Behavioral Ecology Vol. 12 No. 4: 429-438
© 2001 International Society for Behavioral Ecology
Dirty ptarmigan: behavioral modification of conspicuous male plumage
a Department of Biology, Queen's University, Kingston, Ontario, Canada K7L 3N6 b Biology Department, Earth and Marine Sciences Building, University of California, Santa Cruz, CA 95064, USA c Center for Tropical Research, Department of Biology, San Francisco State University, San Francisco, CA 94132, USA
Address correspondence to R. Montgomerie. E-mail: montgome{at}biology.queensu.ca .
Received 5 April 2000; revised 25 September 2000; accepted 2 October 2000.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Males of many bird species acquire a conspicuous breeding plumage through molt. Male rock ptarmigan (Lagopus mutus), however, become conspicuous in a unique way—as snow melts away from the tundra, their cryptic white winter plumage suddenly becomes exceptionally conspicuous, and remains so for at least 3 weeks. While males remain white, females molt into one of the most cryptic plumages known in birds. From our 17-year field study in arctic North America, we show that, unlike other birds, male rock ptarmigan eventually change from conspicuous to cryptic by soiling their plumage, thereby reducing their conspicuousness six fold before they molt to their cryptic summer plumage. Individual males began to soil their plumage as soon as their mates began egg-laying, and were maximally dirty and relatively cryptic by the time incubation began and their mates no longer fertilizable. Thus male plumage conspicuousness appears to serve a reproductive function. Moreover, both polygynous and bachelor males delayed soiling for a few days after monogamous males, as expected because of the prolonged mating opportunities available to them. We use these data to address a variety of hypotheses to explain both the conspicuousness of breeding males and their subsequent plumage soiling. Given the high predation rate recorded for male ptarmigan during the breeding season, we argue that male conspicuousness is best explained by sexual selection and that plumage soiling is an adaptation that reduces predation risk by increasing camouflage.
Key words: color, conspicuousness, crypsis, plumage, ptarmigan, sexual selection.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
The explanation of sexual differences in size, weapons, and ornamentation is a cornerstone of Darwin's (1871
) theory of sexual
selection. In some species such sexual dimorphism occurs year-round (e.g.,
differences in body size) and might be explained by intersexual differences in
foraging, dominance or habitat use (see
Andersson, 1994). When the
sexes are most dimorphic during the breeding season, sexual selection would
seem to be the most compelling explanation. In many species, males (or
sometimes females) acquire conspicuous signals like bright colors, distinctive
odors, fancy ornaments, or dangerous weapons just before the period of mate
attraction and lose them just as rapidly when the breeding season ends,
suggesting that these traits are both important for mate acquisition and
costly.
Birds provide many of the best examples for which the benefits of
conspicuous breeding colors have been documented. In most waterfowl and
songbirds, males and females have similar, cryptic plumages in the nonbreeding
season but, before the onset of breeding, males molt into a brightly colored
plumage while females remain dull-colored. While the influence of sexual
selection on such striking dimorphism seems clear
(Andersson, 1983;
Butcher and Rohwer, 1988),
other explanations for this seasonal plumage change have been proposed: bright
male plumage might advertise to predators that males are difficult to capture
(Baker and Parker, 1979), or
might be important in resource holding or species recognition
(Butcher and Rohwer, 1988).
Only in the past two decades has the pervasive influence of female choice and
male—male competition for mates on male plumage traits finally been
documented (Andersson, 1994).
Thus, the mating benefits of conspicuous male plumage now seem clear but the
fact that such plumage is seasonal suggests that there may be associated
costs.
The most obvious potential costs of conspicuous plumage are the time and
energy required to produce it and an increase in predation risk. While
production costs have been difficult to quantify, there is now ample evidence
that more conspicuous species suffer greater predation risk
(Andersson, 1994). Indeed,
comparative studies suggest that interspecific variation in male plumage
brightness may be related to mortality costs in both songbirds and waterfowl
(Promislow et al., 1992,
1994). Intraspecific variation
in conspicuousness has been less well studied and the relation between
brightness, conspicuousness, and predation risk within species is still poorly
understood
(Götmark and
Hohlfält, 1995).
Rock ptarmigan (Lagopus mutus) are the classical case of both
conspicuous and cryptic plumage in birds. Darwin
(1871), Huxley
(1938), and Cott
(1940) all discussed these
birds as having the most striking case of seasonal change in plumage resulting
from the need for camouflage. Rock ptarmigan need to be cryptic because they
live year-round on the open tundra where they are particularly vulnerable to
predation from falcons and hawks—they comprise 66-100% of the diet of
arctic-nesting gyrfalcons (Falco rusticolus) during the short, high
arctic breeding season (Bergerud,
1988). Moreover, male rock ptarmigan are selectively hunted by
gyrfalcons (Cade, 1960;
Gardarsson, 1988;
Wayne and Jolly, 1958) and
male mortality in the breeding season is higher than that of females, being
highest in May-June (by gyrfalcons; Cotter
et al., 1992; Gardarsson,
1971; Nielsen and Cade,
1990; by hunters; Olpinski,
1986) when they are most conspicuous.
Given this high predation risk, it is surprising that, during the early
part of their breeding season (late May to mid-June), male rock ptarmigan are
one of the most conspicuous birds known. Both sexes of rock ptarmigan are
almost completely white in winter, particularly cryptic against the snow (at
least to human eyes; Figure
1a), and their plumage does not reflect in the UV-range in a way
that would be visible to avian predators and conspicuous against the snow
(Montgomerie R, unpublished data). When snow melts in spring, females molt
quickly to a mottled brown plumage that makes them cryptic against the tundra
(Figure 1b)—one of the
best examples of camouflage in vertebrates—while males remain white and
thus are highly conspicuous (Figure
1c). Early in the breeding season, females on the tundra are
visible to humans at no more than a few meters, whereas males can readily be
detected with the naked eye at 1-2 km. It seems clear that female crypticity
is an adaptation to reduce predation. Males, too, molt into a cryptic brown
plumage in summer but male molt does not begin until well after females have
already molted (Holder and Montgomerie,
1993). Why then do males remain conspicuous for so long and how do
they deal with the potentially high predation risk of their white plumage
early in the breeding season?
|
In this study, we quantified the patterns of changing conspicuousness of male and female rock ptarmigan in the spring, during 17 years of fieldwork in the North American arctic. We document here an unusual form of plumage modification that helps males mitigate the potentially high costs of conspicuousness—males in all but one of our study populations actively soiled their plumage (Figure 1d), apparently when their conspicuousness no longer served a function. Thus both the process by which male ptarmigan become conspicuous and the behavior that they later use to make their plumage more cryptic are extraordinary. Our analyses of the timing of plumage dirtying suggest that male plumage conspicuousness and dirtiness both serve an adaptive function.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
We conducted most of this research from 1981-1993 on 13 km2 of upland high arctic tundra at Sarcpa Lake, Nunavut, Canada (see Montgomerie et al., 1983
for
details). Each year we spent varying periods from 29 May-10 August at this
study site, often arriving while ptarmigan were still in late winter flocks
and usually staying at least until all females were incubating clutches.
Though our research spanned many years, comprehensive data on many aspects of
this study were obtained in only 1-2 seasons due to variable weather and
working conditions, changing ptarmigan sex ratios, and mating tactics
(Brodsky, 1988), a 10-year
cycle of population fluctuations of more than an order of magnitude, and the
demands of other research. Consequently we often report data from only a
single year to illustrate a point, though much more limited data from other
years are entirely consistent. All quantitative data presented here are from
the Sarcpa Lake population. At Sarcpa Lake, the snow typically begins to melt in early June and birds of all species begin breeding by the middle of the month. Every year, we monitored ptarmigan population size and mating success, and the distribution and size of male territories. Most ptarmigan were individually color banded in most years. During the first year of our study, we observed that male ptarmigan soiled their immaculate white plumage during the breeding season and we spent the subsequent years gathering data to try to understand why they performed this behavior.
In addition to this long-term study at Sarcpa Lake, we studied rock
ptarmigan at seven sites across the Nearctic (Attu Island, Kodiak Island, and
Deadhorse, Alaska, Gros Morne, NF, and Ellesmere Island, Bathurst Island, and
Igloolik Island, Nunavut) from 1992-1997. At each of these sites, we
determined the timing and extent of molt and plumage soiling and recorded
behavioral data during the breeding season in the course of other studies
(e.g., Holder et al.,
1999).
Plumage characteristics
Throughout June of 1983 and 1987-1989, weather permitting, we monitored
daily the molt and plumage status of all male and female ptarmigan on our
study site. For each bird we recorded the identity, location, stage of molt
(percent of feathers molted, to the nearest 5%), and degree of plumage
dirtiness on a 0-4 scale (males only). To standardize dirt scores among years
and observers, we used the following criteria: 0 = immaculate or nearly so
(Figure 1c) with no more than a
few light stains on the belly; 1 = light wash of yellowish or brown visible
only at close range (<5 m); 2 = pale graybrown all over; 3 = distinct dirty
streaks on breast and back; 4 = dirty and bedraggled all over, feathers look
worn (Figure 1d). Most males
were scored from <20 m distance so any slight plumage dirtiness was easily
detectable with binoculars. Dirt scores were highly repeatable
(rI =.93; 20 males scored independently by two or more
observers within 24 h). Because male dirt scores often alternated between 0
and 1 for a few days when they began to get dirty, we used the last date that
they were observed with a score of 0 as an index of the onset of
dirtiness.
To examine experimentally how plumage dirtiness might influence mate choice we soiled the plumage of three males with a black "indelible" marker in 1987, as soon as they settled on territories. After we darkened their plumage, the plumage color of these males was equivalent to a dirt score of 4 where all other males in the population were scored 0 at the time. Within 2 days all of these males' plumages were immaculate and a female had settled on each male's territory. We could not alter male plumage color more permanently without destroying the insulating properties of their feathers, so the experiment was terminated.
Phenology
To help understand why plumage characteristics of males and females
changed, we also quantified snow melt and clutch initiation each year. Snow
cover on the whole study area was estimated by eye to the nearest 5% every
day. Clutch initiation was determined (1) by direct observation at 2-7 nests
each year, (2) by estimation for clutches found during egg-laying or
incubation, or (3) by using daily observations of female behavior to estimate
the date of clutch initiation of females whose nests were not found. When they
begin laying eggs, females are more wary, have almost completed their molt
into summer plumage (Figure 1b) and spend little time with their mates. As a result, they are much harder to
find (Montgomerie R, Lyon B, and Holder K, personal observations) and their
apparent disappearance from their territories, where they are almost always
visible before clutch initiation, is an excellent sign that egg-laying has
begun (Montgomerie R, unpublished data). To estimate the beginning of egg
laying, we assumed that the clutch size was nine, that one egg was laid each
day and that the incubation period was 21 days (see
Holder and Montgomerie, 1993).
Though rock ptarmigan raise only one brood each year, females will lay a
second clutch if their first clutch is destroyed during egg-laying or early in
the incubation period (Holder and
Montgomerie, 1993). We rarely recorded such clutch replacement but
we use data only for first clutches here.
Behavioral characteristics
During time budget observations, we recorded the substrate that the bird
was on (sentinel rock, ground, or snow) to determine whether the birds tended
to stay on the substrate that best matched their plumage. Sentinel rocks were
large boulders (up to 5 m3) scattered about the tundra;
"ground" refers to snow-free tundra that might be vegetated,
stones, gravel, or just bare soil. Time budget data were typically collected
in the course of other research by watching focal birds for up to several
hours at a time and recording the amount of time spent in different activities
(e.g., Brodsky, 1988;
Brodsky and Montgomerie,
1987).
In 1987-1993, we scanned for ptarmigan by eye during daily censuses across
the study area and recorded the distance (to the nearest 10 m) at which a male
was first sighted, his dirt score, and his identity (from color bands).
Distances were log-transformed to normalize distributions. A similar approach
to quantifying conspicuousness, based on the distance that an individual is
first detected by eye, has recently been used in a study of reef fishes
(Warner and Dill, 2000).
Because it has been suggested that male conspicuousness might deflect
predator attention away from the female
(Huxley, 1938), we conducted a
simple experiment in 1984 on 10 pairs to determine male reaction to the
approach of a predator. Humans have probably been a major predator of
ptarmigan, at least near human habitation, since humans first settled on
tundra regions (see Discussion) but our intention was to use humans as a
general predator model as has been done in most studies of nest defense
(Montgomerie and Weatherhead,
1988). Whenever a pair was sighted from more than 500 m during the
2-week period before egg-laying began (5-17 June), one of us walked slowly
toward the pair while another observer recorded when and how the male moved
with respect to the female's location (fly or walk; toward or away from the
female). We chose only birds that were clearly paired (i.e., had been seen
together often for at least 3 days) and within 50 m of each other when first
sighted. We analyzed data from only the first trial on each pair to minimize
any effects of habituation.
Statistical analyses
All variables in analyses of variance (ANOVA) were checked for normality
and equality of variances and transformed to meet those assumptions when
necessary. We used repeated measures ANOVAs to minimize the effects of
pseudoreplication in the analysis of detection distances when marked
individuals were sighted more than once, even in different years. Unmarked
individuals were all considered to be the same individual in these analyses.
In constructing ANOVA models we removed nonsignificant terms from the analyses
reported here.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Conspicuousness and crypsis in rock ptarmigan are influenced by changes in plumage and background (Figure 1), and differ between the sexes in spring due to divergent molting schedules (Figure 2). Thus, males become conspicuous in a unique way—due to a change in background (Figure 1c) rather than a change in plumage. Females molt during the males' courtship and territory establishment phase, where males delay extensive body molt until well after females begin incubation (Figure 2). In a typical year, female molt occurs during snow melt, whereas males delay body molt until the tundra is virtually free of snow (Figure 2).
|
Despite the delay in molt, male plumage does not remain immaculate. About 10 days after females begin molting, males alter their appearance by increasingly soiling their plumage (Figures 1d and 2), presumably by bathing in dirt and mud. We distinguish this plumage soiling behavior from the usual dust-bathing performed by ptarmigan and many other bird species because dust-bathing is used by birds to clean their plumage (see Discussion). Though we sometimes observed males actively dust-bathing during focal animal time budget studies, they spent very little time at this activity (usually only a few min per day) and never got dirty in the process. Unfortunately, we have never observed a male soiling his plumage in any way and can only assume that they actively bathe in muddy soil.
We observed males with dirty plumage in all years at all study sites except
Attu Island (see below), suggesting that male plumage soiling is a general
phenomenon in this species, at least in North America (see also
MacDonald, 1970;
Salomonsen, 1939, for
observations of dirty males at other sites). All males in our study population
at Sarcpa Lake soiled their plumage before their body molt began in every year
of our study.
By soiling their plumage, male ptarmigan greatly reduced their conspicuousness (Figure 1d). The distance that male ptarmigan were visible (i.e., first detected by us) on all substrates decreased significantly as dirtiness increased (repeated measures ANOVA: dirt score, F4,60 = 27.3, p <.0001; Figure 3) with no significant difference among substrates (F2,70 = 0.68, p =.51; score x substrate interaction, p =.69). To control for the potentially confounding effect of behavior on conspicuousness, we analyzed the 90 observations of 29 males seen foraging on the ground, and found the same pattern (F4,46 = 26.9, p <.0001). Moreover, the maximum distances at which males were first sighted (Figure 3) declined dramatically from 750 m to 300 m when the males first began dirtying their plumage (i.e., changed dirt score from 0 to 1). Mean first-sighting distances (Figure 3) eventually decreased more than 6-fold, from 138 to 22 m (least squares means from ANOVAs).
|
Given that dirty plumage reduces conspicuousness so dramatically, why do males soil their plumages so late? One possibility is that males cannot soil their plumage until sufficient snow melts to allow them access to dirt, but our data suggest otherwise. In the 8 years for which we observed the entire progress of snow melt, plumage soiling began 1-19 days (mean 9.6 days) after bare patches of ground first appeared (e.g., Figure 2). Thus the delay between the availability of dirt and plumage soiling was highly variable among years, with no significant correlation (r =.50, p =.20) between the first date of male plumage soiling and the first date that large bare patches of ground were visible (approximately 10% of the snow had melted). Though the sample size is small and the power of this analysis is low, this result suggests that plumage soiling is not related to the availability of dirt. Moreover, we show below that the timing of plumage soiling is variable among males within years and is much more closely related to the end of the period when females are fertilizable.
Another possibility is that males stay clean and white while females are molting because they spend most of their time on snow patches, where they would be cryptic, during the period of snow melt. However, after the snow began to melt, males with immaculate plumage (score 0) spent almost all of their time (96.4%, range 79-100% for 15 males) on bare ground and rocks, where they were highly conspicuous.
The failure of dirt availability or habitat selection to explain the timing of male dirtiness suggests that males delay dirtying their plumage to obtain some benefit from conspicuous plumage. Indeed, plumage soiling was closely associated with the timing of egg-laying by females. In all 4 years of intensive study (1983, 1987-1989), males began soiling their plumage within 1 or 2 days of females laying their first egg (Figure 4) and were maximally soiled 14-17 days later when clutches were complete and females no longer fertilizable.
|
In 1987-1989, the date that each mated male was last seen with a dirt score of 0 was significantly related to (r =.62, p =.003; analysis of means from 21 males) and, on average, 2.1 days (± 0.5 SE) later than the date his mate began egg-laying. To examine year and snow melt effects on this pattern we performed analyses of covariance (ANCOVA) on these data with clutch initiation date as the covariate. The beginning of plumage soiling (last day of score 0) was significantly related to the onset of egg-laying and year of study whether we consider each individual male-female pairing to be independent (ANCOVA: clutch initiation, F1,25 = 26.5, p <.0001; year, F1,25 = 16.6, p =.0004) or analyze mean values for each male across all years (ANCOVA: clutch initiation, F1,18 = 26.1, p <.0001; year, F1,18 = 12.1, p =.003). However the beginning of plumage soiling was not related to the timing of snow melt (analysis of pairs, F1,25 = 2.9, p =.10; analysis of means, F1,18 = 1.7, p =.21). Further support for a causal link between female fertility and male conspicuousness comes from data on two males who immediately cleaned their plumages from medium dirtiness (score 2) to immaculate (score 0) within 24 h of their mates losing their clutches to a predator (Figure 4), and presumably again being fertilizable (as at least one of these females did lay a second clutch).
Data from polygynous and bachelor males provide additional evidence that
the onset of plumage dirtying is related to female fertility. (Bachelors are
males that were never paired during a given breeding season.) If the timing of
dirtying is influenced by sexual selection, polygynous males should soil their
plumage later than monogamous males because polygynous males mate sequentially
(Brodsky, 1988) and thus have a
longer period of female fertility. In 1988, the year for which we had the most
data on both polygynous and monogamous males, polygynous males soiled their
plumage significantly later than monogamous males (repeated measures ANOVA,
F1,88 = 7.30, p =.015,
Figure 5), on average reaching
a dirt score of 2 about 4 days later. Similarly, bachelors should delay
plumage soiling since they do not have a partner and thus have extended mating
opportunities via extrapair copulations
(Brodsky, 1988). In 1983, the
year for which we had the most data on bachelor males, the average date that
bachelors reached a dirt score of 2 was 2 days later than that for mated
males, though the difference was not significant (t test, t
= 1.54, p =.15, n = 6 mated, 7 bachelor). Thus both bachelor
and polygynous males soiled their plumage later than would be expected if
dirtying was not related to female fertility (see Discussion).
|
Finally, our predator deflection experiment yielded results that do not provide strong support for the predator deflection hypothesis. In six of 10 pairs the male flew toward or stayed close to the female, and in four pairs the male flew or walked away. Though the initial response of four males was to move away from the female, three of these males returned within a few minutes and settled close to the female, thereby drawing our attention to the female's location.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
We have documented here an apparently unique process by which a male bird acquires a cryptic plumage when his conspicuous plumage no longer serves a reproductive function—by soiling the plumage rather than by molt. This accompanies a unique way, long known to biologists, that male rock ptarmigan become conspicuous in the first place as their habitat changes from white to brown while their plumage remains white. In this study, we quantified this conspicuousness in the field and we document how conspicuousness changes as the males soil their plumage.
Most previous studies of plumage conspicuousness have simply compared
pictures of birds and quantified relative conspicuousness to the observer on a
fairly subjective scale (Baker and Parker,
1979; Promislow et al.,
1992,
1994). However, Endler and
Théry
(1996) measured both the
colors and visual backgrounds of three lekking birds in the rainforest and
found that the birds' colors and behaviors maximized the amount of visual
contrast during their displays. More recently, Andersson et al.
(1998) measured the reflectance
spectra of both blue tit plumage and the microhabitats visited by the birds
and found that reflected light in the UV range contributed significantly to
conspicuousness. We have taken a different approach here by quantifying the
distance that live birds on the tundra could be detected by human observers.
Near human habitation in the arctic, humans are a major predator on ptarmigan
(Smith, 1991; Montgomerie R,
Lyon B, and Holder K, personal observations) and probably have been as long as
humans have inhabited tundra regions. Thus our method of measuring
conspicuousness is relevant to the risk of predation by humans. Birds of prey
and foxes are also important predators of adult ptarmigan in the breeding
season (see below). Immaculate ptarmigan would probably be detectable only at
shorter distances by foxes but at much farther distances by raptors, based on
their visual acuity compared to humans.
Plumage change by soiling rather than molting offers male ptarmigan the
opportunity to become relatively cryptic more quickly, with more flexible
timing than molt, and presumably at lower energy cost. Thus, by soiling their
plumage, males were able to become relatively cryptic within a few days, as
opposed to the 14 days required for females to molt from white to brown
plumage (Holder and Montgomerie,
1993). In early July, when there is no more opportunity for
breeding, males molt to their brown summer plumage over a 3-week period
(Holder and Montgomerie,
1993). Moreover, two males that we studied reversed their crypsis
quickly, by cleaning their plumage from dirty to immaculate within 1 day, when
their females lost their clutches (and presumably were again fertilizable), a
feat that would have been impossible for a molting male. It is not so
surprising that this behavior is probably unique among birds because few land
birds are white during periods of highest predation risk.
Among birds, a change in the color of existing plumage (rather than a
change in color by molt) has been reported in many waterfowl (e.g., snow
geese, Chen caerulescens) and cranes (e.g., sandhill crane, Grus
canadensis), in bearded vultures (Gypaetus barbatus) and in the
red knot (Calidris canutus). In waterfowl and cranes the reddish
stain on the heads and necks of many individuals is thought to be a passive
consequence of foraging in iron-rich water
(Höhn,
1955; Kennard,
1918). Bearded vultures, however, actively stain the feathers of
their underparts, head and neck by bathing in red soil and the degree of red
staining may serve as a status signal in intraspecific encounters
(Negro et al., 1999). Red
knots also change the color of their plumage at the beginning of the breeding
season, as a consequence of a change in the composition of their preening
waxes that causes their plumage to become more red when it is preened
(Piersma et al., 1999). Most
important, plumage redness seems to be a signal used during mate choice in
this species (Piersma et al.,
1999). Thus plumage coloring in bearded vultures and red knots may
serve a cosmetic function whereas in rock ptarmigan the function appears to be
camouflage.
Work done elsewhere on predation on ptarmigan during the breeding season
indicates that conspicuousness is costly for males. Indeed, gyrfalcons, a
major predator of rock ptarmigan, hunt them in a distinctive manner wherein
they spot their prey at some distance from a high altitude (200-400 m) then
drop low to the ground and approach their quarry less than a few meters over
the tundra, where they are less likely to be detected
(White and Weeden, 1966).
Ptarmigan mortality rates (due to falcon predation) during the breeding season
are exceptionally high and most of that predation is on males, which are more
conspicuous than females. In an 18-month study of 31 gyrfalcon territories in
Iceland, Nielsen and Cade
(1990) found that rock
ptarmigan constituted as much as 87% of the prey of these raptors during the
breeding season (depending on habitat) and comparable figures have been
reported from other regions (Bengston,
1971; Cotter et al.,
1992; Gardarsson,
1971,
1988;
Langvatn, 1977;
Poole and Boag, 1988;
Wayne and Jolly, 1958). Most
important, Icelandic gyrfalcons preyed mainly on males in white plumage in the
spring, up until the time when males stopped defending territories
(Nielsen, 1986;
Nielsen and Cade,
1990)—just when we observed them beginning to soil their
plumage. Over the entire breeding season, Cotter
(1991) found that gyrfalcons
were responsible for 95% of all predation on rock ptarmigan and that mortality
rates in June and July were 50% higher for males (22%) than females (14%).
Similarly in Iceland, Gardarsson
(1971) found that annual male
mortality rates (65%) were higher than those of females (47%) and, in
particular, that predation on males during their short (< 2 months)
breeding season was extremely high (33%). In that study, gyrfalcons were
responsible for all losses by predators and nine territorial males were
actually observed being taken by these raptors. It is abundantly clear that
breeding male rock ptarmigan suffer one of the highest predation rates ever
recorded for birds (e.g., higher than total annual male mortality listed for
any species in Promislow et al.,
1992,
1994). Thus, we would expect a
costly trait like white plumage, that makes a male so conspicuous, to confer
significant survival or mating advantages in order to be maintained by natural
or sexual selection.
A number of hypotheses can be formulated to explain both the conspicuousness of male rock ptarmigan in spring and their subsequent crypsis resulting from dirty plumage. We discuss each of these below in relation to the evidence that we have presented and data currently available on this species in the literature.
Hypotheses about plumage conspicuousness
Molting constraint hypotheses
While female rock ptarmigan molt to become camouflaged, males might remain
conspicuous because they are constrained by energy availability or hormones,
and not because conspicuous plumage serves an adaptive function. For example,
male flight song displays and territory defense are probably energetically
costly. Thus one might argue that male ptarmigan delay molt, which is also
thought to be energetically costly (Murphy
and King, 1992), until after females begin incubating. By waiting
until courtship and territorial defense are finished, males could devote more
time to foraging and more energy towards the molt.
Salomonsen (1950-1951) also
suggested that conspicuous male ptarmigan plumage may not serve an adaptive
function but rather may be the result of a hormonal constraint. Since
testosterone can act as an inhibitor to molting, Salomonsen argued that males
remain conspicuous simply because the spring surge in testosterone coincides
with (and triggers) male territoriality and aggression. Thus molting would be
inhibited until after testosterone titres subside (see also
Stokkan, 1979). An injection
of testosterone solution into a single male rock ptarmigan on Bathurst Island,
Nunavut, for example, did delay his molt out of white plumage by at least
three weeks compared to other males in the population
(MacDonald, 1970).
Despite the possibility that hormones and energy may constrain male molt, a constraint on molting cannot explain conspicuousness because males can quickly alter their conspicuousness by soiling their plumage, as we have shown, and the timing of such dirtying behavior appears to be quite flexible. Thus, if there were no particular advantage to conspicuousness males should soil their plumage at the same time that females become cryptic by molting.
Soil availability hypothesis
Although male ptarmigan are able to achieve crypsis by means other than
molting, perhaps there are temporal constraints on their ability to soil their
plumage. For example, since male rock ptarmigan do not begin to get dirty
until 2-4 weeks after the snow begins to melt off the tundra, the timing of
male dirtiness may simply be related to the availability of mud or dirt.
Though we could not monitor the dirtying properties of the soil on our study
areas, the tundra appears to dry out in parallel with the degree of snow melt.
As an indirect test of this hypothesis we found no consistency between the
average onset of male dirtiness and the timing of snow melt in 8 years of
study. Thus in some years the snow was 50% melted by late May where in other
years not until mid-June. In all of these years, however, the onset of male
dirtiness occurred within 2 days of the beginning of incubation by females,
when they were no longer fertilizable. Moreover, the onset of plumage soiling
by individual males within years was significantly correlated with the date of
clutch initiation by their mate. Thus the maintenance of a conspicuous plumage
is more likely to have an adaptive function than simply resulting from factors
that constrain a male's ability to soil his plumage.
Background matching hypothesis
Bright plumage could simply be the result of differential background
matching by males and females (Cott,
1940; Endler and
Théry, 1996). In many species
males and females occupy different microhabitats and even brightly colored
males may thus be difficult for predators to see. However, male rock ptarmigan
in conspicuous white plumage spent less than 5% of their time on snow, where
they would have been more cryptic, even when their territories were still
largely snow covered. We reject this background matching hypothesis because
males did not preferentially stay on white backgrounds matching their
plumage.
Unprofitable prey hypothesis
Baker and Parker (1979)
proposed that bright males might actually advertise to predators that they are
better able to escape than are females. This unprofitable prey hypothesis can
be rejected because conspicuous male ptarmigan suffer more predation than
inconspicuous females (Gardarsson and
Moss, 1970; Nielsen,
1986; Nielsen and Cade,
1990) and thus appear to be profitable for avian predators.
Predator deflection hypothesis
Huxley (1938), referring
specifically to ptarmigan, suggested that conspicuous males might deflect
predator attention away from females. Our data, however, show that mated males
did not consistently deflect the attention of humans away from their females,
as this hypothesis would predict. This experiment needs to be repeated with
(preferably trained) avian predators since these are the main cause of
mortality on breeding male ptarmigan, except near human habitation
(Montgomerie R, Lyon B, and Holder K, personal observations).
This hypothesis is also not supported by data from bachelors. Since
bachelor males spend so little time in the presence of females (only during
attempts to sneak onto other males' territories in pursuit of extrapair
copulations; Brodsky, 1988), an
immaculate plumage would serve little or no predator deflection function for
those females. Thus, bachelors would be expected to soil their plumage once
all females have settled on male territories (and were no longer available for
pairing, and predator deflection), at least 10 days before they actually did
become dirty. Indeed, bachelors soiled their plumage on average 2 days later
than paired males.
Sexual selection hypotheses
Two lines of evidence, both related to the timing of dirtiness in males,
support the idea that the conspicuous male rock ptarmigan plumage has evolved
via sexual selection. The strong correlation between the onset of male
dirtiness and the date of clutch initiation within pairs suggests that
conspicuous male plumage serves a reproductive function either through female
preference for immaculate males (mate choice) or through some advantage to
immaculate males in territorial defense (male-male competition). Differences
in the timing of plumage soiling between monogamous, polygynous and bachelor
males also suggest a role for sexual selection in the maintenance of
conspicuous plumage. Polygynous males soiled their plumage significantly later
than monogamous males as expected if males delay soiling their plumage until
their females begin egg-laying (Figure
5). Females settle with polygynous males sequentially
(Brodsky, 1988) so second and
third females should be fertilizable later than first females and females
mated to monogamous males. The mean difference of 4 days between the plumage
soiling of monogamous and polygynous males corresponds with our observations
of female settling patterns, which show a 2-4 days lag between successive
females settling with a given polygynous male (Montgomerie R, unpublished
data). Bachelor males also soiled their plumage slightly later than mated
males. Since bachelor males roam about seeking copulations with females mated
to other males (Brodsky, 1988),
such a delay soiling their plumage—until most females in the population
were no longer fertilizable (Figures
2 and
4)—would be expected if
conspicuousness was important for mate attraction.
If mate choice is the reason that male rock ptarmigan remain conspicuous,
why would females prefer to mate with males whose plumage is not molted or
soiled? Presumably immaculate plumage signals some aspect of male quality that
is useful to females. Since male rock ptarmigan do not participate directly in
parental care (Holder and Montgomerie,
1993), it is unlikely that females use male plumage as a signal of
parenting ability. However, immaculate male rock ptarmigan may honestly
advertise their ability to avoid predation. Low quality males, that for
whatever reason (health, poor condition, unwariness) need to become
inconspicuous to avoid predation, should therefore fail to obtain a mate.
Females could benefit from mating with a high quality male by passing his
genes on to her offspring (Andersson,
1994; Zahavi,
1975), by gaining some predator deflection advantage as discussed
above, or by obtaining a better territory for food and refuge from harassment
by other males seeking extrapair copulations. Mate choice experiments, though
difficult in this case, are clearly needed to determine whether females prefer
immaculate over soiled males.
Alternatively, male conspicuousness may reduce the energy costs of territorial defense by signaling over long distances and minimizing costly territorial intrusions and chases. Immaculate plumage certainly enhances the effectiveness of the male's plumage as a long-distance signal and thus may reduce intrusion and harassment from neighbors. Thus conspicuousness of territorial males could confer an advantage in male-male interactions, though it is difficult to apply this explanation to bachelors since they did not defend territories.
Interpopulation differences in molt patterns might also be instructive.
Molt data from a large number of populations worldwide (Greenland:
Salomonsen, 1939; Svalbard:
Steen and Unander, 1985;
France: Boudarel, 1988; Russia:
Dement'ev and Gladkov, 1967)
suggest that male rock ptarmigan typically maintain a conspicuous white
plumage in the spring, while females molt to crypsis. Only in Scotland
(Watson, 1973) and on the
Aleutian Islands, Alaska, USA (Murie,
1959), do males molt at roughly the same time as females. Thus,
for example, male rock ptarmigan on Attu Island molt as the snow melts and are
never highly conspicuous in spring, even though they are at that time just as
active, aggressive, courting and territorial as males in the other populations
we have studied (Montgomerie R and Holder K, unpublished data). On Attu, at
least, males do not soil their plumage, presumably because plumage soiling
would serve no function in making them less conspicuous since they have
already molted out of their white winter plumage. If male conspicuousness is
due to sexual selection then we would expect plumage conspicuousness (and also
plumage soiling) to be absent whenever predation rate is too high for males to
bear the cost or too low to make conspicuousness advantageous under sexual
selection (Andersson, 1994;
Zahavi, 1975). No quantitative
data are currently available to test these ideas but our own observations on
Attu Island suggest that the predation risk by avian predators there is
high.
Time constraint hypothesis
Correlates of the timing of male plumage change from conspicuous white to a
more cryptic dirty plumage provide strong support for a role of sexual
selection. However, males defending territories and courting/guarding females
might simply not have time to spend soiling their plumage. Thus the relation
between the timing of female egg-laying and plumage soiling by males could
reflect a time constraint whereby males have more time to soil their plumage
after their mate is no longer fertilizable. However, bachelor males soiled
their plumage slightly later than mated males even though they did not defend
territories and had no female(s) to guard. We have few time budget data on
these males because color-banded bachelors were not always easy to locate
(since they did not hold territories) but our limited data indicate that they
spent only a few min per day time intruding on the territories of mated males
(Brodsky and Montgomerie,
1987). While not intruding they foraged and slept and thus
apparently had plenty of time to soil their plumage if they could have
benefited from the reduced conspicuousness. In addition, our observations that
the plumage of territorial males changed from dirty to clean (1) for two males
when their females became newly fertilizable due to nest predation and (2) for
three other males whose plumage we experimentally soiled suggests that
immaculate plumage serves a useful function. In fact those males presumably
cleaned their plumage by dust-bathing and preening.
Hypotheses about plumage dirtiness
Why does male rock ptarmigan plumage become soiled at about the same time
as females are no longer sexually receptive?
Nonfunctional hypothesis
Plumage soiling could conceivably be a nonfunctional side effect of dust
bathing. While dust-bathing is common in gallinaceous birds
(Johnsgard, 1973), there is no
evidence that the plumage of any other species becomes noticeably soiled in
the process. Indeed, birds engage in dust-bathing to remove oils and possibly
ectoparasites from their plumage and reduce feather damage. The removal of
oils thus cleans plumage rather than making it dirty
(van Liere and Bokma, 1987).
Consequently, the soiling of plumage via dust-bathing would itself be unusual
in birds and it appears as though male rock ptarmigan actively stain and soil
their plumage rather than dust-bathing, as suggested for the plumage staining
of bearded vultures (Negro et al.,
1999). If we assume that male rock ptarmigan get dirty in the
course of normal dust-bathing then both the timing and the degree of plumage
dirtiness require explanation.
Camouflage hypothesis
It seems clear that plumage dirtiness in male rock ptarmigan serves the
adaptive function of camouflage. In this study we have documented that dirty
males are indeed more cryptic—at least to human predators—than
immaculate males. We also know that breeding male rock ptarmigan suffer one of
the highest daily mortality rates known in birds. Further research should be
directed at comparing the daily mortality rates of dirty and clean males.
Polygynous males might also be expected to suffer higher mortality rates due
their prolonged conspicuousness. Assuming that predation risk and
conspicuousness are highly correlated, as has been found in comparative
studies (Promislow et al.,
1992,
1994) and assumed in most work
on plumage conspicuousness (e.g., Baker and
Parker, 1979), then it is likely that dirty plumage does reduce
the risk of predation.
Conclusions
Based on the data and arguments presented here, we conclude that the
conspicuous plumage of male rock ptarmigan is a product of sexual selection
that favors the retention of immaculate (and at the time, cryptic) winter
plumage after the snow melts and the birds become highly conspicuous on the
tundra. Whether the mechanism of sexual selection is (1) female choice for
males who are better able to avoid (honest advertisement hypothesis) or
deflect (predator deflection hypothesis) predators, or (2) male-male
competition (territory advertisement and defense) is an open question that is
best addressed by some critical experiments. For example, it would be most
informative to experimentally manipulate male plumages at a site where
predation is high (e.g., Iceland, Bengston,
1971; Nielsen and Cade,
1990) and then examine the effects of plumage change on male
behavior, predation rates, and female choice. Like many problems in sexual
selection, it seems likely that plumage conspicuousness in male rock ptarmigan
will have more than one explanation, so the challenge will be to determine the
relative importance of different mechanisms in the evolution of this
trait.
|
ACKNOWLEDGEMENTS |
|---|
We are grateful to numerous colleagues and field assistants for help with the fieldwork but especially Lynn Brodsky, Ralph Cartar, Rob McLaughlin, Tarmo Poldmaa, and Mary Reid. We also thank Peter Grant, Kathy Martin, Pat Weatherhead, and George Williams for useful discussion. We are particularly grateful to both anonymous reviewers and Ron Ydenberg for insightful comments on the manuscript that helped us to focus our interpretation of findings more clearly. This work was supported by research and equipment grants from the Natural Sciences and Engineering Research Council of Canada (to R.M.) and Northern Scientific Training Grants from the Canada Department of Indian and Northern Affairs (to B.L. and K.H.).
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Andersson M, 1983. On the function of conspicuous seasonal plumages in birds. Anim Behav 31: 1262-1263.[Web of Science]
Andersson M, 1994. Sexual selection. Princeton, New Jersey: Princeton University Press.
Andersson S, Örnborg J, Andersson M,
1998. Ultraviolet sexual dimorphism and assortative mating in
blue tits. Proc R Soc Lond B 265:
445-450.
Baker RR, Parker GA, 1979. The evolution of bird coloration. Phil Trans R Soc B 287: 63-130.
Bengston SA, 1971. Hunting methods and choice of prey of gyrfalcons Falco rusticola at Myvatn in northeast Iceland. Ibis 113: 468-476.[Web of Science]
Bergerud AT, 1988. Mating systems in grouse. In: Adaptive strategies and population ecology of northern grouse (Bergerud AT, Gratson MW, eds). Minneapolis: University of Minnesota Press; 439-472.
Boudarel P, 1988. Recherche sur l'habitat et le comportement spatial du lagopede alpin (Lagopus mutus) dans les Pyrenées-Occidentales francaises. Gibier faune sauvage 5: 227-254.
Brodsky LM, 1988. Mating tactics of male rock ptarmigan (Lagopus mutus): a conditional mating strategy. Anim Behav 36: 335-342.
Brodsky LM, Montgomerie RD, 1987. Asymmetrical contests in defence of rock ptarmigan territories. Behav Ecol Sociobiol 21: 267-272.
Butcher GS, Rohwer S, 1988. The evolution of conspicuous and distinctive coloration for communication in birds. In: Current ornithology (Power DM, ed). New York: Plenum Press; 51-108.
Cade TJ, 1960. Ecology of the peregrine and gyrfalcon populations in Alaska. Univ Cal Publ Zool 63: 151-290.
Cott H, 1940. Adaptive coloration of animals. London: Methuen.
Cotter R, 1991. Population attributes and reproductive biology of rock ptarmigan (Lagopus mutus) in the central Canadian arctic (MSc thesis). Edmonton: University of Alberta.
Cotter RC, Boag DA, Shank CC, 1992. Raptor predation on rock ptarmigan (Lagopus mutus) in the central Canadian arctic. J Raptor Res 26: 146-151.
Darwin C, 1871. The descent of man, and selection in relation to sex. London: John Murray.
Dement'ev GP, Gladkov NA, 1967. Birds of the Soviet Union. Jerusalem: Israel Program for Scientific Translations.
Endler JA, Théry M, 1996. Interacting effects of lek placement, display behavior, ambient light, and color patterns in three neotropical forest-dwelling birds. Am Nat 148: 421-452.[Web of Science]
Gardarsson A, 1971. Food ecology and spacing behavior of rock ptarmigan Lagopus mutus in Iceland (PhD dissertation). Berkeley: University of California.
Gardarsson A, 1988. Cyclic population changes and some related events in rock ptarmigan in Iceland. In: Adaptive strategies and population ecology of northern grouse (Bergerud AT, Gratson MW, eds). Minneapolis: University of Minnesota Press; 465-519.
Gardarsson A, Moss R, 1970. Selection of food by Icelandic ptarmigan in relation to its availability and nutritive value. In: Animal populations in relation to their food resources (Watson A, ed). Oxford: Oxford University Press; 47-71.
Götmark F, Hohlfält A, 1995. Bright male plumage and predation risk in passerine birds: are males easier to detect than females? Oikos 74: 475-484.[Web of Science]
Höhn EO, 1955. Evidence of iron staining as the cause of rusty discoloration of normally white feathers in Anserine birds. Auk 72: 414.
Holder K, Montgomerie R, 1993. Rock ptarmigan (Lagopus mutus). In: The birds of North America (Poole A, Gill F, eds). Philadelphia: Academy National Science; 1-24.
Holder K, Montgomerie R, Friesen V, 1999. A test of the glacial refugium hypothesis using patterns of mitochondrial and nuclear DNA sequence variation in rock ptarmigan (Lagopus mutus). Evolution 53: 1936-1950.[Web of Science]
Huxley JS, 1938. Darwin's theory of sexual selection and the data subsumed by it, in the light of recent research. Am Nat 72: 416-433.[Web of Science]
Johnsgard PA, 1973. Grouse and quails of North America. Lincoln: University of Nebraska Press.
Kennard F, 1918. Ferruginous stains on waterfowl. Auk 35: 123-132.
Langvatn R, 1977. Characteristics and relative occurrence of remmants of prey found at nesting places of gyrfalcon Falco rusticolus. Ornis Scand 8: 113-125.
MacDonald SD, 1970. The breeding behavior of the rock ptarmigan. Living Bird 9: 195-238.
Montgomerie RD, Cartar RD, McLaughlin RL, Lyon B, 1983. Birds of Sarcpa Lake, Melville Peninsula, Northwest Territories: breeding phenologies, densities and biogeography. Arctic 36: 65-75.
Montgomerie RD, Weatherhead PJ, 1988. Risks and rewards of nest defense by parent birds. Q Rev Biol 63: 167-187.[Web of Science]
Murie OJ, 1959. Fauna of the Aleutian Islands and Alaska Peninsula. North Am Fauna 61: 1-406.
Murphy ME, King JR, 1992. Energy and nutrient use during molt by White-crowned Sparrows Zonotrichia leucrophrys gambelii. Ornis Scand 23: 304-313.
Negro J, Margalida A, Hiraldo F, Heredia R, 1999. The function of the cosmetic coloration of bearded vultures: when art imitates life. Anim Behav 58: F14-F17.[Medline]
Nielsen ÓK, 1986. Population ecology of the gyrfalcon in Iceland with comparative notes on the merlin and the raven (PhD thesis). Cornell: Cornell University.
Nielsen ÓK, Cade TJ, 1990. Seasonal changes in food habits of Gyrfalcons in NE-Iceland. Ornis Scand 21: 202-211.
Olpinski SC, 1986. Breeding ecology, habitat and morphometrics of rock ptarmigan Lagopus mutus L. in Nouveau-Québec (MSc thesis). Montréal: McGill University.
Piersma T, Dekker M, Damsté JSS, 1999. An avian equivalent of makeup? Ecol Letters 2: 201-203.
Poole KG, Boag DA, 1988. Ecology of gyrfalcons, Falco rusticola, in the central Canadian Arctic: diet and feeding behaviour. Can J Zool 66: 334-344.
Promislow DEL, Montgomerie R, Martin TE, 1992.
Mortality costs of sexual dimorphism in birds. Proc R Soc Lond
B 250:
143-150.
Promislow DEL, Montgomerie R, Martin TE, 1994. Sexual selection and survival in North American waterfowl. Evolution 48: 2045-2050.[Web of Science]
Salomonsen F, 1939. Molts and sequence of plumages in the rock ptarmigan (Lagopus mutus (Montin)). Copenhagen: P. Haase & Son.
Salomonsen F, 1950-1951. The birds of Greenland. Copenhagen: Ejnar Munksgaard.
Smith E, 1991. Inujjuamiut foraging strategies: evolutionary ecology of an arctic hunting economy. New York: Aldine de Gruyter.
Steen JB, Unander, S, 1985. Breeding biology of the Svalbard rock ptarmigan Lagopus mutus hyperboreus. Ornis Scand 16: 191-197.
Stokkan K-A, 1979. Testosterone and daylength-dependent development of comb size and breeding plumage of male willow ptarmigan (Lagopus lagopus lagopus). Auk 96: 106-115.[Web of Science]
van Liere D, Bokma S, 1987. Short-term feather maintenance as a function of dust-bathing in hens. Appl Anim Behav Sci 18: 197-204.
Warner RR, Dill LM, 2000. Courtship displays and
coloration as indicators of safety rather than of male quality: the safety
assurance hypothesis. Behav Ecol 11:
444-451.
Watson A, 1973. Molts of wild Scottish ptarmigan, Lagopus mutus, in relation to sex, climate and status. J Zool Lond 171: 207-223.
Wayne P, Jolly GF, 1958. Notes on the breeding of the Iceland gyrfalcon. Brit Birds 51: 285-290.
White CM, Weeden RB, 1966. Hunting methods of gyrfalcons and behavior of their prey (ptarmigan). Condor 68: 517-519.[Web of Science]
Zahavi A, 1975. Mate selection: a selection for a handicap. J Theor Biol 53: 205-214.[Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  T. Caro Contrasting coloration in terrestrial mammals Phil Trans R Soc B, February 27, 2009; 364(1516): 537 - 548. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Delhey, A. Peters, A. Johnsen, and B. Kempenaers Seasonal changes in blue tit crown color: do they signal individual quality? Behav. Ecol., September 1, 2006; 17(5): 790 - 798. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Blanco, O. Frias, J. Garrido-Fernandez, and D. Hornero-Mendez Environmental-induced acquisition of nuptial plumage expression: a role of denaturation of feather carotenoproteins? Proc R Soc B, September 22, 2005; 272(1575): 1893 - 1900. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||