Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2004? 2004
822
237248
Original Article
COLOUR POLYMORPHISM AND NICHE WIDTH IN BIRDS
P. GALEOTTI and D. RUBOLINI
Biological Journal of the Linnean Society, 2004, 82, 237–248. With 1 figure
The niche variation hypothesis and the evolution of
colour polymorphism in birds: a comparative study of
owls, nightjars and raptors
PAOLO GALEOTTI* and DIEGO RUBOLINI
Laboratorio di Eco-Etologia, Dipartimento di Biologia Animale, Università di Pavia, P.zza
Botta 9, 27100 Pavia, Italy
Received 1 September 2003; accepted for publication 22 December 2003
We studied the evolution of colour polymorphism in diurnal raptors, owls and nightjars, the avian taxa in which this
trait is most widespread, in relation to species ecological niche width and diet. Two main mechanisms have been put
forward to explain the maintenance of polymorphism, namely apostatic selection and disruptive selection. The niche
variation hypothesis states that species with broader ecological niches should be more variable compared with those
with narrow niches because of the action of disruptive selection; the apostatic selection hypothesis conversely suggests that intraspecific colour variation should be promoted in predators by prey forming an avoidance image for the
more common colour morph. Our aim was to determine if colour polymorphism occurrence was associated with broad
ecological niches as predicted by the niche variation hypothesis, or with predation on intelligent and sharp-sighted
prey as predicted by the avoidance image hypothesis. Pairwise comparisons were made between pairs of closely
related species differing in variables expected to influence the occurrence of polymorphism. We found that polymorphic species of all three groups showed wider and more continuous distribution ranges, frequented many different
habitats, both open and closed, and lived in seasonally alternating dry/wet climates. Polymorphic species were more
migratory compared with monomorphic ones, and they showed an activity pattern covering both day and night. Conversely, colour polymorphism was not higher in species preying on birds and mammals. All these findings support the
hypothesis that colour polymorphism evolved in bird species with wider niche breadth and not in species preying on
intelligent prey. Therefore, we propose that disruptive selection may be the main mechanism maintaining colour
polymorphism in these bird groups by favouring different morphs in different environmental conditions. © 2004
The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248.
ADDITIONAL KEYWORDS: apostatic selection – comparative method – disruptive selection – morphs – niche
width – plumage colour – speciation.
INTRODUCTION
Polymorphism in colour is a widespread phenomenon
in many animal taxa, and is defined as the coexistence
of two or more distinct and genetically determined
colour morphs in one interbreeding population (Huxley, 1955). Such intraspecific colour variation is independent of sex, age and season (Butcher & Rohwer,
1989), and evidence for birds suggests a strong genetic
control of colour morphs (e.g. Van Camp & Henny,
1975; Roulin, Richner & Ducrest, 1998; Krüger, Lindstrom & Amos, 2001; Roulin & Dijkstra, 2003). Following the seminal review by Huxley (1955), a number of
*Corresponding author. E-mail: [email protected]
papers have treated this topic in single avian species
or genera (see Galeotti et al., 2003 and references
therein). A comprehensive review of this phenomenon
in birds as a whole showed that colour polymorphism
is relatively rare, involving only 3.5% of species (Galeotti et al., 2003). However, 61% of the 23 bird orders
and 37% (53) of the 143 families contain polymorphic
species, and the occurrence of polymorphic species is
particularly high in Strigiformes, i.e. owls and nightjars (33.5%), Cuculiformes (12%), Galliformes (9.5%)
and Ciconiiformes (9%), particularly among diurnal
raptors. Small families such as Podargidae and
Aegothelidae include more than 50% of polymorphic
species, but also two large families, Strigidae and
Accipitridae, show a great incidence of colour polymor-
© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248
237
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P. GALEOTTI and D. RUBOLINI
phism (38.5% and 22.1%, respectively, Galeotti et al.,
2003).
Owls and nightjars form closely related orders, but
their relationship with diurnal raptors is more distant. Similarly, cuckoos and pheasants are not closely
related taxa (Sibley, Ahlquist & Monroe, 1988; Sibley
& Ahlquist, 1990). Moreover, Galliformes belong to the
Eoaves, whereas all the others are Neoaves; this suggests that the potential to develop colour polymorphism is common to both ancestral and modern bird
taxa, and it appears to have evolved independently
many times in birds. Indeed, colour polymorphism
might reflect similar selective pressures under which
avian species are evolving.
Two main hypotheses have been proposed to explain
the maintenance of colour polymorphism: apostatic
selection, and disruptive selection (Ford, 1945; Huxley,
1955; Butcher & Rohwer, 1989; Lank, 2002). These
two hypotheses have received most attention, while a
third mechanism, namely sexual selection (Butcher &
Rohwer, 1989) is apparently hardly applicable to polymorphic species, because individuals of each morph
are generally quite uniform and the occurrence of sexual dichromatism is not higher in polymorphic species,
as could be expected if sexual selection was involved in
the evolution of this trait (Galeotti et al., 2003; but see
Fowlie & Krüger, 2003).
Apostatic selection in the form of the avoidance
image hypothesis has been invoked repeatedly to
explain polymorphism in birds of prey (Paulson, 1973;
Rohwer, 1983; Rohwer & Paulson, 1987). The logic
behind this hypothesis is fascinating: it may be advantageous for a morph of an avian predator to be different from other conspecifics in the area as it will be less
familiar to potential prey. In short, prey do not form an
‘avoidance image’ for the rare morph in the predator
population and therefore do not react quickly to it; the
slight advantage in prey capture thus accrued would
presumably lead to a balanced polymorphism in predator species. Under this hypothesis, prey are considered the apostatic selective agents.
The avoidance image hypothesis has been proposed to explain colour polymorphism in avian predators such as hawks (Accipitridae and Falconidae)
and skuas (Laridae) that prey on intelligent and
sharp-sighted prey (birds, medium-sized mammals
and some lizards). However, Preston (1980) argued
effectively against such a selection mechanism, and
recent comparative studies controlling for phylogeny
failed to find support for this hypothesis as a general rule to explain the maintenance of colour polymorphism in birds (Galeotti et al., 2003; Fowlie &
Krüger, 2003).
Conversely, a balanced colour polymorphism may be
due to disruptive selection that favours extreme individuals but disadvantages intermediate individuals of
a normally distributed population. Clearly, for an
equilibrium between the morphs to be established,
selective pressures must favour alternately one of the
two (or more) phenotypes. As Fisher (1930) first suggested, heterogeneity in space and time is an evolutionary prerequisite, since habitat and climate
differences in selective pressures may be responsible
for producing a balanced colour polymorphism in species with broad ecological niches. Moreover, a large
population size and hence a large gene pool may
favour the evolution of plumage variability (Fowlie &
Krüger, 2003). Van Valen & Grant (1970) pointed out
that a species may occupy a wide range of environments either because individuals are generalist in
their habitat use, or because the species is made up of
a number of divergent individuals, each specialized in
its habitat use. Van Valen (1965) suggested that if different sections of a species are each adapted to their
specialized habitat then polymorphism would be promoted in species with broad habitat use. This idea has
become known as the ‘niche variation hypothesis’,
which states that species with broader ecological
niches should be more variable compared with those
with narrow niches because of the action of disruptive
selection. Following this hypothesis, colour polymorphism could enhance foraging efficiency or defensive
camouflage of members of a species, depending on
their habitat use, thus providing additional survival
advantages to different morphs of a polymorphic species colonizing environments highly heterogeneous in
space, time and light conditions. Colour polymorphism
may therefore function in helping a bird to avoid
detection by its predators (Baker & Parker, 1979),
reducing the chances of it being seen by its prey (Götmark, 1987), and limiting inter- and intraspecific competition (Spear & Ainley, 1993), allowing different
morphs to realize different ecological niches. If morphs
show selective habitat preference, polymorphism
could be maintained even in the presence of high gene
flow between the different habitats, and might lead to
species divergence. Some studies support this contention (Rothstein, 1973; Grant et al., 1976; Grant, 1985;
Hedrick, 1986) while others apparently do not (Wilson, 1969; Soulé & Stewart, 1970). According to the
disruptive selection hypothesis, colour polymorphism
is greatest in avian species living in both open and
closed habitats and particularly in species which are
active during both day and night (Galeotti et al.,
2003). These patterns suggest that varying light conditions may be the most important selective mechanism maintaining colour polymorphism in birds, and
crypsis, i.e. matching habitat background, may represent the major function.
Here we present a further comparative analysis of
colour polymorphism, within bird groups showing the
highest occurrence of this phenomenon, namely rap-
© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248
COLOUR POLYMORPHISM AND NICHE WIDTH IN BIRDS
tors, owls and nightjars. Owls and nightjars are genetically very close, and raptors share with owls a
number of morphological and ecological traits due to
their predatory habit. In particular, we focused on apostatic selection and disruptive selection as the main
potential mechanisms of polymorphism maintenance
in predatory birds.
The avoidance image hypothesis makes two predictions referring mainly to diurnal raptors: first, polymorphism should be higher in species hunting birds or
mammals with good vision and learning/memory
capabilities; second, polymorphism should be higher
in migratory species than it is in resident species. This
follows from the assumption that resident predators
have non-overlapping hunting ranges throughout the
year, while migrant predators are likely to have overlapping hunting ranges in winter. Therefore, during
winter prey have more chances to meet many different
individuals of a migrant predator species, so that a
rare predator morph may invade a monomorphic population more easily. This last prediction is, however,
weak, since (a) it is based on several untested assumptions (Rohwer & Paulson, 1987), and (b) the development of an avoidance image must require, by analogy
with search image formation, a certain amount of time
and repeated encounters between the prey and a specific predator, i.e. the formation of a specific prey–
predator system. However, it is highly unlikely that
prey faces only one predator species during winter
when many different predator species share hunting
ranges, and this may strongly interfere with the formation of a specific avoidance image (see Pietrewicz &
Kamil, 1979, 1981 for problems related to search
image formation).
On the other hand, if colour polymorphism is an evolutionary adaptation to alternating extremes of condition, or to a wider range of habitats or niches, we may
predict that polymorphic species will share a wider
distribution range, exploit more habitats, live in seasonally alternating climates, and frequent both open
and closed habitats. Furthermore, we would expect
polymorphism to occur preferentially in species experiencing more variable light conditions, i.e. those that
are active during both day and night (Galeotti et al.,
2003), and being characterized by larger dispersal
movements, because migrants realize wider niches
than do residents (Greenberg, 1985; Leisler, 1990).
Following this line of reasoning, we might theoretically expect polymorphic species to have wider trophic
niches, but in fact we did not have a specific prediction
regarding trophic niche width of polymorphic species,
since colour morphs of a species do not differ in morphological traits related to feeding, such as involving
the bill or claws, which may influence exploitation of
food supplies. Therefore, we did not consider trophic
niche width in these analyses.
239
In this study, we examined the role of the two
proposed selective mechanisms in the evolutionary
transition between monomorphic and polymorphic
plumage, by contrasting several ecological features in
a dataset including a large number of closely related
pairs of species differing in plumage colour pattern.
Pairwise comparisons provided a control for phylogeny
and other confounding factors, since closely related
species usually show similar morphological and ecological traits due to their common ancestry (Møller &
Birkhead, 1992; Maddison, 2000).
METHODS
DATA
COLLECTION
We collected data on plumage coloration pattern and
several behavioural and ecological traits for all species
belonging to the orders Ciconiiformes (diurnal raptors:
families Accipitridae and Falconidae), Strigiformes
(owls: families Tytonidae, Strigidae; nightjars: families Nyctibidae, Caprimulgidae, Podargidae, Batrachostomidae, Aegothelidae) by consulting the existing
specialist literature on these bird groups (King &
Dickinson, 1975; Howard & Moore, 1980; Brown,
Urban & Newman, 1992; Meyer De Schauensee, 1992;
Pizzey & Knight, 1997; Cleere & Nurney, 1998;
Cramp, 1998; Grimmet, Inskipp & Inskipp, 1998; Westoll, 1998; del Hoyo, Elliott & Sargatal, 1999; König,
Weick & Becking, 1999; Scott, 1999; Ferguson-Lees &
Christie, 2001). Species were classified as monomorphic (all individuals of a given sex show the same
plumage colour) or polymorphic (individuals of both
sexes may occur in two or more colour morphs). We
considered only species in which colour polymorphism
occurred in adults of both sexes. A degree of colour
polymorphism in a species could be attributed also to
sexual dichromatism; to reduce a possible confounding
effect of sexual dichromatism in our analyses, we
selected pairs of species in which the monomorphic
member was also sexually monochromatic or pairs
of species in which both members were sexually
dichromatic.
For each species we recorded the following ecological
and behavioural variables:
distribution range: extent of distribution range
scored as follows: 1, isolated; 2, small (<30% of the
biogeographical region) and fragmented; 3, small and
continuous; 4, wide (>30% of the biogeographical
region) and fragmented; 5, wide and continuous;
main food: main food categories indicated with values ranging from 0 for species preying mainly on
invertebrates, fishes, amphibians and reptiles, to 1 for
species preying mainly on birds and mammals; this
variable was collected only for raptors and owls
because all nightjars are insectivorous;
© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248
240
P. GALEOTTI and D. RUBOLINI
number of habitats: number of main habitats used
by the species;
vegetation cover: vegetation cover of frequented
habitats: 1, species frequenting only a single habitat
type in terms of vegetation cover being open (canopy
cover absent or very scarce) or closed (dense canopy
cover); 2, species frequenting a mixture of open and
closed habitats; closed habitats included forested
areas, while open habitats included areas mostly
devoid of tree cover, such as savannahs, grasslands,
deserts, tundra, lakes or coastal shores;
climate: 1, species living in a single climate type,
wet (absence of dry seasons) or dry (absence of rainy
seasons throughout the year); 2, species living in dry/
wet climates (alternating dry and wet seasons);
activity rhythm: 1, species active only during daytime, only during night time, or only during twilight;
2, species active during twilight/day or twilight/night;
3, species active throughout the day (daytime, night
time and twilight);
phenology: 1, resident (species living all year in the
same location); 2, nomadic (species showing dispersive
and erratic movements within and outside breeding
areas); 3, partial migrant (species with both migrant
and resident populations); 4, migrant (species showing
regular migratory movements).
PHYLOGENETIC
ANALYSIS AND STATISTICS
Data for different species cannot be considered as
independent points in comparative studies because
closely related species are more likely to share similar
ecological features due to a common ancestor (Felsenstein, 1985; Harvey & Pagel, 1991). Therefore, we used
the pairwise comparative method to control for possible similarities among closely related species due to
phylogeny (Møller & Birkhead, 1992; Maddison,
2000).
We used recent phylogenetic information based on
molecular or morphological traits to form closely
related pairs of species with contrasting plumage
colour patterns (Cleere & Nurney, 1998; Griffith, 1999;
Wink & Heidrich, 1999; Ferguson-Lees & Christie,
2001). A lack of variance in plumage pattern within
clades often limited the number of species pairs that
could be used for comparisons. Pairs were chosen to be
phylogenetically separate, i.e. the path between members of a pair, along the branch of the tree, did not
touch the path of any other pair (Maddison, 2000).
One phylogenetic tree could yield several pairs as long
as pairs failed to share common branches. When several species were available as sister taxa, we selected,
if possible, species that occurred in the same geographical area. When phylogenetic information was
not available, we formed pairs by selecting two species
from the same genera, with a preference for species
occurring in the same geographical area. In the few
cases (10 of 91 pairs) for which a proper congener species was not available, we chose a species belonging to
a sister genera occurring in the same geographical
area (e.g. Morphnus guaianensis and Harpia harpyja).
We selected pairs from as many families as possible to
reduce the problem of sampling repeatedly in the
same clades (Beauchamp & Heeb, 2001).
The Wilcoxon signed-rank test was used to test the
hypothesis of consistent changes across the set of species pairs in the states of ecological and behavioural
variables associated with the two plumage patterns.
Tests were performed for all pairs of all bird groups
together and for each bird group separately. Sample
sizes varied slightly among different tests because of
missing data for some species (see Results). We used
the sequential Bonferroni test procedure to adjust the
observed significance level to the number of tests
made with the same data set (Rice, 1989). We present
the P-values of the tests before performing the Bonferroni test and describe whether the correction modified their significance. For clarity, means and SEs are
presented for analysed variables instead of medians
and quartiles.
RESULTS
The search in the published literature provided a total
of 91 pairs of species with contrasting plumage colour
pattern, of which 41 were raptors, 31 owls, and 19
nightjars (see Appendix).
Polymorphic species of owls, nightjars and raptors
shared similar ecological features that differed significantly from those of their monomorphic counterparts
(Table 1). Overall, polymorphic species showed wider
and more continuous distribution ranges, frequented
many different habitats, both open and closed, and
lived in seasonally alternating dry/wet climates. Polymorphic species also showed a stronger migratory
tendency compared with their monomorphic counterparts. Finally, they exhibited an extended day/night
activity pattern. In contrast, polymorphic species of
raptors and owls were not more specialized on intelligent prey than were their monomorphic counterparts
(Table 1).
Considering bird groups separately (Fig. 1), we
found that polymorphic species of raptors showed a
wider distribution range compared with their monomorphic counterparts (Z = -4.2, P < 0.0001, N = 41
pairs); they also frequented more habitats (Z = -3.03,
P = 0.002, N = 41 pairs), and showed a stronger migratory habit (Z = -2.7, P = 0.007, N = 41 pairs). After
Bonferroni correction no other traits were found to be
associated with colour polymorphism in raptor species
(climate: Z = -2.1, P = 0.039, N = 41 pairs; activity
pattern: Z = -1.6, P = 0.10, N = 41 pairs; main food:
© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248
241
COLOUR POLYMORPHISM AND NICHE WIDTH IN BIRDS
Table 1. Mean (SE) of variables measured for monomorphic and polymorphic pairs of species of raptors, owls and nightjars
Variable
Monomorphic species
Polymorphic species
N pairs
Z
P
Distribution range
No. of habitats
Main fooda
Vegetation cover
Climate
Activity
Phenology
2.59
1.91
0.58
0.29
0.22
1.36
1.37
3.70
2.79
0.59
0.54
0.45
1.50
1.74
91
91
66
91
89
88
91
-5.57
-4.88
-0.33
-3.29
-3.33
-2.60
-3.20
0.000*
0.000*
0.74
0.001*
0.001*
0.011*
0.001*
(0.13)
(0.12)
(0.06)
(0.04)
(0.04)
(0.06)
(0.08)
(0.14)
(0.15)
(0.06)
(0.05)
(0.05)
(0.07)
(0.11)
Wilcoxon signed-rank test; asterisks indicate significant P-values after sequential Bonferroni correction. arecorded only
for raptors and owls.
Z = -1.3, P = 0.18, N = 37; vegetation cover: Z = -1.15,
P = 0.25, N = 41).
In owls, the number of habitats frequented was significantly higher in polymorphic species than it was in
monomorphic ones (Z = -2.95, P = 0.002, N = 31 pairs),
and polymorphic species used more varied habitats in
terms of vegetation cover (Z = -2.7, P = 0.007, N = 31
pairs). The distribution range of polymorphic owls was
wider than that of monomorphic ones (Z = -2.5,
P = 0.01, N = 31 pairs), and polymorphic species
tended to be active during both day and night
(Z = -2.1, P = 0.035, N = 28 pairs), but these differences were no longer significant after Bonferroni correction. Other variables did not differ between
polymorphic and monomorphic owls (all P > 0.05).
In nightjars only the extent of distribution range
was significantly associated with colour polymorphism
(Z = -2.7, P = 0.008, N = 19 pairs), and no other traits
were found to differ between monomorphic and polymorphic species after Bonferroni correction (e.g. number of habitats: Z = -2.3, P = 0.019, N = 19 pairs;
phenology: Z = -2.3, P = 0.021, N = 19 pairs, climate:
Z = -2.0, P = 0.046, N = 19 pairs).
The observed differences between bird groups in the
ecological and behavioural features associated with
colour polymorphism may be due to different sample
sizes or to some differences in the general biology of
groups, for example, nightjars are mostly crepuscular
and most owls show strong residency and nocturnal
habits. However, the trends were remarkably similar
among the three groups for most variables (Fig. 1).
DISCUSSION
The results of this study indicate that, across a wide
range of bird species, the evolutionary transition
from monomorphic to polymorphic plumage is associated with a broad ecological niche, thus supporting
the niche variation hypothesis (Van Valen, 1965) for
the maintenance of colour polymorphism in predatory
birds. Most polymorphic species of raptors, owls and
nightjars were widely distributed and adapted to a
broader range of environmental conditions compared
with their monomorphic counterparts. This may be
the result of different individuals within a species
occupying different parts of a broad niche. The evolution of polymorphism is therefore favoured if individuals have a better than random chance of colonizing
the kind of microhabitat to which their genotype best
suits them, and this occurs if animals can accomplish
the correlation between genotype and environment
by habitat selection. Thus, adaptation to different
aspects of the environment appears to be a major
cause of intraspecific variation in plumage colour
among these bird groups. In this sense morphs may
actually be ecotypes of a species. Indeed, our results
met most predictions stemming from the disruptive
selection mechanism of polymorphism maintenance.
Conversely, the alternative hypothesis for the maintenance of colour polymorphism, i.e. apostatic
selection in the form of avoidance image development (Paulson, 1973; Rohwer, 1983; Rohwer & Paulson, 1987) did not find support in this study. We
showed that polymorphic raptors did not differ in the
main food categories consumed compared with monomorphic species, i.e. polymorphic raptors were not
more likely to catch birds and mammals (intelligent
prey) than were monomorphic ones. The second prediction of the avoidance image hypothesis, namely
that migratory species should be more polymorphic
compared with resident species, was met in this
study. However, this result is equally compatible with
the niche variation hypothesis, because generally
migratory and/or nomadic species occur in a wider
range of habitats and exploit environments more
variable in terms of climate, type, and vegetation
cover than do residents (e.g. Greenberg, 1985; Leisler,
1990). In addition, explaining the association
between plumage polymorphism and migratory habit
under the niche variation hypothesis is more parsimonious, because it does not require any underlying
assumption, as conversely required under the apos-
© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248
242
P. GALEOTTI and D. RUBOLINI
B) 4.0
4.0
No. of habitats
Distribu tion r ange
A) 5.0
3.0
2.0
1.0
0.0
2.0
1.0
0.0
Raptors
Owls
Night jars
Raptors
Owls
Nightjars
Raptors
Owls
Nightjars
Raptors
Owls
Nightjars
D) 0.8
C) 1.0
Vegetation cover
0.8
Main food
3.0
0.6
0.4
0.2
0.0
0.6
0.4
0.2
0.0
Raptors
Owls
Night jars
E) 0.8
F) 2.4
2.0
Ac tivity
Climate
0.6
0.4
1.6
1.2
0.8
0.2
0.4
0.0
0.0
Raptors
Owls
Night jars
Raptors
Owls
Night jars
G) 2.5
Phenol ogy
2.0
1.5
1.0
0.5
0.0
Figure 1. Mean (+ SE) of ecological and behavioural traits for monomorphic (open bars) and polymorphic (black bars)
species of raptors, owls and nightjars.
© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248
COLOUR POLYMORPHISM AND NICHE WIDTH IN BIRDS
tatic selection hypothesis (see Introduction and
Rohwer & Paulson, 1987).
In fact, the avoidance image hypothesis has several
weaknesses (see also Preston, 1980): (a) no evidence
exists to show that prey develop an ‘avoidance image’
of common avian predator morphs; assuming they do
by analogy with search image formation by predators
may seem appealing at first glance, but it certainly
does not represent a solid basis for further speculation; (b) it would be maladaptive for prey to focus on
plumage pattern while ignoring other cues indicative
of a predator, such as silhouette, vocalizations, noises,
movements (e.g. Hendrie, Weiss & Eilam, 1998); (c)
intelligent prey must constitute an unknown but
clearly substantial fraction of a predator diet to effectively exert a selection pressure on the predator itself
(see Paulson, 1973); however, to the best of our knowledge, very few polymorphic raptor species can be considered to be so specialized on this kind of prey (e.g.
some large falcons); (d) prey must repeatedly encounter a single predator morph in order to effectively
develop a specific avoidance image (by analogy with
search image formation, see Pietrewicz & Kamil,
1979, 1981); this contrasts with the common notion
that many predator pairs are mixed-coloured, and
with the fact that prey may encounter many predator
types and should learn to avoid them regardless of
their plumage pattern (Arnason, 1978).
Moreover, recent comparative studies failed to support the apostatic selection mechanism for colour polymorphism maintenance in birds: first, among all
polymorphic species, colour polymorphism was not
expressed more in diurnal predator species as postulated by the hypothesis, but in fact was more widespread in vegetarian taxa and in those active during
both day and night (Galeotti et al., 2003); second,
among raptors and owls, plumage polymorphism was
not more common in taxa preying on avian or mammalian prey, but was consistently related to population and range size of species (Fowlie & Kruger, 2003),
which is in accordance with predictions based on the
niche variation hypothesis. Although a large population size may be a precursor to the occurrence of plumage polymorphism, as advocated by Fowlie & Kruger
(2003), it may also be a consequence of intraspecific
variation in niche occupancy, which permits a population size greater than would otherwise be possible
(Van Valen, 1965). Therefore, the present evidence
suggests that apostatic selection is an unlikely mechanism to explain colour polymorphism maintenance in
birds.
In conclusion, broad-niche species have a higher
potential to develop different colour patterns that may
be adaptive in different environmental conditions by
providing efficient crypsis to bearers. Different morphs may vary in success in different habitats or in the
243
same habitat under different conditions, because of
variation in foraging efficiency or survival due to
hunting or defensive camouflage. If fitness of different
morphs differs between habitats, then polymorphism
can be established with different equilibrium gene frequencies in the different habitats or in the same habitat under different conditions. The high frequency of
morph ratio-clines according to several environmental
factors further supports this prediction based on disruptive selection (Galeotti et al., 2003). A common
environmental feature of these morph ratio-clines is
variation in light conditions (Galeotti et al., 2003). It is
now well documented that the conspicuousness or
crypsis of colour patterns of an animal strongly
depend on the interaction between light levels, spectral composition of ambient light and the reflectance
spectra of colour pattern elements (Endler, 1978, 1986,
1990, 1991; Endler & Théry, 1996). Thus, the balance
between different plumage coloration in a bird species
may be determined by the relative benefits of conspicuousness or crypsis to predators, prey, conspecifics and
guild members, in a variety of different habitats or
habitat conditions, and light levels appear to play a
major role (Galeotti et al., 2003).
Based on our results, we conclude that colour polymorphism may be maintained by disruptive selection
acting on species with broader ecological niches, and
might be a first step towards species divergence (Marchetti, 1993). A further empirical and intraspecific test
of the niche variation hypothesis may be provided by
comparison between members of the same population
in order to demonstrate that different morphs differ in
habitat use. Alternatively, one may compare the level
of polymorphism among different populations of the
same species, in order to demonstrate that habitat use
is wider in some populations, and then to show that
plumage colour is more variable in populations in
which the habitat use is broader.
ACKNOWLEDGEMENT
We thank Dr A. Roulin for his useful criticisms and
suggestions on an early draft of the paper.
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APPENDIX
List of closely related pairs of monomorphic and polymorphic species of raptor (families Accipitridae and Falconidae), owls
and nightjars (order Strigiformes) and associated scores for ecological and behavioural traits (see Methods for explanation
of scores). The variable ‘Polymorphism’ indicated whether a species was monomorphic (score 0) or polymorphic (score 1).
Species
Raptors (N = 41 pairs)
Rostrhamus sociabilis
Chondrohierax uncinatus
Pernis celebensis
Pernis apivorus
Circaetus fasciolatus
Terathopius ecaudatus
Circus ranivorus
Circus aeruginosus
Circus cinereus
Circus buffoni
Circus macrourus
Circus pygargus
Accipiter castanilius
Micronisus (Melierax) gabar
Accipiter toussenelii
Accipiter tachiro
Accipiter fasciatus
Accipiter novaehollandiae
Accipiter melanochlamys
Accipiter albogularis
Accipiter luteoschistaceus
Accipiter imitator
Accipiter princeps
Accipiter poliocephalus
Accipiter rufiventris
Accipiter ovampensis
Accipiter chionogaster
Distribution No. of
Main Vegetation
Polymorphism range
habitats food cover
Climate Activity Phenology
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
4
5
2
5
3
5
2
4
5
5
3
4
3
5
3
5
4
2
2
1
1
1
1
3
2
4
1
1
5
1
2
1
2
3
3
3
3
3
5
1
3
1
2
4
2
2
3
2
1
1
2
4
3
1
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
–
–
–
1
1
1
1
0
1
0
1
0
1
0
0
0
0
0
0
0
0
0
0
1
0
0
0
1
0
0
1
1
1
0
0
1
0
1
0
0
1
1
0
0
0
1
0
0
0
1
1
0
0
0
0
0
0
0
1
0
0
© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
1
1
4
2
2
2
3
3
3
4
4
1
1
1
1
1
1
1
1
1
1
1
1
1
2
1
246
P. GALEOTTI and D. RUBOLINI
APPENDIX Continued
Distribution No. of
Main Vegetation
Polymorphism range
habitats food cover
Climate Activity Phenology
Species
Accipiter ventralis
Accipiter gundlachi
Accipiter bicolor
Accipiter henstii
Accipiter melanoleucos
Erythrotriorchis radiatus
Erythrotriorchis buergensi
Megatriorchis doriae
Urotriorchis macrourus
Buteo magnirostris
Buteo platypterus
Buteo albigula
Buteo brachyurus
Buteo albonotatus
Buteo swainsoni
Buteo galapagoensis
Buteo polyosoma
Buteogallus anthracinus
Buteo jamaicensis
Buteo oreophilus
Buteo buteo
Buteo auguralis
Buteo rufinus
Parabuteo unicinctus
Buteo regalis
Buteo archeri
Buteo augur
Harpia harpyja
Morphnus guaianensis
Aquila nipalensis
Aquila pomarina
Aquila verreauxii
Aquila wahlbergi
Hieraaetus fasciatus
Hieraaetus pennatus
Hieraaetus kienerii
Hieraaetus morphnoides
Spizaetus alboniger
Spizaetus cirrathus
Micrastur gilvicollis
Micrastur ruficollis
Micrastur buckleyi
Micrastur semitorquatus
Falco tinnunculus
Falco sparverius
Falco araea
Falco newtonii
Falco concolor
Falco eleonorae
Falco novaeseelandiae
Falco berigora
Falco mexicanus
Falco rusticolus
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
2
1
5
1
4
5
3
3
4
5
4
3
5
4
4
1
5
2
5
2
5
2
4
4
3
1
4
5
5
4
2
2
5
2
4
2
5
2
4
3
5
3
5
5
5
1
3
2
2
1
5
3
5
1
3
3
1
2
1
1
1
1
4
2
1
4
4
3
2
4
3
4
2
4
3
3
2
2
1
3
1
1
1
2
1
2
1
1
1
3
1
3
1
1
1
2
4
4
2
4
3
3
2
5
3
2
1
1
1
1
1
1
1
1
1
0
1
1
1
1
1
1
1
1
1
1
1
0
1
1
1
–
1
1
1
1
1
1
1
1
1
1
1
1
1
0
1
–
1
0
0
1
0
0
0
1
1
1
1
1
1
1
0
1
1
0
0
0
1
1
0
1
1
1
1
0
1
1
1
1
1
0
0
0
0
1
0
0
0
1
0
1
0
1
0
1
1
1
0
0
0
0
1
1
1
0
0
0
0
0
0
0
1
1
1
1
1
1
0
0
0
1
1
0
1
1
0
0
0
1
1
0
1
1
0
0
0
0
1
0
0
0
1
0
1
0
0
0
1
0
1
0
0
0
0
1
1
0
0
1
1
0
1
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
1
3
1
1
1
2
1
1
1
1
3
1
1
1
1
1
4
1
3
3
4
1
3
3
3
3
3
3
3
1
3
1
1
1
1
4
3
1
4
1
3
1
1
1
1
1
1
1
1
3
3
1
1
4
4
1
1
2
2
© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248
247
COLOUR POLYMORPHISM AND NICHE WIDTH IN BIRDS
APPENDIX Continued
Species
Falco subbuteo
Falco peregrinus
Owls (N = 31 pairs)
Tyto tenebricosa
Tyto novaehollandiae
Otus icterorhynchus
Otus ireneae
Otus angelinae
Otus balli
Otus semitorques
Otus bakkamoena
Otus elegans
Otus sunia
Otus umbra
Otus beccarii
Otus longicornis
Otus rutilus
Otus insularis
Otus pembaensis
Otus cooperi
Otus asio
Otus sagittatus
Otus trichopsis
Otus mindorensis
Otus choliba
Otus koepckeae
Otus roboratus
Otus clarkii
Otus barbarus
Otus petersoni
Otus ingens
Otus albogularis
Otus guatemalae
Bubo magellanicus
Bubo virginianus
Bubo ascalaphus
Bubo bubo
Bubo capensis
Bubo africanus
Strix uralensis
Strix aluco
Strix occidentalis
Strix woodfordii
Strix hylophila
Strix rufipes
Strix albitarsis
Strix virgata
Pulsatrix perspicillata
Lophostrix cristata
Glaucidium passerinum
Glaucidium brodiei
Glaucidium perlatum
Glaucidium gnoma
Distribution No. of
Main Vegetation
Polymorphism range
habitats food cover
Climate Activity Phenology
0
1
3
4
4
5
0
1
1
0
1
1
1
1
4
3
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
2
5
2
1
1
1
3
5
1
5
1
1
1
3
1
1
3
5
3
3
1
5
2
3
3
3
3
4
3
2
3
4
4
5
2
4
4
4
2
4
3
3
3
5
5
4
4
4
4
3
1
3
2
1
1
2
1
3
1
5
1
1
1
4
1
1
5
5
1
1
1
7
1
2
1
1
1
2
3
3
3
5
2
4
3
3
1
4
1
2
1
1
2
4
4
1
1
2
3
1
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
–
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
0
1
1
1
0
1
1
–
1
1
0
1
1
0
0
0
1
0
0
0
0
0
1
0
1
1
1
0
1
0
0
1
1
0
0
0
1
0
1
0
0
0
1
1
0
0
1
0
1
1
0
0
1
0
0
0
0
0
1
1
0
0
1
1
0
0
0
0
0
0
0
–
0
0
0
0
0
0
1
–
0
0
1
0
0
0
0
0
0
0
0
0
0
0
1
0
1
0
1
0
0
1
1
1
1
1
0
0
1
1
0
1
0
0
0
1
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
–
3
–
1
1
1
1
1
2
1
1
2
1
1
2
3
2
3
2
3
2
2
1
1
1
2
1
2
1
1
2
3
3
2
1
1
1
1
1
1
3
1
1
3
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248
248
P. GALEOTTI and D. RUBOLINI
APPENDIX Continued
Distribution No. of
Main Vegetation
Polymorphism range
habitats food cover
Climate Activity Phenology
Species
Glaucidium nubicola
Glaucidium costaricanum
Glaucidium minutissimum
Glaucidium jardinii
Glaucidium peruanum
Glaucidium brasilianum
Glaucidium tephronotum
Glaucidium siju
Athene brama
Athene noctua
Ninox scutulata
Ninox superciliaris
Nightjars (N = 19 pairs)
Aegotheles tatei
Aegotheles crinifrons
Aegotheles wallacii
Aegotheles albertisi
Aegotheles bennettii
Aegotheles cristatus
Batrachostomus auritus
Podargus ocellatus
Batrachostomus moniliger
Batrachostomus septimus
Batrachostomus poliolophus
Batrachostomus stellatus
Nyctibius maculosus
Nyctibius griseus
Chordeiles pusillus
Chordeiles gundlachii
Podager nacunda
Nyctidromus albicollis
Nyctiphrynus rosenbergi
Nyctiphrynus yucatanicus
Siphonorhis brewsteri
Nyctiphrynus ocellatus
Caprimulgus rufus
Caprimulgus carolinensis
Caprimulgus cayennensis
Caprimulgus longirostris
Caprimulgus poliocephalus
Caprimulgus pectoralis
Caprimulgus
madagascariensis
Caprimulgus asiaticus
Caprimulgus tristigma
Caprimulgus natalensis
Caprimulgus batesi
Caprimulgus inornatus
Caprimulgus pulchellus
Caprimulgus affinis
Caprimulgus enarratus
Caprimulgus climacurus
0
1
0
1
0
1
0
1
0
1
0
1
3
3
3
3
3
5
2
1
5
5
4
2
1
2
1
3
3
6
2
3
5
5
4
5
0
0
0
1
0
0
0
0
0
0
0
0
0
1
0
1
1
1
0
1
0
0
0
1
0
0
0
1
0
1
0
1
0
0
0
1
–
3
3
3
3
3
3
3
2
3
2
2
1
1
1
1
1
1
1
1
1
1
3
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
1
1
1
2
2
5
2
2
2
2
1
2
3
5
4
2
4
5
3
3
1
4
4
3
3
4
2
5
1
2
1
3
1
4
1
1
1
1
1
1
1
4
3
2
4
4
1
4
2
1
4
3
2
4
2
3
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
0
0
0
1
0
1
0
0
0
0
0
0
0
1
0
1
0
1
0
1
1
0
1
1
0
0
1
1
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
1
1
0
0
0
1
2
1
2
2
2
2
1
2
2
2
1
1
1
2
1
2
3
2
2
2
2
2
2
2
2
2
2
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
4
3
1
1
1
1
1
1
4
1
3
1
3
0
1
0
1
0
1
0
1
0
1
3
5
3
3
2
5
1
4
2
4
3
2
1
2
2
2
1
4
1
4
–
–
–
–
–
–
–
–
–
–
0
1
0
0
1
0
0
0
0
1
0
1
0
0
0
0
0
1
0
0
2
2
2
2
2
2
2
2
2
2
1
3
1
1
1
3
1
3
1
3
© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82, 237–248