Variation in Carotenoid-Based Color in Northern Flickers in a Hybrid Zone

8 Pages·2002·6.1 MB·English

by  Karen L Wiebe

Wilson Bull., 114(3), 2002, pp. 393^00
VARIATION IN CAROTENOID-BASED COLOR IN NORTHERN
FLICKERS IN A HYBRID ZONE
KAREN L. WIEBE' 2 AND GARY R. BORTOLOTTI'
—
ABSTRACT. We studied variation in the carotenoid color of flight feathers of hybrid Northern Flickers
{Colaptes auratus) and its correlation with reproductive performance and survival. Color scores provided by a
digital camerarevealed in 218 individuals acontinuous spectrum from yellow to red. Males tended tobe slightly
redder than females. Within individuals, an analysis of color change with age revealed that males, but not
females, became redder with age. Except for yearling females, body condition did not improve with age, sug-
gesting that coloris not linked to body condition measuredduring incubation. We did notdetect anycorrelations
between feather color and measures of reproductive performance, such as clutch size, hatching success, or
fledging success, or return rate to the study area. In a hybrid population where intraspecific variation in color is
controlled partly by genes, hue or brightness may not be a useful signal ofindividual quality, contrary to other
studies ofbirds. About 25% offlickers had one or more tail feathers that differed from the rest ofthe plumage.
In each case, the “odd” feathers were paler or yellower in color and may have been caused by diet or stress
when the feathers were lost and regrown during winter. Such odd colors support the hypothesis that red carot-
enoid pigments are costly to maintain under stressful conditions. Received25January 2002, accepted5August
2002.
“The flicker situation will puzzle all the intrapopulation plumage variation in the
naturalists in the world” (Audubon 1843:71). Northern Flicker {Colaptes auratus), a wood-
pecker with extensive and conspicuous carot-
Documentation ofvariation in plumage col-
enoid pigmentation on the undersides of the
or, whether across a species’ range or within flight feathers of both the wing and tail. Two
a population, has been the foundation for
subspecies (formerly species) are recognized:
many subdisciplines in ornithology. Trends in
C. auratus auratus, the Yellow-shafted Flicker
coloration are the raw material in avian sys-
of eastern North America and the Great
tematics, allow us to describe the demography
of populations, and more recently in behav- Plains, and C. a. cafer, the Red-shafted Flick-
ioral ecology, reveal the power of sexual se- er of western North America. As the common
lection in shaping bird morphology (Hill names suggest, the color of flight feathers is
1991, Gray 1996). In general, males are more yellow or red and has a genetic basis (Short
brightly colored than females, and juveniles 1965, Moore 1995). The two subspecies
have a drab appearance compared to adults groups hybridize along a zone extending
(Butcher and Rohwer 1989). Bright colors in along the Rocky Mountains from Texas to
birds may function in numerous ways as sig- Alaska; birds with an intermediate feathercol-
nals to conspecifics or predators (reviews in or, shades of orange, are identified as hybrids
Burtt 1981, Butcher and Rohwer 1989, Savalli (Moore 1995, Wiebe 2000).
1995, Fitzpatrick 1998). Of particular interest The bright colors of the flight feathers of
in recent years are the bright yellows, oranges, the Yellow-shafted Flicker are derived from
and reds, so common in the feathers of birds, three carotenoids that are absorbed untrans-
that are a product of carotenoids. These pig- formed from the diet: lutein, zeaxanthin, and
ments are of such interest because the same (3-cryptoxanthin. In contrast, the colors of the
molecules have a variety of important physi- Red-shafted Flicker are derived from oxida-
ological functions related to the health ofbirds tion of ingested carotenoids such that the pre-
(see Lozano 1994, Olsen and Owens 1998, dominant pigments are astaxanthin, adoniru-
Moller et al. 2000). In this paper, we examine bin, a-doradexanthin, and canthaxanthin
(Stradi 1998). In a previous study (Wiebe and
Bortolotti 2001), we examined the frequency
too'n,DepStK, Sof7NBi5oEl2o,gyC,anUanidva.. of Saskatchewan, Saska- ofyellow-orange-red color morphs in a hybrid
2Corresponding author; E-mail: population by using color scores from a digital
[email protected] camera.
393
394 THE WILSON BULLETIN • Vol. 114, No. 3, September 2002
Relationships between color and individual 1999 from the time they arrived on territories during
traits have not been examined in flickers; late April until the young fledged during late July. Po-
however, the potential role of color in com- tential territories and peripheral regions were searched
intensively every 2-3 days during spring using tape-
munication is suggested by ritualized displays recordedcalls. Becausethe habitatwasfairlyopenand
during which both males and females fan their flickers were responsivetothetapes, webelievenearly
wings and tails and expose the colored under- all nesting birds were located. We also trapped most
sides of their flight feathers in exaggerated birds each year (see below) to estimate return rates.
motions (Moore 1995). The display may be During 1998, 111 breeding adults were banded, of
directed either to a member of the same sex, which 36 returned in 1999. As we detected only one
bird from 1998 in 2000 but not in 1999, we are con-
in which case it probably is agonistic, or to fident that we detected most color-bandedbirds (36/37
the opposite sex, in which case it may func- = 97%) ifthey returned and therefore our return rates
tion in mate choice. Thus, it is not implausible are an accurate measure of local survival.
that color variation may be used to select an Adultflickersweretrappedatthenesteitherbystuff-
appropriate mate either with regard to species, ing the nest hole during incubation, orby pulling anet
olarttienrscealseec,tiiotnisofpraehdiicgthedqutahlaittycopalrotrnemra.yInctohre- oinnevgsetr(isntehgeeaWhdouilletebseweiatachnhdaynSewaarit,fttaacn2hd0e0dt1h)se.trreiWniegsdntuorrairpnepgaesdborn>ot9ood6tr%heianork-f
relate with traits such as age and body con- trapping success was biasedaccordingtoplumagecol-
dition. or. Flickers were aged as 1, 2, or 3 years old by molt
In a hybrid zone, correlations between color of upper primary coverts (Pyle et al. 1997) but for
and reproductive success are especially inter- some analyses we used two age classes by combining
esting. If a wide range of color variation is all birds >2 years as “adults.” We entered six body
cboentaroploloerdsbiygnaglenoefsaigneaorhyebxrpiedrieznocnee., Oitnmtahye tpsairrzisenucsmi,peaaclseunctroremamlpeonrnteecstn,rtibsxi,lalanlnaeldnygsntiihsn,tahbnildplrudisempeatdrhy,thwleeinfngigrtshtc,hcoiornmd-,a
other hand, if the fitness of hybrids is higher ponent(PCI asameasureofoverallbody size(Rising
)
or lower than parental types in the hybrid and Somers 1989). Because ofsexual dimorphism, we
zone, color could be an excellent indicator of performed separate analyses for each sex and made
potential fitness. The leading hypothesis for PCI values positive by scaling them to a hypothetical
the stability of the hybrid zone in flickers is individual of zero size (Bortolotti and Iko 1992). The
third rectrix on the right side was collected from each
tthyapteshyinbrithdes hhyabvreidhziognheer(Mhtonoerses atnhdanBupcuhr-e asdauvletdfilnicakerpawpherenenivtewlaospetrtaopbpeedphinotMoagryapohreJdunleat,era.nIdf
anan 1985). Therefore, orange flickers should the individual had multiple colors in its tail, we col-
have greater success than yellow or red birds lected two feathers.
—
there. Despite potential fitness differences Determining color. Quantifying subtle variation in
among flickers of different colors related to feathercolorisdifficultbecauseobservers’ perceptions
their genetic makeup, most previous studies depend upon the context, the degree of illumination,
and individual differences (Endler 1990). Previous
have failed to detect mate choice according to
studiesofflickersubspeciesrankedthecoloroffeather
color (Bock 1971, Moore 1987, but see Wiebe shafts and vanes into 3-5 categories (Short 1965,Bock
2000). In this paper, our aim is not to test the 1971), or named the feather vane color according to
function of color, but to examine proximate standardized color chips (Test 1940). Such categories
correlates of color variation such as age, sex, are too coarse for many questions. In a previous paper
body condition, reproductive success, and re- (Wiebe and Bortolotti 2001), we used a digital camera
turn rates of adults. It is our hope that this tNoegmreoasu1r99e8)c.oloAroNnikaonconCtoionlupoiuxsEs9ca0l0es(Vdiilgliatafluerctaemearnda
baseline information will be useful in future was u.sed to photograph each rectrix. Wephotographed
studies that may focus on the adaptive signif- all feathers during November 1999 alongside twogray
icance of color variation in Northern Flickers. scale reference cards so that we could adjust colors to
METHODS cNoengtrrool1f9o9r8)d.ifAflertehnocuegshinthiellcuammienrataiodnid(Vnioltlarfeuceorrtde UanVd
Study site and field methods.—The study area near reflectance, we do not believe this was aseriousdraw-
Riske Creek, in central British Columbia (51°52' N, back as carotenoids reflect light mainly in the visible
e1r2s2,°e2n1c'oWmp)aswsitehdinaptpherohxyibmraitdelzyon7e5ofkmN^orotfhegrrnasEslliacnkd- rpaencgkee,ra{nDdenrdedrotcaiolpcuosvemratjsoro)ftdhiedGnroetatshSopwottUeVd Wreofoledc--
with scatteredpatchesoftremblingaspen{Popidustre- tance (Burkhardt 1989).
muloides) and mixedconiferousforest (MartinandEa- Toderive a singlecolorvariable, weplottedfeathers
die 1999). Flickers were observed during 1998 and on the red and blue brightness axes provided by the
Wiehe and Bortolotti • FLICKER PLUMAGE COLOR 395
camera. That scatter plot revealed that a single axis
(e.g., the “red” axis) was not sufficient to distinguish
color hues perceived by us. Rather, color hues were
segregated in tight diagonal bands across both axes.
We used the reduced major axis technique to fit a re-
gression line through the median red and blue values
and then usedresidualsfromthisregressionasthe new
single color variable (Wiebe and Bortolotti 2001).
These color residuals corresponded well to a scale of
paint chips ranked from yellow through orange and
red; higher residuals indicated more reddish feathers
and lower residuals indicated yellow hues. Wiebe and
Bortolotti (2001) also confirmed that feather hues as
ranked by human test subjects matched the ranking of 25
the feather color residuals as calculated by us.
—
Statistical analyses. We analyzed body size be-
causethe Red-shafted Flickerwasreportedtobelarger
than the yellow-shafted subspecies (Moore 1995) and
also because body size may influence social domi-
nance and territory acquisition, and therefore quality
of the individual. As an index of body condition, we
used the residuals of a reduced major axis regression
ofbody mass on PCI (Green 2001). We recaptured27
flickers during 1998 and 1999. To avoid pseudorepli-
cation in analyses involving color frequencies and re-
productive performance, we randomly chose one ob-
-.375 -.325-.275 -.225 -.175-.125-.075 -.025 .025 .075 .125 .175
servation perindividual in the datasetexcept whenan- Vane color
alyzing within individual variation. Foranalyses ofre-
turn rates and changes in body condition within FIG. 1. Distribution of color scores in the hybrid
individuals between years, recaptured birds from 2000 flicker population at Riske Creek, British Columbia,
were included. We performed statistical analysesusing 1998-2000, as determined with a digital camera.
SPSS, andalltestsweretwotailed. Meansarereported Maleswere redderthanfemalesas shownbythegreat-
± SE. InitialANOVAmodelsincludedallhigherorder er frequency ofhigher (positive) color scores.
interaction terms, but in order to increase powerthese
were dropped from the model if nonsignificant.
flight feathers that differed conspicuously in
RESULTS color from the majority of their rectrices and
primaries. In the tail, these odd feathers often
Not counting “odd” colored feathers but were shorter or stunted, but not more worn
including recaptures, we collected and pho- compared to other feathers, suggesting they
tographed 245 flicker tail feathers: 111 from had been lost and regrown after the normal
1998 and 133 from 1999. Using the reduced period of postbreeding molt during the fall.
dataset with one feather per individual, a One third ofthese odd feathers had a “washed
ANOVA
three-way revealed no signihcant ef- out” appearance, (i.e., pale pink or pale yel-
f(eacgtesof1-y3e;ar^2(,T21,32=i3 0=.560,.1P2,=P0=.570).7o2n) foeratahgeer lviobwr)a,ntbuhtue6,6%butofyoeldldowfeera.thTerhsewsehrifet sitinllcoolfora
color but a significant sex effect = 4.6, was sometimes extreme; “red-shafted” flick-
P = 0.032). After pooling years, males were ers could have a feather almost as yellow as
slightly more reddish {n = 107, mean color typical yellow-shafted C. a. auratus birds. In
residual = 0.0064 ± 0.01) than females {n = one case, a bird was bilaterally asymmetrical
111, mean color = -0.026 ± 0.01; Fig. 1). with one entire side of the tail red and the
For both sexes, the modal color in the popu- other yellow. Paired Mests confirmed that
lation was about 0.05, a dark orangish red (ap- such regrown feathers were significantly yel-
proximately the “Chrome Orange” of Smithe lower (r,5 = 4.13, P = 0.001; Fig. 2). Of 19
1975). birds with odd feathers that were trapped in
A fraction of individuals trapped during two consecutive years, only four 21%) had
(
spring during the two years (22% of 114 fe- odd feathers in both years, which was ex-
males and 25% of 105 males) had one ormore pected based on the overall frequency of odd
396 THE WILSON BULLETIN • VoL 114, No. 3, September2002
FIG. 2. The color ofodd feathers and typical feathers collected from an individual flicker’s tail at the same
time, Riske Creek, British Columbia, 1998-2000. A shift to yellowerhues in the odd, regrown feathers is shown
by points below the diagonal line.
feathers in the population. In these four indi- the population, simple correlations between
viduals, the odd feather in the tail was at a color and body condition at the population
different location each year. It also is clearthat level may have little value. Instead, we ana-
replacement feathers did not always grow in lyzed longitudinal changes in body condition
as a different color. Nine adults that were re- with age to test whether the increase in red-
trapped on the study area in July (i.e., after ness with age (see above) might be explained
their extracted tail feather had begun to re- by a proximate mechanism of an increase in
grow), had replacement feathers that were in- body condition. Including recapture data from
distinguishable to our eye from the older rec- 2000 and pooling all ages, body condition
trices. measured during incubation improved with
For age-related changes in color within in- age for females (paired-/29 = 2.83, P = 0.007)
dividuals, we used paired /-tests to compare but not males (paired-Zjg == 0.68, P = 0.58).
feathers of individuals trapped in both years. Thus, within each gender, any changes in
With all ages pooled, there was no significant body condition with age did not correspond
change in color with age for females (/,, = with an increase in redness with age.
0.29, P = 0.78; Fig. 3a) but a significant in- With respect to reproductive performance,
crease in redness for males — 2.92, P = color was not associated with clutch size (r^
0.014; Fig. 3b). This age effect was not simply = 0.05, n = 2\6, P = 0.54) in the hybrid
a product of a change in age class (i.e., from population and feather color was not related
sftiirlslt stiognsieficcoanndt wyehaer)n,oanslythmealreeslattiwoonsyheiaprswaosf tfoledtgheed n(ru,m=be0r.03o,f nne=stl2i\n2g,sPth=at0.e7v3e)n.tuTahlilry-
age and older were analyzed (/^ = 2.4, P = ty-six of 1 1 1 (32%) individuals examined in
0.044). The degree of color change with age 1998 returned to the study area in 1999, and
(mean difference in residual = 0.045 ± 0.06) 41 of 134 (31%) from 1999 returned the sub-
wwiatshnootddasremgarrokwend afseatthheersdif(fmeeraenncedsififnecreonlcoer sniefqiuceannttlyyeabre.twReeteunrnyeraartses(dy^iid n=ot0d.i1f0f,erPsig=-
0.14 ± 0.13; compare Figs. 2 and 3). 0.83) or between sexes (x^i = 1.4, P = 0.27).
Color was not associated with our measures Color did not differ significantly between
of individual quality. There was no associa- b=irds thPat-returned and those that did not (/243
tion between PC1 and feather color for either 1.1, 0.23).
males (r = 0.03, n = 107, P - 0.75) or fe- DISCUSSION
males (r = —0.02, n = 1 1 1, P = 0.82). Be- Color in relation to age and sex.—Unlike
cause color extremes had a genetic basis in many species of birds that have bright plum-
Wiehe and Bortolotti • FLICKER PLUMAGE COLOR 397
flickers in the Held based on color. Villafuerte
and Negro (1998) also found a subtle differ-
ence between the brightness of captive male
and female Red-legged Partridges (Alectoris
rufa) that was revealed only by a digital cam-
A
era. sex difference in age-related carotenoid
coloration also has been reported for Ameri-
can Kestrels (Falco spar\’eriiis\ Bortolotti et
al. 1996).
Color variation and reproductive perfor-
—
mance. Subtle variation in color within an
age class or sex is of interest because it may
indicate a bird’s quality as measured by body
condition, immunocompetence, or survivor-
ship (Hill and Montgomerie 1994, Bortolotti
et al. 1996, Nolan et al. 1998, Hill 2000, Lind-
strom and Lundstrom 2000, Horak et al.
2001). We did not find any evidence that body
condition, reproductive output, or return rate
varied along the color spectrum in a hybrid
flicker population. In contrast to our results,
redder male Northern Cardinals (Cardinalis
cardinalis) obtained higher quality territories
and produced more offspring than paler males
(Wolfenbarger 1999). Redder male House
Finches (Carpodacus rnexicanus) had higher
provisioning rates to nestlings and higher sur-
vival (Hill 1991, Nolan et al. 1998). However,
the genetic basis of color variation in this hy-
FIG. 3. A longitudinalcomparisonoffeathercolor brid population complicates the analysis and
in Northern Flickers as they age from one year to the interpretation of potential relationships with
next, Riske Creek, British Columbia, 1998-2000. Cir-
cles indicate yearlings and triangles indicate birds >2 condition. While it still is plausible that flick-
years old. The feathers of males but not females be- ers within the core range of the pure subspe-
came redder with age as shown by the position above cies may show subtle variation in color that
the diagonal line. functions in social situations (e.g., mate
choice), the reliability of color as an honest
signal ofquality may have been compromised
age (Butcher and Rohwer 1989, Gray 1996, in the hybrid zone.
Badyaev and Hill 2000), carotenoid-based The second aspect ofcolor that complicates
coloration in flickers does not play a major our analysis is that the variation we observed
role in variation with regard to age or sex. is unlike that of most populations of birds. In
Instead, the melanin-based malar stripe is im- other species, the size of the carotenoid-based
portant for sex recognition (Noble 1936). The color patch (Hill 1993) or the intensity of hue
brighter red score of males in our population along a gradient of dull to bright (Bortolotti
of hybrids (Fig. 1) could be merely the result et al. 1996, Wolfenbarger 1999) is quantified.
of different proportions of individuals ofeach In such studies, brighter birds likely had more
sex along the hybrid continuum, rather than a circulating carotenoids, which in turn may ex-
difference related to the biology of the sexes. plain why there was a correlation between col-
The fact that only males became redder with or and health (Lozano 1994). In contrast,
age (Fig. 3) may explain how the difference flickers varied along a continuum of hues
arose in mean coloration between the sexes. from bright yellow to bright red, displaying
However, the relatively subtle shifts in color different, but not necessarily more, caroten-
with age means that it is not possible to age oids. Instead, our find of yellow odd feathers
398 THE WILSON BULLETIN • Vol. 114, No. 3, September2002
is consistent with the hypothesis that the ex- were deposited in feathers in a typical color
pression of red pigments per se is costly (Hill for the individual. Pale pink or pale yellow
1996, 2000). feathers also occur in nestling flickers, which
Regardless of any potential signaling func- often share the nest with normal, brightly col-
tions, the leading hypothesis about the flicker ored siblings. Such uniformly pale chicks of-
hybrid zone suggests there should be a rela- ten are the smallest of the brood (KLW pers.
tionship between color and reproductive per- obs.), but probably receive the same types of
formance (Moore and Buchanan 1985, Wiebe food items as bright siblings. Therefore, pale-
and Bortolotti 2001). However, we did not ness in nestlings appears to be caused by a
find support for the idea that intermediate phe- general lack of food and poor health rather
notypes performed better in terms of repro- than different dietary items. We can not rule
duction than parental types in the hybrid zone, out seasonal diet changes as a cause of pale
and return rates to the study area were not feathers in adults because the diet of flickers
associated with color. Similarly, with a smaller shifts from nearly 100% insect prey (ants)
sample size and categorical classification of during summer, to mainly fruits and seeds dur-
phenotypes, Moore and Koenig (1986) did not ing winter (Beal 1911, Test 1969). However,
detect differences in clutch size within a hy- many fruits contain abundant carotenoids
brid population in the central Unite—d States. (Gross 1987), so it is more probable that pale,
Causes ofodd-colored rectrices. In many regrown feathers indicate greater energetic or
species, the brightness of carotenoid colors physiological stress during winter.
may be influenced by a number of environ- It is more difficult to explain odd feathers
mental factors. Since birds must obtain carot- that were still bright, but yellower than nor-
enoid molecules from their food, and they mal. Red flickers grew odd bright yellow
grow pale feathers on artificial diets lacking feathers, but yellow birds never grew odd red
carotenoids (Brush 1978), different diets in feathers. Test (1969) also reported flickers
the wild have been implicated in intraspecific with mixed plumages but was not clear wheth-
variation (Slagsvold and Lifjeld 1985, Hill er these were red-shafted individuals growing
1992, Eeva et al. 1998). However, the idea yellow feathers or vice versa. It is well doc-
that carotenoids are limiting in the wild is umented that diverse avian taxa are capable of
controversial (Hudon 1994, Thompson et al. metabolic conversion of ingested carotenoids
1997, Bortolotti et al. 20()0). Instead, physio- into other forms (Goodwin 1984, Brush
logical capabilities to absorb and use carot- 1990). Red-shafted Flickers have a biochem-
enoids in the diet may be influenced by phys- ical pathway, probably lacking in yellow-
ical condition, stress, or degree of parasitism shafted individuals, which oxidizes yellow ca-
(Weber 1961, Thompson et al. 1997). Gender, rotenoid pigments into red ones (Stradi 1998).
age, and seasonality influenced circulating ca- Such biochemical pathways may be costly
rotenoids and color in American Kestrels even (Hudon 1991, review in Hill 1996) and the
when diet was controlled (Bortolotti et al. amount ofyellow carotenoids converted to red
1996, Negro et al. 1998). ones may depend upon a bird’s physical con-
Surprising to us was the high prevalence dition. For example, male Eurasian Bullfinch-
(nearly 25%) of flickers with odd colored es {Pyrr/uda pyrrhula) experimentally fed a
feathers in their wings or tail. Fading in sun- constant amount ofyellow pigments produced
light does not change the hue of flicker feath- brighter red feathers when given an energy
ers (Wiebe and Bortolotti 2001). Odd feathers rich diet (Schereschewsky 1929). If Red-
must be explained by differences in diet or shafted Flickers are energetically stressed dur-
physiology (or both) at the time the feathers ing winter, costly pigment conversion may be
were regrown compared to conditions during limited, causing feathers grown during winter
the normal period of postbreeding molt from to be yellower than normal. Test (1969) found
August to October. Feathers pulled in May that Red-shafted Flickers fed ground carrots
and examined in July matched the normal col- in captivity produced orange feathers. Psycho-
or of the other rectrices. This suggests that logical stress associated with being held in
there is a seasonal window, at least between captivity may reduce the expression of red
May and October, during which carotenoids pigment in birds even though carotenoid rich
Wiehe and Bortolotti • FLICKER PLUMAGE COL.OR 399
diets are provided (Weber 1961 cited in Hu- erius). Proc. R. Soc. Lond. B Biol. Sci. 267:1433-
don 1994). 1438.
Plumage color has been a basis for the clas- Brush, A. H. 1978. Avian pigmentation. Pp. 141—164
in Chemical zoology (A. H. Brush, Ed.). Academ-
sification of flicker subspecies, but our study ic Press, New York.
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nongenetic components to color variation. For ments in birds. Fed. Am. Sci. Exp. Biol. J. 4:
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ACKNOWLEDGMENTS Gray, D. A. 1996. Carotenoids and sexual dichroma-
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