differences in their visual systems (Hastad et al. 2005). These
potential solutions are relatively rare, however, and animals more commonly adjust their
conspicuousness by varying the timing and/or location of their displays. For example,
guppies (Poecilia reticulata) adjust the timing and location of their displays such that
their coloration patterns are more conspicuous during courtship and less conspicuous at
times of high predation risk (Endler 1991).
Species with lek mating systems tend to display at fixed locations and thereby
offer a tractable system in which to investigate the influence of the visual environment on
the conspicuousness of colorful male ornaments. Endler and Th?ry (1996) discovered that
each of three neotropical, lek?mating species displayed in a subset of the light
environment that enhanced the conspicuousness of their coloration patterns at the time of
display. Heindl and Winkler (2003a) showed that male wire?tailed manakins (Pipra
filicauda) displayed in light environments that enhanced their conspicuousness at short
104
viewing distances while reducing their conspicuousness at long viewing distances,
suggesting a possible resolution of the trade?off between performing conspicuous
courtship displays while avoiding detection by predators. In a separate study, Heindl and
Winkler (2003b) showed that each of four sympatric species of manakins displayed at a
height in the rainforest where the corresponding light environment enhanced some
component of its plumage conspicuousness. Finally, Uy and Endler (2004) found that by
clearing display courts on the ground, male golden?collared manakins (Manacus
vitellinus) modified their visual background in a manner that increased their plumage
contrast and hence conspicuousness.
In this study, we modeled how variation in light environment and visual
background influenced plumage conspicuousness in male and female long?tailed
manakins (Chiroxiphia linearis). We also investigated whether males of this species
varied the location or timing of their displays to take advantage of particular visual
environments. Long?tailed manakins are strikingly sexually dichromatic: males in
definitive plumage have a bright red crown, a sky blue mantle, and contrasting black
body and flight feathers, whereas females are olive green throughout. Before attaining
this definitive plumage in their fifth year, young males progress through several
age?specific intermediate plumages (Doucet et al. 2006a). Long?tailed manakins follow a
lek?based mating system where several males gather at dispersed lek arenas to display to
females. Each lek is characterized by a generally age?graded dominance hierarchy
(Foster 1977; McDonald 1989a; McDonald 1989b). Only the two most dominant males at
each lek perform courtship displays for females (Foster 1977; McDonald 1989a;
McDonald 1989b). These males advertise to females by singing ?toledo? duets from
105
within the subcanopy (Trainer and McDonald 1993). If these duets succeed in attracting a
female to the lek, all three birds fly to a display perch, typically a horizontal vine near the
ground, and the males begin to perform their cooperative displays. During leapfrog
displays, the two males cartwheel over one another in a highly coordinated fashion.
During butterfly flights, the two males alternately or simultaneously perform slow,
labored flights and fast dives between the dance perch and vines or branches up to 20 m
away (Foster 1977; McDonald 1989a; McDonald 1989b). At each lek arena, the vast
majority of these displays are performed on a single perch (McDonald 1989a), which we
term the primary display perch. However, some leks also encompass secondary and
tertiary display perches.
We used irradiance and reflectance spectrometry, visual modeling, and
behavioural observations of long?tailed manakins to achieve five primary objectives.
First, we quantified and compared the reflectance of male and female plumage and the
reflectance of the vegetation comprising the visual background of manakin display areas.
Second, we used irradiance spectrometry to identify and quantify light environments at
display perches and at control sites. Third, we used an avian tetrachromatic color space
model to document how variation in the light environment and the visual background
influences the conspicuous of plumage coloration in male and female manakins. Fourth,
we investigated whether manakins adjust the location of their displays to enhance their
plumage conspicuousness. Finally, we investigated whether manakins adjust the timing
of their displays to enhance their plumage coloration.
106
METHODS
Study site
We studied long?tailed manakins from March to July 2003?2004 in Santa Rosa National
Park, Guanacaste Conservation Area, Costa Rica (10? 40? N, 85? 30 W). This region of
Costa Rica exhibits a pronounced seasonality, with a dry season extending from
December to May, and a rainy season extending from June to November. Our study site
was located in an isolated tract of bottomland moist tropical forest. This forest, locally
known as the Bosque Humedo, consists of primarily evergreen trees and retains a thick
canopy cover year?round (Janzen 1983). The breeding season of long?tailed manakins
extend from February to August, with a marked peak in male display activity and female
lek visitation between March and June (Foster 1977; McDonald 1989a; McDonald 1993).
At our study site, male long?tailed manakins begin to advertise at sunrise and display
throughout the morning. Display activity is sparse and sporadic in the afternoons.
Reflectance of manakin plumage patches
We captured long?tailed manakins by placing mist nets near active display
perches. We marked each individual with a unique combination of one numbered
aluminum leg band and up to three colored leg bands. At the time of capture, we recorded
standard morphometric measurements and collected plumage reflectance data from each
individual. We used a USB2000 reflectance spectrometer and PX?2 pulsed xenon lamp
(Ocean Optics, Dunedin, FL) to collect reflectance readings. Light was delivered from
the light source to the measurement surface, and from the measurement surface to the
spectrometer, via a bifurcated fiber?optic cable and reflectance probe. The probe was
107
encased in a black rubber sheath that excluded external light from the measurement area
and maintained the probe at a fixed distance to, and perpendicular from, the measurement
surface. We measured five body regions for each bird (crown, mantle, tail, wing, breast),
taking five readings from each region. Each reading was composed of 20 readings
collected in rapid succession and averaged by the operating software. Reflectance was
calculated relative to a WS?1 white standard, which reflects > 97% of incident light
(Ocean Optics).
Reflectance of the visual background
Using the equipment and procedures described above for plumage patches, we
measured the reflectance of objects comprising the visual background of manakin display
sites. At each of 14 leks, we measured the reflectance of the bark of the primary display
perch (n = 14), the reflectance of two dead leaves arbitrarily selected from the leaf litter
below the perch (n = 28), the reflectance of the bark of all trees with dbh > 5 cm that
were within a 2 m radius of the display perch (n = 18), and the reflectance of one green
leaf from each of the four saplings nearest to the display perch (n = 56). As with plumage
patches, we collected five readings from each object.
Available light environments
Manakins perform their coordinated dual?male displays on low, horizontal vines
or branches in the forest understory (McDonald 1989b). Based on opportunistic
observations and scheduled behavioral observations (see Light environments and timing
of displays below), we noted that three types of light environment were available for
108
manakin displays: forest shade, small gaps, and cloudy (sensu Endler 1993a). In the first
half of the breeding season, which coincides with the dry season, sunny conditions
prevail and only forest shade and small gap light environments were available for display.
Forest shade light environments characterize the shady understory of closed?canopy
forests in sunny conditions (Endler 1993a). Small gaps interrupt forest shade where small
breaks in the canopy allow small patches of direct sunlight to reach the understory
(Endler 1993a). Cloudy light environments became available during the rainy season,
when intermittent sunny, cloudy, and rainy weather, provided access to all three light
environments. Cloudy light environments characterize the forest understory when the sun
is completely obstructed by clouds (Endler 1993a).
To incorporate the effect of variation in the light environment into our visual
models, we measured these light environments at 24 primary display perches. At each
display perch, we measured the color of ambient light spectra with a USB2000
spectrometer and a cosine corrected fiber optic irradiance probe with a 180? angle of
acceptance and a measurement surface of 6 mm in diameter (CC?3?UV, Ocean Optics).
At each measurement location, we calibrated the spectrometer with a calibration light
source of known color temperature (LS?1?CAL, Ocean Optics). We collected five
readings per location with the probe oriented skyward (perpendicular to the ground) at
the height of the display perch. All spectra were collected between 0540 and 1130 CST.
To control for time of day and seasonal effects, readings at each lek were collected in a
single measurement session, so that we were able to obtain irradiance spectra for all three
light environments in only a few cases (i.e., when sunny and cloudy conditions occurred
in close succession). We obtained forest shade readings at 24 primary display perches,
109
small gap readings at 15 primary display perches, and cloudy readings at 3 primary
display perches. We transformed readings into units of photon flux as described by
Endler (1990) and used a mean irradiance spectrum from each of the three light
environments in the visual models described below.
Visual modeling
Single?cone photoreceptors are responsible for color discrimination in birds, and
most diurnal birds have four types (Cuthill et al. 2000; Hart 2001). These four cone types
are characterized by the wavelengths to which they are most sensitive: long?wavelength
sensitive (LWS), medium?wavelength sensitive (MWS), short?wavelength sensitive
(SWS), and ultraviolet/violet sensitive (UVS/VS). The spectral sensitivity of LWS,
MWS, and SWS photoreceptors is highly conserved in birds, whereas the spectral
sensitivity of UVS/VS photoreceptors peaks near 370 nm (UVS) in most passerines or
near 410 nm (VS) in most non?passerines (Hart 2001).
The color of an object can be represented by a point in perceptual color space
whose coordinate axes represent the quantum catches of cone photoreceptors (Goldsmith
1990). For birds, this perceptual space can be likened to a tetrahedron, with each of the
four photoreceptor types located at a vertex of this tetrahedron (Burkhardt 1989;
Goldsmith 1990). Variation in how two different colors are perceived can be
approximated by calculating Euclidean distances between two points in this
tetrachromatic color space (Goldsmith 1990). However, distances between points in such
a color space do not correspond directly to perceived differences in color because these
distances must exceed a certain threshold to be distinguishable, and this threshold
110
depends on noise that originates in photoreceptors and at further stages of neural
processing (Vorobyev and Osorio 1998; Vorobyev et al. 1998). Vorobyev and colleagues
have developed receptor?noise limited color space models that take into account visual
sensitivities, transmission of the ocular media, light environment, visual background, and
receptor noise, and these models agree well with behavioral data in a variety of taxa
(Vorobyev and Osorio 1998; Vorobyev et al. 1998; Vorobyev et al. 2001; Osorio and
Vorobyev 2005).
We implemented an avian version of this color space model to calculate how
different colored plumage patches would be perceived by manakins. All equations follow
Vorobyev et al. (1998) and further details are provided in Doucet et al. (2006b). Spectral
sensitivities have not been measured in manakins; however, most passerine birds have
UVS photoreceptors (Hart 2001), and long?tailed manakins have SWS1 opsin sequences
consistent with ultraviolet sensitivity (S. M. Doucet, H. L. Mays, and G. E. Hill, unpubl.
data). We therefore used spectral sensitivity data from the blue tit, (Parus caeruleus) a
species with UVS cones (Hart et al. 2000; Hart 2001), to estimate photoreceptor quantum
catches in manakins. These data include the effects of colored oil droplets, and
photoreceptor sensitivities are calculated based on best?fitted pigment templates
(Govardovskii et al. 2000; Hart et al. 2000; Hart 2001).
For all manakin plumage patches, we calculated photoreceptor quantum catch (Q)
as a proportion of total quantum catch for each of the four types of avian photoreceptors
using the following equation:
Q
i
= ?
?
R
i
(?)S(?)I(?)O(?)d?                                                     (1)
                                                               ?
?
R
i
(?)d?
111
where ? represents wavelength, R
i
(?) is the spectral sensitivity of receptor type i, S(?) is
the reflectance of the color patch, I(?) is the irradiance of the light environment, and O(?)
is the transmission of the ocular media. Data for spectral sensitivities, irradiance, and
ocular transmission were normalized to one and all data spanned the range from 300 nm
to 700 nm. Using equation 1, we calculated receptor quantum catches for each single
cone type (UVS, SWS, MWS, LWS). Photoreceptors undergo chromatic adaptation to
pre?exposed or surrounding background stimuli, and we accounted for this by
normalizing the photoreceptor quantum catches of plumage patches to the photoreceptor
quantum catches of the adapting background using the von Kries scaling algorithm
(Wyszecki and Stiles 1982):
q
i
 = k
i
 Q
i               
                                                          (2)
where the scaling factor, k
i 
, is defined as:
k
i
 = 1/ ?
?
R
i
(?)S(?)I(?)O(?)d?                                                     (3)
?
?
R
i
(?)d?
where S(?) is the reflectance spectrum of the background. According to Fechner?s law,
the perceived magnitude of a visual stimulus is proportional to the physical magnitude of
that stimulus (Wyszecki and Stiles 1982). the receptor signal (f
i
) 
 
is therefore
proportional to the normalized receptor quantum catch (q
i
) and can be calculated as
follows:
f
i 
= ln(q
i
)                                                                 (4)
Using equation 4, we calculated receptor signals for each of the four avian cone
types. Color perception is achieved by comparing receptor signals across different
112
receptor types. Similarly, perceived differences in color between two objects can be
determined by comparing differences in receptor signals across different receptor types.
For each receptor type, the difference in receptor signals between two colored patches
will equal ?f
i
. For an avian tetrachromat, we can calculate the discriminability between
two colored patches using the following equation:
?S
2
 = (?
1
?
2
)
2
(?f
4
?? f
3
)
2
+(?
1
?
3
)
2
(?f
4
??f
2
)
2
+(?
1
?
4
)
2
(?f
3
??f
2
)
2
+
(?
2
?
3
)
 2
(?f
4
??f
1
)
2
+(?
2
?
4
)
2
(?f
3
??f
1
)
2
+(?
3
?
4
)
2
(?f
2
??f
1
)
2
/                       (5)
[(?
1
?
2
?
3
)
2
+(?
1
?
2
?
4
)
2
+(?
1
?
3
?
4
)
2
+(?
2
?
3
?
4
)
2
]
where ?S is the distance in tetrachromatic perceptual color space, ?f
i
 is the difference in
receptor signals at each of the four avian receptor types (UVS, SWS, MWS, LWS), and
?
i 
is the noise?to?signal ratio (Weber fraction). Under bright viewing conditions, the
Weber fraction can be modeled as follows:
?
i 
= ?
i
 /??
i         
                                                        (6)
where ? is the noise?to?signal ratio in a single photoreceptor of type i and ? is a scaling
factor that accounts for the relative number of photoreceptors of type i. We used data
from the red?billed leiothrix, Leiothrix lutea, (Maier 1992) to estimate noise?to?signal
ratios and data from the blue tit to estimate the relative abundance of receptor types (Hart
et al. 2000). ?S can be used to measure the distance in avian perceptual color space
between any two colors.
Quantifying chromatic contrast
Calculated values of ?S quantify differences in color and not differences in
brightness, so we refer to distances in perceptual color space (?S) as chromatic contrast.
113
We calculated two measures of chromatic contrast. The degree of contrast against the
background influences long?distance conspicuousness ? the greater the contrast, the more
perceptible the signal will be from a distance (Endler 1990; Endler and Th?ry 1996;
Heindl and Winkler 2003a). As a measure of long?distance conspicuousness, we
measured the distance in perceptual color space (?S) between manakin plumage patches
and different visual backgrounds (chromatic contrast against the background). The degree
of contrast between different body regions influences short?distance conspicuousness.
From a close distance, plumage patches that contrast against each other will be highly
conspicuous. Beyond a certain distance, however, individual elements within a color
pattern cannot be resolved and their spectral properties are summed together by the eye
(Endler 1978; Heindl and Winkler 2003a). As a measure of short?distance
conspicuousness, we calculated distances in perceptual color space (?S) between all
possible combinations of plumage patches for each individual (for a total of 10
combinations) and then averaged these to obtain a mean value of chromatic contrast
between body regions for each bird.
Quantifying achromatic contrast
Because variation in brightness also influences the conspicuousness of signals, we
calculated measures of brightness contrast (hereafter achromatic contrast) to correspond
to the measures of chromatic contrast described above. In birds, double cones are thought
to be used for achromatic signal detection (Cuthill et al. 2000; Hart 2001). We therefore
calculated receptor signals for double cones (f
D
) using the formulae described above and
spectral sensitivity data from blue tit double cones (Hart et al. 2000). We calculated f
D
114
directly from Q
D
. Receptor noise is not known for double cones, and we therefore
estimated the perceived brightness of a color patch as f
D
 and the perceived difference in
brightness between any two patches (achromatic contrast) as ?f
D
. Because there is only
one type of double cone, receptor noise would be the same for all comparisons and would
only affect absolute and not relative differences in receptor signals (Stuart?Fox et al.
2003); ?f
D 
should therefore serve as a good approximation of differences in perceived
brightness. High achromatic contrast can result from the reflection of more light than the
patch of comparison or less light than the patch of comparison, so we used absolute
values in our analyses. As described above for chromatic contrast, we measured
achromatic contrast against the background as a measure of long?distance
conspicuousness and achromatic contrast between body regions as a measure of
short?distance conspicuousness.
We used these models to compare plumage conspicuousness in three light
environments (forest shade, small gap, or cloudy) and against two visual backgrounds
(green leaves or brownish bark). We focused on these two visual backgrounds as they are
representative of the background from the perspective of an observer on the display perch
(male or female) or an observer located some distance away but at the same height in the
forest (potential predator). Moreover, the reflectance spectra of the brownish leaf litter,
display perches, and bark were all of similar shape (see below). The two backgrounds we
modeled should therefore provide a good approximation of conspicuousness for a variety
of viewing geometries.
115
Light environments and display perch location
To determine whether light environment influences display perch location in
long?tailed manakins, we compared light environments at primary display perches with
light environments at other locations in the forest understory. For each of 24 leks, we
used the methods described above (see Available light environments) to measure the
color of ambient light at each of four sites: (1) the primary display perch, (2) the
secondary display perch (when present), (3) a control vine that resembled the primary
display perch in physical characteristics but was not used as a display perch, and (4) a site
10m from the primary display perch in a pre?determined, arbitrary compass direction.
For the first three sites we collected irradiance readings at the height of the perch and at
the fourth site we collected readings from 65 cm above the ground (a height typical of
display perches). We purposely chose control perches that appeared to be of similar
dimensions to typical display perches, as we sought to determine whether differences in
light environment precluded their use as display perches. We noted the light environment
at the time the readings were taken and collected readings from multiple light
environments at each perch when possible. To control for time of day and seasonal
effects, we collected readings at each lek in a single measurement session and used
pairwise comparisons within leks in our analyses.
Perch characteristics
To determine whether long?tailed manakins might choose display locations based
on features other than light environment, we measured a number of physical
characteristics of primary display perches, secondary display perches, and control perches
116
(measurement sites 1?3 above) for a subset of leks (n = 18). We measured the height of
the perch, the length of the perch, the diameter of the perch, and the distance to the
nearest vegetation on both sides of the perch. We averaged these last two measurements
to obtain a mean value of distance to the nearest vegetation.
Light environments and timing of displays
We collected behavioral observations of male advertisement rate and display
activity at each of 12 leks. Observations were recorded from blinds or concealed
locations 8?10 m from primary display perches. Manakins did not display in rainy
weather, and we therefore terminated any ongoing observation at the first sign of rain.
Observation sessions ranged in duration from 55 to 300 minutes, and each lek was
observed for a total of 340 ? 42.9 minutes (mean ? SE). During observations, we
recorded all vocalizations and displays performed by male manakins in five?minute
blocks. For the purposes of this study, we focused on ?toledo? vocalizations, as these are
advertisement duets sung by dominant males to attract females to the lek (McDonald
1989b; Trainer and McDonald 1993). We separated instances of attendance at the display
perch into ?displays? (two dominant males performing behavioral displays in the
presence of one or more females), and ?practice dances? (one or several males, dominant
or subordinate, performing behavioral displays in the absence of females). Female
presence was either noted directly or, when females could not be seen due to obstructing
vegetation, implied by a combination of the utterance of ?owng? vocalizations (Trainer
and McDonald 1993) and the distinct sequence and rhythm of vocalizations and
behaviors that precede and accompany displays directed at females (McDonald 1989a;
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McDonald 1989b; Trainer and McDonald 1993). If the presence of a female could not be
implied by both of these criteria, or if displays took place entirely out of sight at
secondary or tertiary display perches, they were excluded from our analyses. We
recorded the light environment throughout observation bouts as sunny (forest shade) or
cloudy. For any displays performed in sunny conditions, we also noted whether a small
gap was illuminating part of the display perch. All observations were collected between
June 13 and July 11, in 2003 and 2004 (i.e., during the rainy season). Because we did not
encounter all weather conditions at all 12 leks, our sample size was too small to allow for
paired analyses. We therefore compared advertisement and display rates in different light
environments using mixed models that included lek ID as a random effect.
RESULTS
Plumage and background reflectance
The black breast and flight feathers of adult male long?tailed manakins exhibited
uniformly low reflectance across the bird?visible spectrum, from 300 to 700 nm (Fig.
1A). The reflectance of the blue mantle of males increased at short wavelengths, peaking
in the ultraviolet, and decreased at longer wavelengths (Fig. 1A). The red crown
coloration of males exhibited uniformly low reflectance at middle wavelengths, with a
subtle increase in reflectance at short wavelengths and a steep increase at long
wavelengths (Fig. 1A). In females, reflectance spectra for different body regions, all of
which were olive?green in color, were of similar shape, increasing at short wavelengths,
decreasing between 400 and 500 nm, and increasing to a plateau at longer wavelengths
(Fig. 1B).
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The green leaves of saplings surrounding manakin display perches exhibited a
peak in reflectance between 500 and 600 nm (Fig. 2A). The brownish leaf litter below the
perches, the bark of nearby trees, and the bark of display perches exhibited reflectance
spectra of similar shape, with reflectance increasing steadily with wavelength across the
bird?visible range (Fig. 2A, B).
We used principal components analysis (PCA) to summarize information from
reflectance spectra (e.g., Endler 1990; Cuthill et al. 1999; Heindl and Winkler 2003a;
Montgomerie 2006). We first reduced the number of variables represented by each
spectrum by calculating average reflectance values in 10 nm?sized bins from 300 to 700
nm, resulting in 40 reflectance values (variables) per spectrum. We included as
observations reflectance spectra from the five body regions of each manakin, as well as
all spectra collected from leaves, leaf litter, bark, and display perches. This PCA
produced three principal component variables with eigenvalues ? 1, together accounting
for more than 99% of the variation in reflectance. Component loadings for the first
principal component (reflectance PC1), which explained 77 % of the variation in
reflectance, were moderate and positive from 300 to 600 nm (Fig. 3). Component
loadings for the second principal component (reflectance PC2), which explained 19% of
the variation in reflectance, were high and positive from 600 nm to 700 nm (Fig. 3).
Component loadings for the third principal component, which explained 4% of the
variation in reflectance, were moderate and positive from 300 to 450 nm and from 650 to
700 nm, whereas they were high and negative from 500 to 625 nm (Fig. 3).
Reflectance PC scores differed significantly between males, females, and the
visual background (reflectance PC1: F = 32.4, df = 2, 168, P = 0.04; reflectance PC2: F =
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5.86, df = 2, 168, P = 0.003; reflectance PC3: F = 301.5, df = 2, 168, P <0.0001). Among
manakins, there were significant differences based on sex, body region, and the
interaction between sex and body region for reflectance PC1 scores (whole model: F =
769.2, df = 9, 599, P < 0.0001; sex: F = 44.0, df = 1, 607, P < 0.0001; body region: F =
802.9, df = 4, 604, P < 0.0001; sex*body region: F = 873.2, df = 4, 604, P < 0.0001),
reflectance PC2 scores (whole model: F = 1193.0, df = 9, 599, P <0.0001; sex: F = 34.2,
df = 1, 607, P < 0.0001; body region: F = 1047.2, df = 4, 604, P < 0.0001; sex*body
region: F = 1536.7, df = 4, 604, P < 0.0001) and reflectance  PC3 scores (whole model: F
= 432.1, df = 9, 599, P < 0.0001; sex: F = 3308.1, df = 1, 608, P < 0.0001 ; body region:
F = 61.4, df = 4, 604, P < 0.0001; sex*body region: F = 54.4, df = 4, 604, P < 0.0001).
These reflectance PC scores can be used to represent reflectance information in a
three?dimensional color space that is independent of the visual system (Endler 1990).
Male plumage patterns generally encompassed a larger portion of this color space than
female patterns and background elements (Fig. 4). In particular, the blue mantle and red
crown of males occupied unique areas of the color space, whereas female plumage
patterns overlap almost entirely with background elements (Fig. 4). Indeed, the 95%
density ellipses of female reflectance PC scores are completely encompassed within the
95% density ellipses of background elements (Fig. 4); that is, variation in female
plumage reflectance is a small subset of the variation in background reflectance. A
discriminant analysis based on these PC scores revealed significant differentiation of
males, females, and background elements (F = 203.9, df = 6, 1438, P < 0.0001).
However, whereas 99% of male values were correctly classified as male, 33% of female
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values were misclassified as background elements, and 49% of background elements
were misclassified as female.
Light environments
In the forest understory at our study site, there were three light environments
available for display: forest shade, small gaps, and cloudy (Endler 1993a). We measured
each of these light environments at long?tailed manakin primary display perches. Forest
shade light was greenish in color, as revealed by relatively high irradiance at middle
wavelengths and relatively low irradiance at short and long wavelengths (Fig. 5A). By
contrast, small gap light exhibited a nearly inverse pattern, with relatively high irradiance
at short and long wavelengths and relatively low irradiance at middle wavelengths (Fig.
5B). Cloudy light exhibited low irradiance at ultraviolet wavelengths and a more even
distribution in irradiance across the remainder of the spectrum (Fig. 5C).
Visual modeling
Effects of sex and body region
In all combinations of light environment (forest shade, small gap, or cloudy) and
visual background (leaves or bark), there were significant effects of sex, body region, and
the interaction between sex and body region on both chromatic (Fig. 6A,Table 1) and
achromatic (Fig. 6B, Table 2) contrast against the background, with males exhibiting
more contrast against the background than females in all cases. Similarly, there were
significant sex differences in chromatic contrast between body regions (Fig. 7A) and
achromatic contrast between body regions (Fig. 7B) in all three light environments (Table
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3), with males exhibiting more contrast between body regions in all cases. Thus, male
plumage coloration was more conspicuous than female plumage coloration from both
long and short distances.
Effects of light environment and the visual background
There was a significant influence of both the light environment and the visual
background on the degree of chromatic plumage contrast against the background in male
(Fig. 8A, Table 4) and female (Fig. 8B, Table 4) long?tailed manakins. Among males,
chromatic plumage contrast against the background was highest in small gaps,
intermediate in cloudy conditions, and lowest in forest shade, for both types of
background (Fig. 8A). A similar pattern was found in females (Fig. 8B). Despite the
significant influence of light environment, however, values of chromatic contrast against
the background were more strongly influenced by the visual background (Fig. 8, Table
5). Among males, chromatic plumage contrast against the background was highest when
the background was composed of bark (Fig. 8A), whereas among females, chromatic
plumage contrast against the background was highest when the background was
composed of leaves (Fig. 8B).
There was a significant influence of both light environment and the visual
background on achromatic plumage contrast against the background in both males (Fig.
9A, Table 4) and females (Fig. 9B, Table 4). Among males, achromatic plumage contrast
against the background was highest in cloudy conditions, intermediate in forest shade,
and lowest in small gaps, for both types of background. Moreover, achromatic plumage
contrast against the background was significantly higher when the background was
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composed of leaves than bark (Fig. 9A, Table 5). Among females, achromatic plumage
contrast against the background was highest in cloudy conditions, intermediate in forest
shade, and lowest in small gaps when the background was composed of leaves (Fig. 9B,
Table 4). However, when the background was composed of bark, achromatic plumage
contrast against the background was higher in small gaps than in forest shade or cloudy
conditions, and there were no significant differences in contrast against the background
between the latter two light environments (Fig. 9B, Table 4). When illuminated by forest
shade or cloudy conditions, females exhibited greater achromatic plumage contrast
against the background when the background was composed of leaves (Fig. 9B, Table 5).
By contrast, where illuminated by small gaps, females exhibited greater achromatic
plumage contrast against the background when that background was composed of bark
(Fig. 9B, Table 5).
The degree of chromatic and achromatic contrast between body regions is also
influenced by variation in the light environment in male and female long?tailed manakins
(Fig. 7A,B, Table 6). Among males, the degree of chromatic and achromatic contrast
between body regions was highest in small gaps, intermediate in forest shade, and lowest
in cloudy conditions (Fig. 7A,B).  Among females, the degree of chromatic and
achromatic contrast between body regions was highest in small gaps, intermediate in
cloudy conditions, and lowest in forest shade (Fig. 7A,B).
Display location and light environment
We compared irradiance readings collected at four locations for each of 24 leks:
the primary display perch, the secondary display perch, a nearby control perch, and a
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location 10 m from the primary display perch in an arbitrary compass direction. We used
PCA to summarize information from irradiance spectra into a few orthogonal variables as
described above for reflectance spectra. This PCA produced 3 principal components with
eigenvalues ? 1. Component loadings for the first principal component (irradiance PC1),
which explained 82% of the variation in irradiance, were moderate and positive from 300
to 700 nm (Fig. 10). Component loadings for the second principal component (irradiance
PC2), which explained 14% of the variation in irradiance, were high and positive 300 to
400 nm and moderate and negative from 500 to 600 nm (Fig. 10). Component loadings
from the third principal component (irradiance PC3), which explained 3% of the variation
in irradiance, were high and positive from 300 to 350 and from 500 to 600 nm and high
and negative from 350 to 400 nm (Fig. 10).
In paired analyses, there were no significant differences in irradiance PC scores
between readings collected in forest shade light environments at primary display perches
versus those collected at secondary perches, nearby control vines not used for display, or
at arbitrary locations 10 m from the primary perch (Table 7). Similarly, there were no
significant differences in irradiance PC scores between readings collected in small gap
light environments at primary display perches versus those collected at secondary
perches, nearby control vines not used for display, or at arbitrary locations 10 m from the
primary perch (Table 7). Our sample size was too small to allow for comparisons in
cloudy light environments.
We also compared the physical characteristics of primary perches, secondary
perches, and control vines. There were no significant differences in perch height (Fig.
12A; F = 0.09, df = 2, 46, P = 0.91). There were significances in perch length (Fig. 12B;
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F = 2.53, df = 2, 46, P = 0.04), although Tukey?Kramer tests did not reveal significant
differences between any particular pair of perches (P > 0.05). There were significant
differences in perch diameter among the three types of perch (Fig. 12C; F = 4.04, df = 2,
46, P = 0.02); primary and control perches were significantly thicker than secondary
perches (Tukey?Kramer tests, P < 0.05). Finally, there were significant differences in the
distance to the nearest vegetation (Fig. 12D; F = 4.91, df = 2, 46, P = 0.01); the nearest
vegetation was significantly farther away from primary display perches than from
secondary and control perches (Tukey?Kramer tests, P < 0.05).
Timing of display and light environment
We collected a total of 3307 minutes of observation in forest shade conditions and
775 minutes of observation in cloudy conditions. We did not continuously monitor the
presence or absence of small gaps on display perches, as these were relatively uncommon
and lasted only for a few seconds. However, we did note whether a small gap illuminated
part of the display perch during displays directed at females or practice dances. In total,
85% of displays directed at females were performed in forest shade, 12 % in cloudy
conditions, and 3% when the perch was partly illuminated by a small gap. By
comparison, 64% of practice dances were performed in forest shade, 34% in cloudy
conditions, and 2% when the perch was partly illuminated by a small gap. Birds made no
attempt to move into or avoid small gaps when they were present and simply displayed in
the usual manner. There was no significant difference in the rates of toledo calls given in
forest shade (2.15 ? 0.58 toledos/min) versus cloudy (1.64 ? 0.71 toledos/min) light
environments (whole model: F = 0.81, df = 12, 14, P = 0.63; light environment: F = 0.57,
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df = 1, 14, P = 0.46; lek: F = 0.85, df = 11,14, P = 0.60). There was no significant
difference in the rates of practice dances performed in forest shade (0.76 ? 1.05
practices/hour) versus cloudy (3.88 ? 1.30 practices/hour) light environments (whole
model: 1.14, df = 12, 14, P = 0.39; light environment: F = 4.92, df = 1, 14, P = 0.04; lek:
F = 0.85, df = 11, 14, P = 0.60). There was no significant difference in the rates of
displays directed at females in forest shade (0.48 ? 1.02 displays/hour) versus cloudy
(2.22 ? 1.27 displays/hour) light environments (whole model: F = 0.54, df = 12, 14, P =
0.85; light environment: F = 0.91, df = 1, 14, P = 0.23; lek: F = 0.90, df = 11, 14, P =
0.35).
DISCUSSION
In this study, we investigated the influence of the light environment and the visual
background on plumage conspicuousness in long?tailed manakins and determined what
influence, if any, these factors exerted on spatial and temporal patterns of display in this
species. Our first objective was to quantify the reflectance of plumage patches of male
and female manakins and to compare them with the reflectance of the leaves, bark,
display perches, and leaf litter constituting the visual background of manakin display
areas. The black wings, tail, and breast feathers of adult males exhibited low, uniform
reflectance across the bird?visible spectrum. By contrast, their sky?blue mantles and
bright red crowns exhibited prominent peaks at opposite ends of the spectrum in the
ultraviolet and red regions, respectively. The plumage patches of females exhibited
reflectance spectra typical of olive?green plumage, with a subtle peak in reflectance in
the UV and a low plateau at longer wavelengths (Dyck 1978; Doucet and Montgomerie
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2003b). The reflectance spectra of green leaves surrounding manakin display perches
peaked at middle wavelengths, as expected from the absorbance properties of chlorophyll
(Endler 1993a; Andersson et al. 1998). The reflectance spectra of the brownish leaf litter
beneath display perches, the bark of nearby trees, and the bark of the display perches
themselves all exhibited similar shapes, with steadily increasing reflectance from short to
long wavelengths (Endler 1993a).
We used principal components analysis (PCA) to summarize reflectance data and
construct a visual color space that is independent of variation in the visual system. There
were significant differences between reflectance PC scores of male and female manakins
and those of background elements. Among manakins, reflectance was strongly influenced
by sex, body region, and the interaction between sex and body region. Male plumage
colors generally occupied larger portions of the PCA color space than female plumage
colors or background elements. Indeed, the red crown and blue mantle males were unique
colors in the signaling environment of manakins. By contrast, female plumage patterns
occupied a small subset of the color space defined by the visual environment of
manakins, overlapping with the coloration of green leaves, brownish leaf litter, and bark.
Moreover, a discriminant function analysis based on reflectance PC scores correctly
classified 99% of male plumage patches, but misclassified 33% of female reflectance
scores as background elements and 49% of background elements as female plumage
patches.
Our second objective was to document the different light environments available
at manakin display sites. Long?tailed manakins performed their displays at fixed
locations on display perches in the understory of evergreen forest. Light environments in
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forests vary as a function of forest geometry (closed versus open canopy, small versus
large canopy gaps), weather conditions (sunny versus cloudy), and time of day
(crepuscular versus daylight) (Endler 1993a). Long?tailed manakin display perches were
not associated with canopy gaps or forest edges, and males displayed for females after
sunrise, precluding the use of crepuscular light environments (cf. Endler and Th?ry 1996;
Doucet and Montgomerie 2003a).
During the first half of the breeding season, which coincides with the dry season,
sunny conditions prevail and only two light environments are available to displaying
manakins: forest shade and small gaps (Endler 1993a). Under such sunny conditions,
forest shade light predominates in the shady understory of closed?canopy forests. Forest
shade irradiance spectra were rich in middle wavelengths and were greenish in color, as
expected since much of the radiant light is reflected from the surrounding vegetation
(Endler 1993a; Endler and Th?ry 1996; Heindl and Winkler 2003a). Forest shade light
environments are usually interspersed with small gaps (or sun flecks), where the sun
penetrates directly to the understory through small interruptions in the canopy. Small gap
light environments are typically dynamic and unpredictable (Heindl and Winkler 2003a).
At our study site, any particular small gap usually lasted for very brief periods only,
especially during the dry season, when strong winds persistently moved the leaves in the
forest canopy. Small gap light environments are usually reddish in color because much of
the light comes directly from the sun (Endler 1993a; Endler and Th?ry 1996; Heindl and
Winkler 2003a), whereas our small gap measurements exhibited two irradiance maxima,
one at short UV/blue wavelengths, and a second at long reddish wavelengths. This
difference may have resulted from our measurement geometry. All of our irradiance
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readings were collected with the probe oriented directly skyward. However, in the
morning, when we collected our measurements, the sunlight of small gaps penetrated the
forest obliquely and the solar disk was usually partially obstructed by vegetation, with the
combined effect of a reduction in the relative contribution of direct sunlight and an
increase the relative contributions of blue sky and vegetation to the total irradiance
(Endler 1993a). Since the direct sunlight and blue sky are much brighter than the
vegetation (Endler 1993a), such conditions could produce a light environment rich in
blue and red wavelengths and poor in green wavelengths.
 In the latter part of the breeding season, which coincides with the rainy season,
intermittent sunny, cloudy, and rainy conditions make a third light environment available
for display: cloudy (Endler 1993a). As in other studies, irradiance measurements
collected in cloudy conditions were relatively poor in UV light and otherwise whitish in
appearance, as revealed by a generally even distribution of light across the remainder
spectrum and as expected from the light?scattering properties of clouds (Endler 1993a;
Endler and Th?ry 1996; Heindl and Winkler 2003a).
We integrated these data on plumage reflectance, background reflectance, and
light environments into an avian perceptual color space model to examine the influence
of the visual environment on the conspicuousness of long?tailed manakin plumage
patterns. We examined the influence of two different backgrounds (green leaves and
brownish bark) and three different light environments (forest shade, small gap, and
cloudy). We found striking sex differences conspicuousness. In all combinations of light
environment and visual background, males exhibited higher chromatic and achromatic
contrast against the background than did females for all body regions. In terms of
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chromatic contrast, this effect was more pronounced for the red crown and blue mantle,
and in terms of achromatic contrast, this effect was more pronounced for the black breast,
wings, and tail, suggesting that these different body regions emphasize different types of
conspicuousness. Males also exhibited more chromatic and achromatic contrast between
body regions than did females.
Three lines of evidence suggest that female long?tailed manakins are remarkably
cryptic. First, female coloration is a subset of the colors constituting the visual
background in the forest understory habitat of manakins. Second, based on our avian
perceptual model, females exhibit low degrees of contrast against the background, a
measure of long?distance conspicuousness. Third, females exhibit low degrees of
contrast between body regions, a measure of short?distance conspicuousness. By these
same arguments, males are relatively conspicuous, as they display unique colors not
found elsewhere in their habitat, exhibit high degrees of contrast against the background,
and even higher degrees of contrast between body regions. Together with recent studies
that have documented similar patterns in other manakins (Endler and Th?ry 1996; Uy and
Endler 2004; Doucet et al. 2006b), our findings highlight the opposing selection pressures
on males and females. Sexual selection is thought to act particularly strongly on males in
lek?mating manakins (McDonald 1993; Prum 1997; Snow 2004) and has probably
played a critical role in the evolution of conspicuous male ornaments. By contrast, natural
selection has likely favored the evolution and maintenance of cryptic coloration in
females, even in the face of opposing pressure from genetic correlations between the
sexes (Lande 1987). Selection for cryptic coloration may be particularly important in
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female manakins as they are solely responsible for rearing offspring (Snow 2004) and
may be particularly vulnerable during incubation and nestling care.
Our findings highlight the importance of considering the different selective
pressures that act on males and females when trying to understand observed patterns of
sexual dichromatism (Badyaev and Hill 2003). In many cases, sexual dichromatism is a
consequence of selection on male coloration to diverge from the background (i.e.,
selection for conspicuousness) and selection on female coloration to match the
background (i.e., selection for crypsis) rather than a consequence of selection on male
coloration to diverge from female coloration. Our findings suggest that caution is
warranted in the use of sexual dichromatism as an index of the intensity of sexual
selection; in species where both males and females experience selection pressures for
plumage coloration that contrasts against the background, the degree of sexual
dichromatism will likely underestimate the intensity of social selection on either sex
(Amundsen 2000; Amundsen 2002).
We found significant influences of both light environment and background
coloration on the conspicuousness of male and female plumage patterns. Regardless of
variation in light environment, males exhibited more chromatic contrast against the
background when the background was composed of bark and more achromatic contrast
against the background when the background was composed of leaves. Females exhibited
more achromatic and chromatic contrast against the background when the background
was composed of leaves. Females would therefore be more cryptic against a background
composed mostly of bark, whereas males would be relatively conspicuous against either
background, one background emphasizing achromatic (brightness) contrast, and the other
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emphasizing chromatic (color) contrast. It is worth noting that background coloration had
a larger influence on conspicuousness than light environment. This makes intuitive sense
because in most situations, a change in light environment will influence the coloration of
the target individual and of the visual background in similar ways. To date, however,
research has emphasized variation in light environments whereas background coloration
has often been overlooked. Our findings argue that the visual background should be given
equal consideration in studies of visual conspicuousness.
The conspicuousness of plumage features varied significantly across the three
primary light environments. Male chromatic plumage contrast against the background
was highest in small gaps, intermediate in cloudy conditions, and lowest in forest shade
whereas achromatic plumage contrast against the background was highest in cloudy
conditions, intermediate in forest shade, and lowest in small gaps. Additionally, among
males, chromatic and achromatic contrast between plumage regions was highest in small
gaps, intermediate in forest shade, and lowest in cloudy conditions. Among females,
chromatic and achromatic contrast against the background and chromatic and achromatic
contrast between body regions were highest in small gaps, intermediate in cloudy
conditions, and lowest in forest shade. Thus, in terms of long?distance conspicuousness,
both males and females were generally most conspicuous in small gaps. In terms of
short?distance conspicuousness, males were most conspicuous in small gaps and least
conspicuous in cloudy conditions whereas females were most conspicuous in small gaps
and least conspicuous in forest shade. If male conspicuousness is the primary selective
target and the timing and location of displays are relatively unconstrained, males should
preferentially display in small gaps. However, both males and females are exposed to the
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same light environments on display perches, and long?tailed manakins may experience
selective pressure to simultaneously minimize female conspicuousness.
Given the substantial influence of light environment on plumage conspicuousness,
we wondered whether light environment might influence the location of display perches.
In paired comparisons, light conditions at primary display perches did not differ from
light conditions at secondary display perches, nearby control vines not used for display,
or an arbitrary location 10 m from the primary display perch in either forest shade or
small gap light environments. That is, light environments at manakin display perches
were no different than light environments in other parts of the forest understory, implying
that long?tailed manakins did not choose display perch locations on the basis of variation
in the light environment. However, a number of other factors may influence the initial
choice of display perch location. First, display perch location is almost certainly
influenced by large?scale factors such as proximity to foraging areas and distance from
other established leks (McDonald 1989b; Th?ry 1992). Second, perches must be located
in areas that allow males to perform butterfly display flights, and must therefore be
relatively unobstructed by vegetation. Indeed, although our control sites (nearby vines not
used for display) resembled primary display perches in physical characteristics,
potentially obstructing vegetation was located significantly farther away from primary
perches than from control perches. The fact that males purposely remove obstructing
leaves (D. B. McDonald, unpubl. data), as has been shown in other species (Snow 1963;
Endler and Th?ry 1996), anecdotally supports this hypothesis. Third, once selected,
display perches are commonly used for up to 10 years and, in some cases, much longer
(D. B. McDonald, unpubl. data). Although such extended use of display perches likely
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facilitates long?term lek fidelity by females (McDonald and Potts 1994), it is probably
longer than most non?random subsets of forest light environments, for example large
canopy gaps, are expected to last. Finally, the location of display perches in non?random
subsets of the light environment would make the entire display area more conspicuous to
predators at a time when both males and females are likely to be less vigilant, their
attention focused on performing or observing displays (Trail 1987).
Finally, we investigated whether variation in light environment influences the
timing of display in long?tailed manakins. In the first half of the breeding season, both
forest shade and small gap environments were available for display and in the latter part
of the breeding season cloudy light environments became available as well. In
comparisons of cloudy versus forest shade light environments, there were no significant
differences in the rates of advertisement duets sung by males, the rates displays
performed for females by dominant males, or the rates practice dances performed by
males. Small gaps were ephemeral in nature, lasting for very brief periods only, often
only a few seconds at a time. Even when a small gap was illuminating part of the display
perch, males did not appear to move into or avoid these gaps. Indeed, the dynamic nature
of the dual?male cooperative display ? where each male must coordinate leapfrog and
butterfly displays with his partner and maneuver around one or more females on the
display perch ? may preclude males from altering their display behavior in relation to
small gaps. Thus, long?tailed manakins do not appear to adjust the timing of their
displays to take advantage of particular subsets of the light environment. Instead, our data
suggest that long?tailed manakins perform their displays in proportion to the availability
of different light environments: 85% of displays were performed in forest shade, 12% in
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cloudy conditions, and 3% in small gaps. Had we performed behavioral during the dry
season, displays would surely be even more skewed toward forest shade light conditions.
The perceptual environment can influence visual signals in animals in two ways.
First, the visual environment can dictate what sort of coloration should evolve for an
individual to achieve either crypsis or conspicuousness. Alternatively, behaviors can
evolve that allow animals to adjust the timing or location of their displays to take
advantage of particular light environments. While the latter does not appear to apply in
long?tailed manakins, the former may still hold true. According to our visual models,
displays in forest shade may offer a partial resolution to the conflict of selection for
conspicuous male coloration and cryptic female coloration. In forest shade, female
conspicuousness is minimized at both short and long distances and male conspicuousness
is intermediate at short distances and intermediate or least conspicuous at long distances.
In comparison with forest shade, small gaps increase the long? and short?distance
conspicuousness of both males and females, and cloudy light environments increase the
conspicuousness of females while reducing that of males. Displays in forest shade
thereby allow males to optimize their short?distance conspicuousness while minimizing
their long?distance conspicuousness and the overall conspicuousness of females (Endler
and Th?ry 1996; Heindl and Winkler 2003a). In addition, among males, contrast between
body regions is greater than contrast against the background in all combinations of light
environment and backgrounds, lending support to the idea that short?distance
conspicuousness is favored over long?distance conspicuousness. While these
interpretations remain speculative, a recent comparative analysis across the Pipridae
revealed that in forest shade light environments and against a green vegetation
135
background, male plumage patterns are relatively conspicuous whereas female plumage
patterns are relatively cryptic, suggesting that the visual environment has had a general
influence on the evolution of coloration patterns in these birds (Doucet et al. 2006b).
Several species of lek?mating birds, including many manakins, have been shown
to display in non?random subsets of the light environment that enhance the
conspicuousness of their color patterns (Endler and Th?ry 1996; Heindl and Winkler
2003b; Heindl and Winkler 2003a; Uy and Endler 2004). Interestingly, long?tailed
manakins differ from all other species investigated in two respects. First, long?tailed
manakins, along with other Chiroxiphia manakins (Snow 1963; Foster 1981), are the only
species that perform obligate cooperative displays (Snow 2004). As described above,
these affiliations may impose constraints on the timing and location of displays in both
the short term (coordination on the display perch) and long term (female lek fidelity).
Second, the distribution of long?tailed manakins does not overlap with any other
manakin, whereas other species investigated are sympatric with multiple other manakins
(Th?ry 1992; Endler and Th?ry 1996; Heindl and Winkler 2003b; Heindl and Winkler
2003a). Because most manakins follow a lek?based mating system (Snow 2004), there
may be some selective pressure for manakins to minimize potential interference from
other species by modifying the timing or location of their displays. Red?capped manakins
(Pipra mentalis), for example, are known to display at greater heights in the forest where
they overlap with blue?crowned manakins (Lepidothrix coronata), a species that displays
in the understory (Stiles and Skutch 1989). Selective pressure to minimize physical,
vocal, or visual interference from other species may therefore drive the spatial and/or
temporal segregation of displays among sympatric manakins species. Of course, any
136
change in the time of day, time of year, or location of manakin displays would likely also
result in a change of light environment (Endler 1993a; Heindl and Winkler 2003b). Thus,
selective pressure for the temporal and/or spatial segregation of displays may have been
sufficient to initiate microhabitat display preferences in sympatric species of manakins, or
may have acted as a reinforcing mechanism, strengthening pre?existing preferences for
light environments that optimized plumage conspicuousness. A comparative analysis of
coloration patterns and light environments used for display in sympatric versus allopatric
manakins would provide a compelling test of these hypotheses.
In conclusion, our study reveals an important influence of the light environment
and visual background on the conspicuousness of male plumage coloration and the
crypsis of female plumage coloration in long?tailed manakins. Our findings contribute to
a growing body of evidence suggesting that the visual environment has and an important
influence on the evolution and diversity of coloration patterns found in animals.
ACKNOWLEDGEMENTS
We thank to A. Lindo, L. Baril, and V. Connolly for field assistance and R. Blanco and
the Area de Conservac?on Guanacaste for logistical support in Costa Rica. We thank D.
B. McDonald and M. S. Foster for generously providing advice and information and D. J.
Mennill, H. Fadamiro, C. Guyer, and F. S. Dobson for comments on this manuscript. We
thank J. Hadfield and D. Osorio for advice, R. Montgomerie for access to his spectral
analysis programs, and D. Osorio and N. Hart for providing cone spectral sensitivity data.
Funding was provided by a Collections Study Grant and the Frank M. Chapman
Memorial Fund from the American Museum of Natural History, a Wetmore Research
137
Award from the American Ornithologists? Union, a Sigma?Xi Grant?in?Aid of Research,
the Exploration Fund of the Explorer?s Club, the Louis Agassiz Fuertes Research Award
from the Wilson Ornithological Society, Auburn University Graduate Research Awards,
and a Natural Sciences and Engineering Research Council of Canada (NSERC)
scholarship to SMD, as well as NSF grant IBN0235778 to GEH.
138
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Table 1. The influence of sex, body region, and sex by body interactions on chromatic
(color) plumage contrast against the background in long?tailed manakins for two
different backgrounds (leaves and bark) and three different light environments (forest
shade, small gap, and cloudy).
Leaves BackgroundBark Background
F df P F df P
Forest shade
Whole model1623.89, 599<0.00011230.19,599<0.0001
Sex 2003.31, 507<0.00013366.81, 507<0.0001
Body region1657.34, 504<0.0001906.734, 504<0.0001
Sex* Body region1391.04, 504<0.0001954.074, 504<0.0001
Small gap
Whole model1633.19, 599<0.00011228.69, 599<0.0001
Sex 1952.71, 507<0.00013396.11, 507<0.0001
Body region1684.44, 504<0.0001900.954, 504<0.0001
Sex* Body region1396.54, 504<0.0001949.554, 504<0.0001
Cloudy
Whole model1604.39, 599<0.00011213.59, 599<0.0001
Sex 1986.21, 507<0.00013331.11, 507<0.0001
Body region1640.14, 504<0.0001894.844, 504<0.0001
Sex* Body region1370.14, 504<0.0001938.464, 504<0.0001
147
Table 2. The influence of sex, body region, and sex by body interactions on achromatic
(brightness) plumage contrast against the background in long?tailed manakins for two
different backgrounds (leaves and bark) and three different light environments (forest
shade, small gap, and cloudy).
Leaves BackgroundBark Background
F df P F df P
Forest shade
Whole model328.19, 599<0.0001319.59,599<0.0001
Sex 2192.61, 507<0.00012168.71, 507<0.0001
Body region77.554, 504<0.000168.684, 504<0.0001
Sex* Body region109.34, 504<0.0001105.44, 504<0.0001
Small gap
Whole model332.29, 599<0.0001333.59, 599<0.0001
Sex 1883.51, 507<0.00011888.41, 507<0.0001
Body region96.884, 504<0.000197.754, 504<0.0001
Sex* Body region174.244, 504<0.0001174.94, 504<0.0001
Cloudy
Whole model321.29, 599<0.0001309.39, 599<0.0001
Sex 2285.61, 507<0.00012252.61, 507<0.0001
Body region67.54, 504<0.000153.214, 504<0.0001
Sex* Body region81.874, 504<0.000178.434, 504<0.0001
148
Table 3. Sex difference in chromatic and achromatic contrast between body regions in
long?tailed manakins for three different light environments (forest shade, small gap, and
cloudy).
F df P
Chromatic
Forest shade2906.21, 119<0.0001
Small gap2953.61, 119<0.0001
Cloudy3012.61, 119<0.0001
Achromatic
Forest shade784.61, 119<0.0001
Small gap867.91, 119<0.0001
Cloudy743.11, 119<0.0001
149
Table 4. Paired comparisons of chromatic and achromatic plumage contrast against the
background for long?tailed manakins in different light environments. Data were analyzed
separately within each sex and against each type of background.
Forest shade vs. small gapForest shade vs. cloudyCloudy vs. small gap
t n P t n P t nP
Chromatic
Females
Leaves?33.159<0.0001?21.059<0.0001?33.659<0.0001
Bark?89.359<0.0001?89.459<0.0001?70.559<0.0001
Males
Leaves?27.162<0.0001?18.562<0.0001?23.562<0.0001
Bark?58.462<0.0001?33.562<0.0001?39.962<0.0001
Achromatic
Females
Leaves6.7459<0.0001?14.3259<0.00019.1159<0.0001
Bark?7.3859<0.0001?1.3159  0.20?4.4859<0.0001
Males
Leaves44.662<0.0001?37.162<0.000142.862<0.0001
Bark35.762<0.0001?27.0362<0.000133.562<0.0001
150
Table 5. Paired comparisons of chromatic and achromatic plumage contrast against the
background for long?tailed manakins in viewed against different backgrounds. Data were
analyzed separately within each sex and light environment.
Leaves vs. bark
t n P
Chromatic
Females
Forest shade7.83 59 <0.0001
Small gap6.72 59 <0.0001
Cloudy7.33 59 <0.0001
Males
Forest shade?28.762 <0.0001
Small gap?34.3762 <0.0001
Cloudy?31.162 <0.0001
Achromatic
Females
Forest shade7.46 59 <0.0001
Small gap?8.1059 <0.0001
Cloudy7.70 59 <0.0001
Males
Forest shade92.0 62 <0.0001
Small gap?92.062 <0.0001
Cloudy92.0 62 <0.0001
151
Table 6. Paired comparisons of chromatic and achromatic plumage contrast between
body regions for long?tailed manakins in different light environments. Data were
analyzed separately within each sex.
Forest shade vs. small gapForest shade vs. cloudyCloudy vs. small gap
t n P t n P t nP
Chromatic
Females?20.859 <0.000124.559<0.0001?13.859<0.0001
Males?6.162 <0.00013.9462  0.0002?31.462<0.0001
Achromatic
Females?13.959 <0.0001?16.359  0.207.2959<0.0001
Males?21.562 <0.000110.662<0.0001?18.562<0.0001
152
Table 7. Paired comparisons of irradiance PC scores at primary display perches of
long?tailed manakins versus secondary display perches, nearby control perches not used
for display, and an arbitrary location 10 m from the primary display perch. Data were
analyzed separately within light environment and PC score.
Forest shadeSmall gap
t n P t n P
Irradiance PC1
primary vs. secondary0.1115 0.910.73110.48
primary vs. control0.4824 0.63?1.15140.27
primary vs. arbitrary2.0524 0.060.33140.74
Irradiance PC2
primary vs. secondary?0.5515 0.59?0.44110.67
primary vs. control?0.4524 0.66?0.48140.64
primary vs. arbitrary?0.2124 0.84?0.27140.79
Irradiance PC3
primary vs. secondary0.6915 0.50?0.53110.61
primary vs. control?0.2924 0.77?0.71140.49
primary vs. arbitrary?0.5324 0.60?0.82140.42
153
FIGURE CAPTIONS
Figure 1. Mean reflectance spectra of the mantle and crown (A) and of the breast, tail,
and wings (B), of adult male long?tailed manakins (n = 62). Mean reflectance spectra of
the mantle and crown (C) and of the breast, tail, and wings (D) of female (n = 59)
long?tailed manakins. Vertical bars indicate standard errors. Note differences in scale of
y?axes.
Figure 2.  (A) Mean reflectance spectra of the green leaves (n = 56) of saplings
surrounding long?tailed manakin display perches and of the leaf litter (n = 28) beneath
manakin display perches. (B) Mean reflectance spectra of primary display perches (n =
14) and the bark of trees near primary display perches (n = 18). Vertical bars indicate
standard errors.
Figure 3. Component loadings for the first three principal components (PC1, PC2, and
PC3) of a principal components analysis (PCA) of reflectance spectra from plumage
patches of male and female long?tailed manakins (Fig. 1) and of the bark and leaves
constituting the visual background of long?tailed manakin display sites (Fig.2).
Figure 4. Scatterplots of reflectance PC scores representing the color space of male
(blue) and female (red) manakin plumage coloration and components of the visual
background (green). The different body regions of manakins are represented by solid
circles (crown), open circles (mantle), solid triangles (tail), solid diamonds (wing), and
solid squares (breast). The different components of the visual background are represented
154
by solid squares (bark), solid circles (leaves), open circles (leaf litter), and solid triangles
(display perches).
Figure 5. Mean irradiance spectra of (A) forest shade (n = 24), (B) small gaps (n = 15),
and (C) cloudy (n = 3) light environments collected at primary display perches of
long?tailed manakins. Vertical bars indicate standard errors.
Figure 6. Long?distance conspicuousness as measured by chromatic contrast against the
background (A) and achromatic contrast against the background (B) for different body
regions of male (solid bars; n = 62) and female (open bars; n = 59) long?tailed manakins
in a forest shade light environment and against a background of green leaves. Standard
errors are shown.
Figure 7. Short?distance conspicuousness as measured by chromatic contrast between
body regions (A) and achromatic contrast between body regions (B) for male (solid bars;
n = 62) and female (open bars; n = 59) long?tailed manakins in three different light
environments. Standard errors are shown.
Figure 8. Mean chromatic contrast against the background for male (A; n = 62) and
female (B; n = 59) long?tailed manakins for a background composed of green leaves
(shaded bars) or brownish bark (diagonally striped bars) in three different light
environments. Standard errors are shown.
155
Figure 9. Mean achromatic contrast against the background for male (A; n = 62) and
female (B; n = 59) long?tailed manakins for a background composed of green leaves
(shaded bars) or brownish bark (diagonally striped bars) in three different light
environments. Standard errors are shown.
Figure 10. Component loadings for the first three principal components (PC1, PC2, and
PC3) of a principal components analysis (PCA) of irradiance spectra from three different
light environments (Fig. 3) measured at primary display perches of long?tailed manakins.
Figure 11. Irradiance PC scores from spectra collected in forest shade (A) and small gap
(B) light environments at primary (solid bars), secondary (open bars), control (diagonally
striped bars), and arbitrary (shaded bars) display perches of long?tailed manakins (see
text for explanation of perch types). Standard errors are shown.
Figure 12. Comparison of physical characteristics of primary, secondary, and control
perches of long?tailed manakins (see text for explanation of perch types).
156
Figure 1
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Figure 2
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Figure 3
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Figure 4
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Figure 5
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Figure 6
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Figure 7
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Figure 10
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167
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168
CHAPTER 4. CAROTENOID, MELANIN, AND STRUCTURAL PLUMAGE
COLOR OF AVIAN STUDY SKINS: EFFECTS OF SPECIMEN AGE AND
GEOGRAPHIC VARIATION
169
ABSTRACT
Museum specimens are an invaluable resource for taxonomic, systematic, and
comparative studies and are increasingly being relied upon for novel research purposes.
Researchers now routinely quantify the color of feathers on study skins to address a broad
range of research questions, but few studies have investigated how well the plumage
coloration of museum specimens reflects the coloration of wild birds. In this study, we
used reflectance spectrometry to compare the reflectance of feathers on museum skins
and the feathers of wild birds and to investigate the effects of specimen age on plumage
coloration. We use the long?tailed manakin, Chiroxiphia linearis, as a model system for
investigating these potential differences in color. Long?tailed manakins are ideal for this
type of study because their colorful plumage patches result from the three primary
plumage coloration mechanisms found in birds: melanin pigmentation, carotenoid
pigmentation, and structural coloration. These features of long?tailed manakin plumage
allowed us to independently assess variation in each plumage coloration mechanism.
Reflectance spectra obtained from museum specimens were generally similar to those
obtained from wild birds. Nonetheless, we found significant differences in coloration
between museum skins and wild birds for all three mechanisms of plumage coloration.
We identified three key sources of variation: 1) overall differences between museum
specimens and wild birds, 2) geographic variation in color, and 3) variation in color
according to specimen age. Changes in color were not evenly distributed across the
reflectance spectrum but rather varied according to which color production mechanism
was involved. We discuss the potential proximate causes of these changes in color, many
of which apply to both museum specimens and wild birds, and identify the types of
170
studies are likely to be most sensitive to these changes. Our study therefore also provides
the first extensive review of potential sources of color wear and fading in avian museum
skins and wild birds.
171
INTRODUCTION
Studies based on museum specimens represent a large portion of the foundation of our
understanding of the diversity of life on earth (Winker 2004). Museum specimens
continue to be an invaluable resource for taxonomic, systematic, and comparative studies
and are increasingly being used for previously unanticipated purposes (Winker 2004).
Many contemporary studies use data from museum specimens as windows into the past,
for example, to document the spread of infectious disease (e.g., Yates et al. 2002), to
investigate the effects of nuclear disasters (Ellegren et al. 1997) or habitat degradation
(Lens et al. 2002) on populations, and to assess ecosystem?level changes in the
environment (Schell 2000). With museum specimens being put to such diverse and
important uses, it seems reasonable to ask whether specimens are an accurate
representation of wild animals. Clearly, for certain stable features such as skeletal size
and genetic or isotopic signature, the answer is ?yes?. However, some features, such as
the coloration of bare parts, fur, or feathers of museum study skins, might be expected to
change over time (Test 1940; Gabrielson and Lincoln 1951).
Evaluating variation in the color of feathers on avian museum skins forms the
basis for a broad range of research questions. The color and pattern of plumage preserved
on study skins can be used as a taxonomic marker (e.g., Brumfield and Remsen 1996;
Prum 1997; Johnson et al. 1998; Brumfield and Braun 2001; Patten and Unitt 2002), to
sex or age birds (e.g., Wood 1992; Jeffrey et al. 1993; Doucet et al. In review), or to
document plumage reflectance patterns of a particular species or group of species (e.g.,
Brumfield et al. 2001). Moreover, color itself is often the primary target of
museum?based studies. Researchers have measured the color of feathers on study skins,
172
for example, to reveal unusual reflectance patterns (Finger and Burkhardt 1994; McGraw
2004), to document historical changes in color (Hudon and Brush 1989), to examine
plumage reflectance and sexual dichromatism from the visual perspective of an avian
receiver (Mahler and Kempenaers 2002; Eaton and Lanyon 2003), or to test broad?scale
predictions about the evolution of particular types of color signals (Endler and Th?ry
1996; Owens and Hartley 1998; Hausmann et al. 2003; Heindl and Winkler 2003; Gomez
and Th?ry 2004). These studies highlight the importance of ascertaining that the plumage
colors of study skins are representative of the coloration of wild birds.
Until recently, studies of plumage coloration involving study skins or wild birds
relied on human visual assessments of color. It has become increasingly clear, however,
that the avian visual system differs substantially from that of humans (Cuthill et al. 2000;
Hart 2001; Cuthill 2006). Most notably, in addition to cone photoreceptors analogous to
the red, blue, and green cone photoreceptors of humans, birds have a fourth,
short?wavelength sensitive cone photoreceptor that, combined with ocular media that
allow the transmission of ultraviolet wavelengths, confers birds with the ability to see
ultraviolet wavelengths (Cuthill et al. 2000; Hart 2001; Cuthill 2006). Moreover, cone
photoreceptors in birds are associated with oil droplets that narrow their spectral
sensitivities and thereby increase wavelength discrimination (Cuthill et al. 2000; Hart
2001; Cuthill 2006). Birds also have double cone photoreceptors that are thought to
facilitate the discrimination of achromatic contrast (Cuthill et al. 2000; Hart 2001; Cuthill
2006). These fundamental differences between human and avian vision have led to the
development of improved methods for quantifying plumage coloration, such as
full?spectrum reflectance spectrometry (Bennett et al. 1994; Cuthill et al. 1999).
173
Our goal in this study was to determine how well the plumage coloration of
museum skins represents the plumage coloration of wild birds. There have been a number
of anecdotal observations of dulling, fading, and foxing of museum specimens in the
literature (Gabrielson and Lincoln 1951; Endler and Th?ry 1996; Mahler and
Kempenaers 2002; Eaton and Lanyon 2003; Hausmann et al. 2003; Jouventin et al.
2005). Until recently, however, there had been no systematic attempt to compare the
coloration of feathers on museum skins and on wild birds (McNett and Marchetti 2005).
Moreover, potential sources of variation in plumage color between study skins and wild
birds have never been comprehensively reviewed. Here, we use full?spectrum reflectance
spectrometry to compare the plumage reflectance of wild?caught long?tailed manakins
Chiroxiphia linearis, with museum skins of this species.
Long?tailed manakins are ideal for this type of investigation, as their colorful
plumage patches are produced by the three primary coloration mechanisms found in
birds: carotenoid pigmentation, melanin pigmentation, and structural coloration.
Definitive?plumaged adult males have bright red carotenoid?based crown patches,
structural sky?blue mantles, and melanin?based black body plumage and flight feathers
(Doucet et al. 2006). These features of manakin plumage ornamentation allowed us to
independently assess the potential effects of wear or fading of plumage colors resulting
from each of these mechanisms. Because our sample of study skins included individuals
from throughout the range of long?tailed manakins, we also assessed the potentially
confounding effect of geographic variation in ornamentation.
174
METHODS
Study system
Long?tailed manakins are distributed along the Pacific coast of North and Central
America from southeastern Mexico to northwestern Costa Rica (Fig. 1). The sexes are
strongly sexually dichromatic and adult males are adorned with a remarkable array of
elaborate sexual ornaments. While female plumage is dull olive?green, adult males are
ornamented with a scarlet crown patch, a sky?blue mantle, velvety black body plumage,
bright orange legs, and elongated central tail plumes. Males progress through a series of
age?specific predefinitive plumages before attaining their definitive adult plumage in
their fifth year (Doucet et al. In review).
We used biochemical and microscopic techniques to confirm the mechanisms of
color production in feathers collected from male long?tailed manakins in definitive adult
plumage. Most red plumage in passerines birds results from the deposition of carotenoids
into growing feathers (McGraw 2006a). To confirm that this mechanism was also
responsible for the red crown coloration of adult male long?tailed manakins, we used a
thermochemical extraction procedure and high performance liquid chromatography to
identify specific carotenoids in the red crowns of adult males (S. M. Doucet and K. J.
McGraw, unpubl. data, McGraw et al. 2004a; McGraw et al. 2005). Most black plumage
in birds results from the deposition of melanin pigments into growing feathers (McGraw
2006b). To confirm that this mechanism was also responsible for the black coloration of
body and flight feathers in adult male long?tailed manakins, we compared the reflectance
spectra of black body regions in long?tailed manakins to known melanin?based spectra
(Mennill et al. 2003; McGraw 2006b) and confirmed the presence of pigment granules of
175
the appropriate shape, size, and density in transmission electron micrographs (S. M.
Doucet, unpubl. data, Doucet et al. 2004). All non?iridescent blue plumage colors in
birds investigated to date result from the constructive interference of light scattered by
materials of different refractive indices (air and keratin) within the medullary keratin
matrix of feather barbs (Prum 2006). To confirm that this mechanism was also
responsible for blue coloration in long?tailed manakins, we immersed blue feathers in
liquid of the same refractive index as keratin and found that the blue color disappeared,
demonstrating that the color is produced structurally (Mason 1923; Shawkey and Hill
2005).  We also used transmission electron microscopy to identify the presence of a
medullary keratin matrix similar to that known to produce blue and ultraviolet coloration
in several passerine birds (Prum et al. 1999; Prum et al. 2003; Shawkey et al. 2003a;
Doucet et al. 2004).
Field methods
From March to July 2003 and 2004, we studied long?tailed manakins at Santa
Rosa National Park, Guanacaste Conservation Area, Costa Rica (10? 40? N, 85? 30 W).
We used mist nets to capture 293 manakins at or near lek sites (all birds captured between
0500 and 1200 CST). We fitted each bird with a numbered aluminum leg band and a
unique combination of three colored leg bands. We measured the spectral reflectance of
wild birds using an Ocean Optics USB 2000 spectrometer and PX?2 flash lamp (Ocean
Optics, Dunedin, FL). Our reflectance probe was mounted in a black rubber probe holder,
which excluded all external light and maintained the probe at a fixed distance (5 mm)
from, and perpendicular to, the feather surface. We measured the reflectance of five body
176
regions, namely the crown, mantle, tail, wing, and breast of each bird. We recorded five
measurements per body region, each of which comprised an average of 10 readings
collected in rapid succession by the operating software. Because the breast, wing, and tail
were of similar coloration within birds, we averaged these together and refer to them as
?body color? throughout. All reflectance data are expressed as the percentage of
reflectance from a white standard (WS?1, Ocean Optics). We collected 5?10 crown and
mantle feathers and the right outer rectrix of each bird for biochemical and structural
analysis of color production mechanisms (described above).
Museum
We visited the collections of the Louisiana State University Museum of Natural
Science in March of 2003 and the American Museum of Natural History in January of
2004. We measured the plumage reflectance of the study skins of 122 long?tailed
manakins as described above. We also recorded the date and location of collection
indicated on specimen tags when available. We then obtained the latitude and longitude
coordinates of all specimen collection locations and recorded these to the nearest degree.
If only a broad region such as a state or province was identified on specimen tags, we
recorded the coordinates of the approximate center of the distribution of long?tailed
manakins within that region.
Colorimetric variables
For each body region, we calculated three color variables to approximate the three
principal dimensions of color: brightness, hue, and saturation (Hailman 1977; Andersson
177
and Prager 2006; Montgomerie 2006a). For all body regions, we calculated brightness as
the total reflectance across the bird visible spectrum from 300 nm to 700 nm. We
calculated saturation, a measure of spectral purity, as the maximum reflectance minus the
minimum reflectance divided by the total reflectance. Because of the large differences in
the shape of the reflectance spectra between different body regions (Fig. 2), we used
different means of calculating hue for each region in order to ensure that this variable
captured relevant information. For the blue mantle and black body, we calculated hue as
the wavelength of maximum reflectance. For the red crown, we calculated hue as the
wavelength at which reflectance reached 50 % of its maximum reflectance. To examine
whether variation in reflectance between wild birds and study skins was evenly
distributed across the visual spectrum of birds, we calculated four measures of chroma
(e.g., Hill et al. 2005). To do this, we divided the visual spectrum into four 100?nm
segments and divided the reflectance in each segment by the total reflectance. We refer to
these as UV?chroma (300?400 nm), blue chroma (400?500 nm), green chroma (500?600
nm), and red chroma (600?700 nm).
Statistical Analysis
Only males in definitive adult plumage had a fully?developed red crown, an
entirely blue mantle, and entirely black body plumage (Doucet et al. In review). We
therefore restricted our analyses to these males. Because the distribution of long?tailed
manakins follows a roughly northwest to southeast axis (Fig. 1), latitude and longitude
coordinates of sampling locations were highly correlated (r
s
 = 0.87, n = 111, P < 0.0001).
We used principal components analysis to combine these two variables into one index of
178
location. Both latitude and longitude loaded highly and positively (component loadings =
0.71) on the first principal component (PC1), which explained 98% of the variation in
these coordinates. We therefore used PC1 as a measure of geographic location in our
analyses. High PC1 location scores correspond to individuals sampled from the
northwestern portion of the range of long?tailed manakins, while low PC1 location scores
correspond to individuals sampled from the southeast portion of the range (Fig. 1). We
used Shapiro?Wilk tests to determine whether the distribution of the original variables, or
of their residuals, met normality assumptions as required by t?tests or regression
analyses, respectively. In many cases where variable distributions departed significantly
from normality, standard transformations did not improve the fit to normality. We
therefore used non?parametric tests where appropriate. Slight variations in sample size
arose because not all information was available from all individuals/specimens.
RESULTS
Plumage reflectance of long?tailed manakins
Adult male long?tailed manakins have highly saturated red crown patches that reflect
very little at short and medium wavelengths, but increase steeply in reflectance at long
wavelengths (Fig. 2). By contrast, their blue mantles reflect maximally at ultraviolet
wavelengths and exhibit lower reflectance at long wavelengths (Fig. 2). The black body
plumage of adult male manakins exhibits low, uniform reflectance across the bird?visible
spectrum (Fig. 2).
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Overall differences between museum specimens and wild birds
There were significant differences in plumage coloration between museum skins
and wild male long?tailed manakins in definitive plumage. In particular, wild males had
significantly brighter and more highly saturated red crown coloration than study skins
(Table 1, Figs. 2, 3). Wild males also had significantly brighter blue mantles that peaked
at shorter (more UV) wavelengths than study skins (Table 1, Figs. 2, 3). The black body
coloration of live?caught males was also significantly darker and less saturated and
peaked at significantly shorter wavelengths than that of museum skins (Table 1, Figs. 2,
3).
Effects of specimen age and geographic location
To determine whether differences in plumage coloration between wild males and
study skins might have resulted from degradation in color over time, we investigated the
relationship between plumage color variables and the age of the specimens. Only the hue
of the black body plumage was significantly correlated with the age of the specimens,
with the hue of older specimens peaking at longer wavelengths than that of younger
specimens (Table 2).
To determine whether plumage color varied geographically among long?tailed
manakins, we investigated the relationship between plumage color variables and
sampling location (location PC1 ? see methods for PCA details). The brightness and
saturation of the crown were significantly negatively correlated with location PC1, such
that males in the southeastern portion of the range of long?tailed manakins (Costa Rica)
had brighter and more highly saturated red crowns than males in the northwestern portion
180
of the range (Mexico; Table 3). Additionally, the brightness of the mantle was
significantly negatively correlated with location PC1, while hue was positively correlated
with PC1, such that males in the southeastern portion of the range had brighter blue
mantles that peaked at shorter (more UV) wavelengths than males in the northwestern
portion of the range (Table 3). None of the black body plumage variables were
significantly correlated with geographic location (Table 3).
Because plumage color varied geographically (see above) and specimen age was
significantly related to sampling location (r
s
 = 0.56, n = 104, P < 0.0001), we used
multiple regression analyses to investigate the relative influence of specimen age and
geographic variation on plumage coloration. Variance inflation factors were less than
1.15 in all of our multiple regression analyses, indicating that colinearity did not unduly
bias our analyses. When controlling for geographic variation in color, there was a
significant negative relationship between crown saturation and specimen age, such that
older specimens had significantly less saturated red crowns than younger specimens
(Table 4, Fig. 4). Additionally, there was a significant negative relationship between
mantle brightness and specimen age whereas there was a significant positive relationship
between mantle hue and specimen age, such that older specimens had duller blue mantle
plumage reflectance that peaked at longer wavelengths (Table 4, Fig. 4). There were also
significant positive relationships between the brightness, hue, and saturation of the black
body plumage and specimen age such that older study skins had lighter, less uniform
body plumage reflectance that peaked at longer wavelengths (Table 4, Fig. 4). Similar
relationships between plumage coloration and specimen age were obtained when only
birds from the southern end of the distribution are considered (unpubl. data).
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These multiple regression models also allowed us to reassess the relationship
between sampling location and variation in color. When controlling for the effects of
specimen age, there was a significant negative relationship between crown brightness and
sampling location, such that birds in the southeastern portion of the range had brighter
red crowns than birds in the northwestern portion of the range (Table 4, Fig. 5).
Similarly, there was a significant negative relationship between mantle brightness and
sampling location, such that birds in the southeastern portion of the range had brighter
blue mantles than birds in the northwestern portion of the range (Table 4, Fig. 5). There
was no significant influence of sampling location on the coloration of the black body
plumage (Table 4, Fig. 5).
To determine whether the relative influence of specimen age and geographic
location on plumage color varied across the bird?visible spectrum, we used multiple
regression models to investigate the relationship between four measures of chroma and
both specimen age and sampling location for each body region. When controlling for
geographic variation in color, there was a significant positive relationship between UV?,
blue?, and green?chroma of the red crown and specimen age (Table 5). By contrast, there
was a significant negative relationship between red?chroma of the red crown and
specimen age (Table 5). Thus, the red crown of older specimens reflected proportionally
less in the red portion of the spectrum and proportionally more in the green, blue, and UV
regions of the spectrum. Additionally, there was a significant negative relationship
between UV?chroma of the blue mantle and specimen age (Table 5). By contrast, there
was a significant positive relationship between green? and red?chroma of the blue mantle
and residual specimen age (Table 5). Thus, the blue mantle of older specimens reflected
182
proportionally less in the UV and proportionally more in the green and red regions of the
spectrum. There was also a significant negative relationship between blue?chroma of the
black body plumage and specimen age. By contrast, there was a significant positive
relationship between red?chroma of the black body plumage and specimen age. Thus, the
black body plumage of older specimens reflected proportionally less in blue and green
portions of the spectrum and proportionally more in red regions of the spectrum.
When controlling for the effects of specimen age, there was a significant positive
relationship between UV?chroma of the red crown and location PC1, such that the
crowns of birds in the northwestern portion of the range reflected proportionally more in
the UV than those of birds in the southeastern portion of the range (Table 5). There was
no significant relationship between any of the chroma variables for the blue mantle and
location PC1. However, there was a significant positive relationship between UV?chroma
of the black body plumage and location PC1 whereas there was a significant negative
relationship between blue? and green?chroma of the black body plumage and location
PC1. Thus, the black body plumage of birds in the northwestern part of the range
reflected proportionally more in the UV and proportionally less in the blue and green
regions of the spectrum than birds in the southeastern portion of the range.
DISCUSSION
Using long?tailed manakins as a model system, we show that there are significant
differences in plumage color between museum specimens and wild birds with respect to
carotenoid, melanin and structural plumage coloration. Our data suggest that these
differences are due in part to a combination of geographic variation and specimen age.
183
Colors produced by different mechanisms also showed spectrally different patterns of
color degradation.
Some of the differences in coloration between the feathers of wild males and
feathers on study skins may result from the specimen preparation process per se. It is
possible, for example, that the feathers of study skins have been stripped of their preen
gland secretions. These uropygial oils create a protective sheen on the feathers (Elder
1954) that could potentially affect plumage brightness (Piersma et al. 1999; Reneerkens
and Korsten 2004; Montgomerie 2006b). Moreover, because some uropygial oils do not
absorb light evenly across the reflectance spectrum, their presence or lack thereof on
feathers has the potential to influence the shape of reflectance spectra (Piersma et al.
1999; Reneerkens and Korsten 2004; Montgomerie 2006b). The preen oil secretions
could be destroyed during the specimen preparation process through absorption by the
corn meal or potato flour used to prepare specimens or by chemical breakdown when
detergents are used to clean the skins. Alternatively, preen oils might simply degrade
over time. Similarly, several taxonomic groups (mostly non?passerines) have powder
down patches that secrete a greasy powdery substance thought to have similar functions
to uropygial secretions (Wetmore 1920; Lowery and O'Neill 1966; Brown and Toft
1999). It is therefore possible that secretions from powder down, or lack thereof, would
influence the plumage coloration of study skins in some species. The potential effects of
uropygial secretions and powder down secretions on plumage reflectance need to be
investigated in more detail. It should be noted that washing museum skins during the
specimen preparation process is often essential to remove blood, fat, or dirt from feathers,
and that, in most cases, any plumage color differences caused by the lack of preen or
184
powder down secretions are likely to be smaller than differences caused by heavily soiled
plumage (Lowery and O'Neill 1966; Reneerkens and Korsten 2004; Montgomerie
2006b).
Differences between prebasic (postbreeding) and prealternate (prebreeding)
plumages aside, overall color differences between study skins and wild birds could also
result from the different times of year at which samples were collected. In this study, all
wild birds were measured within a four?month period during the early part of the
breeding season. By contrast, study skins were collected throughout the year, and might
be expected to show more variation in feather wear, a factor known to influence plumage
color (?rnborg et al. 2002; McGraw and Hill 2004). Within?year variation in color
caused by wear is expected to be even greater in species that attain a bright nuptial
plumage by wearing down the melanized tips of their feathers (e.g., Lyon and
Montgomerie 1995; Willoughby et al. 2002). These effects underscore the importance of
considering annual variation in plumage color when measuring museum specimens and
could be minimized by comparing only samples collected at similar times of year.
Although the specimen preparation process has the potential to influence the color
of study skins, our findings suggest that this is not the only reason for differences in
feather color between study skins and wild birds. In analyses controlling for the age of
the specimens, we found significant geographic variation in color for the red crown, blue
mantle, and black body plumage. In particular, the brightness of the red crown increased
when moving away from the northwestern portion of the range long?tailed manakins
(Mexico) and toward the southeastern portion of the range (Costa Rica). Similarly, the
brightness of the blue mantle increased toward the southeastern portion of the range.
185
Finally, the UV?chroma of the black body plumage increased, whereas the blue? and
green?chroma decreased, toward the southeastern portion of the range. This geographic
variation in color generally corresponds to subspecific distinctions in this species: C. l.
fastuosa, which occupies the southeastern part of the range from El Salvador to Costa
Rica, is described as being ?brighter? that the nominate race, C. l. linearis, which
occupies the northwestern part of the range from Guatemala to Mexico (Snow 2004). Our
data suggest, however, that plumage color changes gradually across the range of
long?tailed manakins rather than showing discontinuous variation between the two
subspecies (see also Zink 2004). Elucidating the potential causes of this geographic
variation is beyond the scope of the present study. Nonetheless, geographic variation in
long?tailed manakin plumage coloration is subtle compared to that documented in other
species, and this potentially confounding variable should be considered in future studies
(e.g., Peterson 1997).
When controlling for geographic variation in color, we found significant
relationships between various aspects of plumage color and the age of study skins. Older
long?tailed manakin museum specimens had less saturated red crowns, blue mantles that
peaked at longer (less UV) wavelengths and black body plumage that was more saturated
(less spectrally flat), brighter (less dark), and peaked at longer wavelengths. Older
museum specimens also had red crowns that reflected proportionally less in red regions
of the spectrum and proportionally more in UV, blue, and green regions of the spectrum,
blue mantles that reflected proportionally less in the UV and proportionally more in green
and red regions of the spectrum, and black body plumage that reflected proportionally
less in blue regions of the spectrum and proportionally more in red regions of the
186
spectrum. These documented relationships between plumage coloration and specimen age
in long?tailed manakins suggest that the plumage colors fade or degrade over time. The
most likely causes of such time?dependent patterns of color degradation are the
accumulation of dust or dirt on the specimens (Eaton and Lanyon 2003; Montgomerie
2006a) or the abrasion or breakage of feather barbs or barbules (?rnborg et al. 2002;
McGraw and Hill 2004). A few other possibilities exist. First, plumage coloration might
be altered by the actions of feather?degrading bacteria (Shawkey and Hill 2004; Shawkey
et al. In review). Uropygial oil has been shown to suppress the growth of
feather?degrading bacteria and fungus (Pugh and Evans 1970; Pugh 1972; Shawkey et al.
2003b). Thus, in addition to the absence of maintenance behaviors like preening
(Zampiga et al. 2004), the removal or degradation of uropygial secretions on museum
skins effectively eliminates this protective mechanism. No study has specifically
investigated the direct effects of feather chewing lice or mites on plumage coloration.
However, correlational and experimental studies suggest an association between louse or
mite abundance and plumage color (Thompson et al. 1997; Harper 1999; Figuerola et al.
2003). Although the effects of these ectoparasites on color could be indirect, it is also
possible they could affect plumage coloration directly in a manner similar to
feather?degrading bacteria. Bactericides and insecticides are sometimes used in specimen
preservation and likely reduce the potential effects of keratinolytic bacteria, fungi, and
feather?chewing ectoparasites.
Interestingly, the time?dependent effects of feather degradation influenced the
three types of plumage color in different ways. Although the brightness of red and blue
feathers did not significantly change with specimen age, the brightness of black feathers
187
increased with specimen age. Only the saturation of red and black feathers was
significantly related to specimen age, whereas only the hue of blue and black feathers
changed significantly with specimen age. Moreover, the proportional changes in color in
different parts of the spectrum in relation to specimen age varied among the three
different types of plumage color. Because feathers did not simply all become duller or
change in color evenly across the spectrum, our findings suggest that the cause of color
degradation varied, at least in part, according to the different color production
mechanisms.
Carotenoid?based colors are produced by the deposition of carotenoid pigments
into growing feathers (Fox and Vevers 1960; McGraw 2006a). The resulting color
depends on the absorptive properties of the carotenoids in question (McGraw 2006a) and
the underlying (usually white) structure of the feather (Shawkey and Hill 2005). Pigment
concentration has been shown to affect the hue and saturation, but not the brightness, of
carotenoid?based colors (Saks et al. 2003). The decrease in saturation and red chroma of
the crown feathers of long?tailed manakins in older specimens, together with the increase
in UV?, blue?, and green?chroma in these specimens, suggests that some degradation of
the carotenoid pigments occurs over time. Carotenoids can degrade by oxidization or
isomerization (Test 1940; Britton 1995). Oxidization breaks down carotenoid pigments
and thereby results in pigment bleaching (Britton 1995). The significant decrease in the
red?chroma and saturation of the red crown with increasing specimen age is consistent
with such a bleaching effect. Not all carotenoids are equally reactive to oxidization
(Britton 1995). The carotenoid responsible for the red crown color of long?tailed
manakins (canthaxanthin; S. M. Doucet and K. J. McGraw, unpubl. data), for example,
188
oxidizes more slowly than one of the carotenoids responsible for epaulet color in
red?winged blackbirds, Agelaius pheniceus (zeaxanthin, Britton 1995; McGraw et al.
2004a). Thus, pigment bleaching may be more pronounced in species where more
reactive carotenoids are used as coloring pigments. Isomerization refers to changes in the
stereochemistry (geometry) of carotenoid pigments (Britton 1995). Carotenoid pigments
in nature, including those in bird feathers, are most often found in the all?trans form
(Britton 1995; McGraw 2006a). Exposure to light, heat, oxygen, humidity, or acidity can
promote the isomerization of carotenoids, resulting in less stable cis?isomers (Shi and Le
Maguer 2000). The absorption maxima of carotenoid cis?isomers are often located at
shorter wavelengths than those of trans isomers (Lyan et al. 2001; Updike and Schwartz
2003). Thus, cis?isomerization can produce changes in hue. Additionally, the instability
of cis?isomers often results in their eventual degradation. Thus, some of our observed
changes in carotenoid coloration may have occurred by pigment isomerization.
Non?iridescent structural colors are produced by the constructive interference of
light in the medullary keratin matrix of feather barbs (Prum et al. 1999; Prum et al. 2003;
Shawkey et al. 2003a; Doucet et al. 2004). In eastern bluebirds, Sialia sialis, variation in
structural blue color results from variation in the dimensions of components of the keratin
matrix as well as variation in larger?scale factors such as the thickness of the feather
cortex and the density of barbules (Shawkey et al. 2003a; Shawkey et al. 2005).
Moreover, experimentally?induced degradation of the barb cortex and keratin matrix
from keratinolytic bacteria results in increases in brightness, hue, and saturation, and a
decrease in chroma, of structural blue feathers (Shawkey et al. In review). Thus,
structural blue colors may be particularly sensitive to damage caused by bacteria and lice.
189
Our documented changes in hue and chroma of the blue mantle with specimen age may
be consistent with some form of parasitic degradation of feather barbs. Such changes in
color could also be caused by soiling and feather wear, however, particularly if soiling
influences some parts of the reflectance spectrum more than others, as has previously
been suggested (?rnborg et al. 2002).
Melanin?based colors are produced by the deposition of melanin pigments into
growing feathers (McGraw 2006b). Eumelanins generally absorb light evenly across the
bird?visible spectrum, resulting in flat reflectance spectra of low amplitude (Mennill et
al. 2003; McGraw 2006b). As such, high concentrations of melanin should result in
darker plumage of lower reflectance. As large polymers with strong cross?links to
proteins, melanins are thought to confer structural stability to animal and plant tissues,
including bird feathers (Burtt 1986; Bonser 1995). Melanized feathers are more resistant
to abrasion than unmelanized feathers (Bonser 1995; McGraw 2006b), and  recent studies
have shown that melanized feathers are less susceptible to the effects of feather chewing
lice (Kose et al. 1999) and feather degrading bacteria (Goldstein et al. 2004) than
unmelanized feathers. Moreover, melanin pigments are highly biochemically stable
(Riley 1997). We therefore expected that, of the three types of color we investigated,
melanins would be the least susceptible to long?term degradation (Test 1940). However,
we found significant, albeit subtle, variation in the black body plumage of long?tailed
manakins. By contrast with crown and mantle coloration, the brightness of the black body
plumage increased with increasing specimen age. One possible explanation is that
superficial damage to barbs and barbules, be it caused by abrasion or degradation from
bacteria or lice, would roughen the surface of the keratin cortex without affecting the
190
melanin granules themselves, which are found below the cortex. Rougher surfaces
increase incoherent scattering of white light (Bradbury and Vehrencamp 1998; Prum
2006), which would thereby increase brightness (Shawkey et al. In review). The changes
in saturation and chroma of black body plumage are rather more difficult to explain. One
possibility is that they result from physical or biochemical changes to other parts of the
feather rather than to the melanin granules. Alternatively, eumelanin pigments, which are
black, may be more susceptible to degradation than phaeomelanin pigments, which are
reddish?brown. Since many melanin?based colors contain both eumelanin and
phaeomelanin pigments (McGraw et al. 2004b), a reduced proportion of eumelanin might
result in higher reflectance at longer wavelengths and a more brownish appearance (Test
1940). Yet another possibility is that biochemical degradation of eumelanin pigments
alters their color.
Using long?tailed manakins as a model system, we have documented differences
in plumage reflectance between museum specimens and wild birds for carotenoid,
structural, and melanin?based colors. Some degradation appeared to be of a generalized
nature, while some changes varied by plumage color type. It is important to note that, in
most cases, differences between study skins and wild birds were quite subtle (Fig. 2).
Indeed, this is somewhat surprising, given that plumage colors have been shown to
change considerably over much shorter time scales (?rnborg et al. 2002; McGraw and
Hill 2004). As such, study skins can serve as an accurate representation of the plumage
reflectance patterns of wild birds, particularly for broad?scale analyses such as
characterizing the reflectance of a particular species or quantifying interspecific
differences in color. Intraspecific studies, however, such as assessments of sexual
191
dichromatism or investigations of geographic variation in ornamentation, should consider
the potential effects of specimen age. In most cases, it is possible account for these
potentially confounding factors by calculating residuals or using multivariate analyses
that include geographic location and specimen age as covariates. Alternatively, one could
restrict samples to a particular time period or geographic location if only a few
individuals of a particular species are required. We also found that time?dependent
plumage color changes varied by plumage type. For example, proportional UV
reflectance decreased with specimen age in structural blue plumage but increased with
specimen age in red carotenoid plumage. Thus, broad scale studies of particular types of
signals based on museum skins, such as investigations of the ubiquity of UV reflectance,
should be interpreted cautiously. Finally, our findings highlight the importance of
museum practices in maintaining not only the structural integrity of museum skins, but
also the quality of their plumage coloration. Minimizing exposure to light, handling,
bacteria, fungi, insects, and lice will help to preserve the quality and color of study skins,
which, in this era of reduced emphasis on collecting (Remsen 1995; Winker 2004), will
allow researchers to benefit from their use for generations to come.
ACKNOWLEDGEMENTS
We thank L. Baril, V. Connolly, A. Lindo, and D. Mennill for assistance in the
field as well as D. Mennill for assistance with museum data collection. We are grateful to
R. Blanco and the Guanacaste Conservation Area for logistical support and permission to
work in Parque Nacional Santa Rosa. We thank the curators at the American Museum of
Natural History and the Louisiana State University Museum of Natural Science for
192
providing access to the research collections under their care. J. V. Remsen provided
helpful information on specimen preparation and storage and C. Guyer, H. Fadamiro, D.
Mennill and F. S. Dobson provided helpful comments on this manuscript. This study was
funded by a Natural Science and Engineering Research Council of Canada Postgraduate
Scholarship, a Sigma?Xi Grant?in?Aid?of?Research, a Wetmore Research Award from
American Ornithologists? Union, the Louis Agassiz Fuertes Award from the Wilson
Ornithological Society, the Exploration Fund of the Explorer?s Club, a Collections Study
Grant and a grant from the Frank M. Chapman Memorial Fund from the American
Museum of Natural History, and Auburn University Graduate Research Grants (to SMD),
as well as NSF grant 420647 (to GEH).
193
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Table 1. Comparison of plumage reflectance (colorimetric variables) between museum
skins and live?caught male long?tailed manakins in definitive plumage. T?tests were
used for normally distributed variables and Wilcoxon tests were used when variables
departed significantly from normality.
Body regionColor variableWild birds
(n = 58)
Study skins
(n = 55)
Test statisticP
Red crownBrightness (%)12.79 ? 1.9211.01 ? 2.45T = 4.31<0.0001*
Hue (nm)632.2 ? 3.74630.9 ? 4.5Z = ?1.20  0.23
Saturation5.62 ? 0.454.85 ? 0.60Z = ?6.39<0.0001*
Blue mantleBrightness (%)31.4 ? 3.5728.9 ? 2.68T = 4.07<0.0001*
Hue (nm)370.8 ? 9.1401.5 ? 30.5Z = 7.54<0.0001*
Saturation0.72 ? 0.090.68 ? 0.06T = ?2.12  0.03
Black bodyBrightness (%)3.36 ? 0.913.70 ? 0.58Z = ?3.43  0.0006*
Hue (nm)588.3 ? 76.4651.6 ? 80.3Z = 5.46<0.0001*
Saturation0.47 ? 0.260.60 ? 0.15Z = 5.04<0.0001*
*Significant after Bonferroni correction
204
Table 2. Relationship between plumage color variables and specimen age (age = 1 for
wild birds) among male long?tailed manakins in definitive adult plumage.
Body regionColor variabler
s
n P
Red crownBrightness (%)0.12 103 0.41
Hue (nm)0.23 102 0.13
Saturation0.06 103 0.69
Blue mantleBrightness (%)0.28 104 0.06
Hue (nm)0.16 104 0.31
Saturation0.10 104 0.51
Black bodyBrightness (%) ?0.14103   0.35
Hue (nm)0.67 104 <0.0001*
Saturation0.15 103   0.32
*Significant after Bonferroni correction
205
Table 3. Relationship between plumage color variables and geographic location (PC1
location ? see methods for details on PCA) among male long?tailed manakins in
definitive adult plumage.
Body regionColor variabler
s
n P
Red crownBrightness (%)?0.38110 <0.0001*
Hue (nm)  0.08109   0.36
Saturation?0.30110   0.001*
Blue mantleBrightness (%)?0.34111   0.0002*
Hue (nm)  0.35111   0.0002*
Saturation?0.20111   0.04
Black bodyBrightness (%)  0.22110   0.02
Hue (nm)  0.17111   0.07
Saturation  0.16110   0.09
*Significant after Bonferroni correction
206
Table 4. Multiple regression of plumage color variables on specimen age and sampling
location (PC1 location ? see methods for details on PCA) among male long?tailed
manakins in definitive adult plumage.
Body regionColor variableR
2
F ? df P
Red crownBrightness (%)Model0.2617.52, 100<0.0001*
Specimen age  0.21?0.041, 101  0.64
Location28.4?0.491, 101<0.0001*
Hue (nm)Model0.03  1.662, 99  0.19
Specimen age  2.63?0.171, 100  0.11
Location  1.860.141, 100  0.18
SaturationModel0.2718.62, 100<0.0001*
Specimen age24.3?0.451, 101<0.0001*
Location  2.51?0.141, 101  0.12
Blue mantleBrightness (%)Model0.1710.12, 101<0.0001*
Specimen age  3.91?0.191, 102  0.05
Location  9.29?0.301, 102  0.003*
Hue (nm)Model0.4236.22, 101<0.0001*
Specimen age66.8 0.661, 100<0.0001*
Location  0.55?0.061, 100  0.46
SaturationModel0.07  4.072, 101  0.02
Specimen age  2.64?0.171, 102  0.11
Location  2.55?0.161, 102  0.11
Black bodyBrightness (%)Model0.05  2.412, 100  0.09
Specimen age  3.350.191, 101  0.07
Location  0.220.051, 101  0.64
Hue (nm)Model0.2113.22, 101<0.0001*
Specimen age25.50.481, 102<0.0001*
Location  1.04?0.101, 102  0.31
SaturationModel0.10  5.342, 100  0.006
Specimen age  9.960.321, 101  0.002*
Location  0.12?0.031, 101  0.73
*Significant after Bonferroni correction
207
Table 5. Multiple regression of plumage chroma variables on specimen age and sampling
location (PC1 location ? see methods for details on PCA) among male long?tailed
manakins in definitive adult plumage.
Body regionColor variableR
2
F ? df P
Red crownUV chromaModel0.3932.0 2, 100<0.0001*
Specimen age23.20.401, 101<0.0001*
Location17.80.351, 101<0.0001*
Blue chromaModel0.3830.6 2, 100<0.0001*
Specimen age35.70.501, 101<0.0001*
Location6.540.221, 101  0.01
Green chromaModel0.3122.0 2, 100<0.0001*
Specimen age32.50.511, 101<0.0001*
Location1.250.101, 101  0.27
Red chromaModel0.3729.9 2, 100<0.0001*
Specimen age32.7?0.481, 101<0.0001*
Location7.8?0.241, 101  0.006
Blue mantleUV chromaModel0.3932.6 2, 101<0.0001*
Specimen age61.3?0.651, 102<0.0001*
Location0.960.081, 102  0.33
Blue chromaModel0.073.84 2, 101  0.02
Specimen age7.680.291, 102  0.007
Location0.85?0.091, 102  0.36
Green chromaModel0.3022.1 2, 101<0.0001*
Specimen age41.50.571, 102<0.0001*
Location0.60?0.071, 102  0.44
Red chromaModel0.137.57 2, 101  0.0009*
Specimen age13.40.361, 102  0.0004*
Location0.01?0.011, 102  0.92
Black bodyUV chromaModel0.2012.5 2, 100<0.0001*
Specimen age1.42?0.111, 101  0.24
Location24.60.481, 101<0.0001*
Blue chromaModel0.4642.7 2, 100<0.0001*
Specimen age39.7?0.501, 101<0.0001*
Location16.3?0.311, 101<0.0001*
Green chromaModel0.3122.212, 100<0.0001*
Specimen age5.34?0.211, 101  0.03
Location25.1?0.451, 101<0.0001*
Red chromaModel0.71123.52, 100<0.0001*
Specimen age204.70.831, 101<0.0001*
Location0.930.051, 101  0.34
*Significant after Bonferroni correction
208
FIGURE CAPTIONS
Figure 1. Map of Central America showing geographic distribution of long?tailed
manakins, Chiroxiphia linearis. The magnitude of location PC1 scores is also shown.
Figure 2. Average reflectance spectra for the red crown, blue mantle, and black body
among male long?tailed manakins in definitive adult plumage. Solid lines represent a
subset of live?caught males (n = 15) and dashed lines represent a subset of study skins (n
= 15).
Figure 3. Box plots showing differences in plumage color variables between live?caught
male long?tailed manakins in definitive adult plumage and study skins. Horizontal lines
in box plots show 10
th
, 25
th
, 50
th
, 75
th
, and 90
th
 percentiles. Asterisk identifies differences
that are statistically significant after Bonferroni correction (see Table 1).
Figure 4. Scatterplots showing relationship between plumage color variables and residual
specimen age (controlling for geographic location) among male long?tailed manakins in
definitive adult plumage. Regression lines are included in plots that show a statistically
significant correlation after Bonferroni correction (see Table 4).
Figure 5. Scatterplots showing relationship between plumage color variables and residual
geographic location (controlling for specimen age) among male long?tailed manakins in
209
definitive adult plumage. Regression lines are included in plots that show a statistically
significant correlation after Bonferroni correction (see Table 4).
210
Figure 1
15?
10?
20?
90?85?80?95?
high             
PC1 
 
 
 
low
211
Figure 2
0
10
20
30
40
50
60
70
0
10
20
30
40
50
0
2
4
6
8
10
12
14
300400500600700
reflectance 
(%)
reflectance 
(%)
reflectance 
(%)
wavelength (nm)
red crown
 blue mantle
black body
212
Figure 3
saturation
0.2
0.4
0.6
0.8
1.0
1.2
wildmuseum
saturation
0.5
0.6
0.7
0.8
0.9
saturation
2.5
3.5
4.5
5.5
6.5
brightness 
(%)
8
12
16
20
brightness 
(%)
20
25
30
35
40
45
hue 
(nm)
300
400
500
600
700
wildmuseum
hue 
(nm)
360
380
400
420
440
brightness 
(%)
1
2
3
4
5
6
wildmuseum
hue 
(nm)
610
620
630
640
red crown
 blue mantle
black body
*
*
* *
***
213
Figure 4
3
4
5
6
7
saturation
0.5
0.6
0.7
0.8
0.9
0.2
0.6
1.0
1.4
8
10
12
14
16
18
brightness 
(%)
20
25
30
35
40
2
3
4
5
6
7
-20020406080100
residual specimen age
370
410
450
490
300
400
500
600
700
610
615
620
625
630
635
640
hue 
(nm)
-20020406080100
residual specimen age
-20020406080100
residual specimen age
saturation
brightness 
(%)
hue 
(nm)
saturation
brightness 
(%)
hue 
(nm)
red crown
 blue mantle
black body
214
Figure 5
brightness 
(%)
brightness 
(%)
brightness 
(%)
saturation
saturation
hue 
(nm)
hue 
(nm)
hue 
(nm)
saturation
6
8
12
14
16
18
20
10
Costa Rica
Mexico
-3-2-10123
residual location (PC1)
610
615
620
625
630
635
640
3
4
5
6
7
20
25
30
35
40
360
380
400
420
440
460
480
500
0.5
0.6
0.7
0.8
0.9
2
3
4
5
6
7
300
400
500
600
700
0.2
0.4
0.6
0.8
1.0
1.2
1.4
Costa Rica
Mexico
-3-2-10123
residual location (PC1)
Costa Rica
Mexico
-3-2-10123
residual location (PC1)
red crown
 blue mantle
black body
215
CONCLUSIONS
As a consequence of their lek-based mating system, manakins have proven to be
an excellent system for investigating the influence of natural and sexual selection on
plumage coloration and morphology. First, I demonstrated that young male long?tailed
manakins, Chiroxiphia linearis, exhibit remarkably age?specific patterns of plumage
coloration before attaining definitive adult plumage in their fifth year. This unusual
pattern of delayed plumage maturation likely serves an important function in maintaining
age?graded dominance hierarchies and mating queues at lek sites. Second, I found that
patterns of sexual dimorphism within C. linearis and among Chiroxiphia manakins are
consistent with predictions of natural and sexual selection hypotheses. Sexual selection
for acrobatic display efficiency appears to act strongly on males, whereas natural
selection through intersexual competition and reproductive role division appears to
constrain dimorphism in some traits while enhancing it in others. Third, I used irradiance
and reflectance spectrometry and avian perceptual models to quantify the degree of
conspicuousness in male plumage and crypsis in female plumage of long?tailed
manakins. Males did not appear to adjust the timing or location of their displays to
enhance conspicuousness, but rather displayed in the most common light environment of
forest shade. Displaying this light environment may reflect a trade?off between
maximizing conspicuousness in males while minimizing it in females. Finally, I found
significant differences in plumage coloration between museum specimens and wild birds.
216
The magnitude and direction of these differences depended in part of the mechanism of
color production. Most differences were relatively subtle, however, and my findings
justify the use of museum specimens to assess plumage coloration for various types of
studies.