Behavioral Ecology
doi:10.1093/beheco/arj027
Advance Access publication 22 December 2005
Rufous-tailed jacamars and aposematic
butterflies: do older birds attack novel prey?
Gary M. Langham
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA
Although avian predators are thought to drive the evolution of warning-color mimicry in butterflies, few empirical studies directly
address this assumption from the predator’s perspective. Heliconius butterflies are textbook examples of Mullerian mimicry, with
perhaps the most remarkable example being the Heliconius erato and Heliconius melpomene mimicry complex. Rufous-tailed jacamars,
Galbula ruficauda (Galbulidae), are well-known butterfly predators and provide an excellent study organism to investigate patterns
of attack behavior in warning-colored butterflies. I investigated patterns of attack behavior by presenting three aposematic butterflies to wild-caught jacamars in a cage trial in Venezuela. I presented 80 jacamars with three Heliconius butterflies: an unaltered wing
pattern (local morph) and two altered wing patterns (novel morphs). Twenty-one of 40 males and 8 of 40 females attacked a butterfly
with a novel wing pattern. Of the morphological variables measured, tail length was the only significant predictor of attack behavior.
Individuals with relatively longer tails attacked novel butterflies more frequently than shorter tailed individuals. Because tail length
tended to increase between seasons, results suggest that older birds are more likely to attack novel aposematic prey than are young
birds, contrary to the expectations that younger adult birds (i.e., more likely to be naive) would attack novel Heliconius more
frequently than older birds. Overall results support the role of specialized avian predators, like jacamars, as important agents in
the evolution of warning-color mimicry in butterflies and the need to investigate different age classes of birds in mimicry studies.
Key words: aposematism, Galbula ruficauda, Heliconius, jacamar, Mullerian mimicry. [Behav Ecol 17:285–290 (2006)]
lthough it is thought that birds drive the evolution of
warning-color mimicry (Mullerian) in butterflies via their
capacity to exert predation pressure on rare wing patterns, few
direct studies with birds exist to explore this phenomenon
from the predator’s perspective. Heliconius butterflies are
often cited as an excellent example of natural selection and
Mullerian mimicry, with perhaps the most spectacular being
the Heliconius erato and Heliconius melpomene complex ( Joron
and Mallet, 1998; Mallet and Joron, 1999). These species cooccur and mimic each other throughout the lowland neotropics, converging on 15 geographically distinct morphs, such that
adjacent conspecifics have strikingly different wing patterns
(Sheppard et al., 1985). Convergence in these two species is
so complete that capture is often necessary for positive specieslevel identification (Holzinger H and Holzinger R, 1994).
Although H. erato and H. melpomene cannot interbreed, intraspecific hybridization is common along contact zones, producing viable hybrids with highly variable wing patterns (Mallet
and Barton, 1989b; Sheppard et al., 1985; Turner, 1971a,b).
Avian predators have long been thought to constrain dispersal across these contact zones by killing rare morphs at disproportionately high rates, resulting in frequency-dependent
selection that enforces narrow contact zones (Mallet and
Barton, 1989a; Mallet et al., 1990). In other words, on either
side of a hybrid zone resident Heliconius enjoy a relatively
attack-free life. Predators become familiar with this morph
and grow averse to it. However, any immigrant Heliconius
with a novel wing pattern is preferentially attacked because
predators have no experience with it. In this way, according
to theory, effective dispersal is minimized and narrow contact
zones are maintained.
A
Address correspondence to G.M. Langham, who is now at the
Museum of Vertebrate Zoology, University of California at Berkeley,
Berkeley, CA 94720-3160, USA. E-mail: [email protected].
Received 9 February 2004; revised 11 October 2005; accepted 22
November 2005.
The Author 2005. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
For birds to drive the evolution of Mullerian mimicry
systems in butterflies via positive frequency-dependent selection, butterflies with locally rare wing patterns must be attacked preferentially. Support for avian-driven selection has
been inferred from reduced recapture rates or wing damage
to experimentally translocated Heliconius (Benson, 1972;
Kapan, 2001; Mallet et al., 1990) and learning and forgetting
rates from computer simulations and laboratory experiments
(reviewed in Speed, 2000; Turner and Speed, 1996). In addition, theoretical models are available to describe predator
foraging in mimicry systems, but empirical data from experiments with avian predators would help in developing improved models. Predictable patterns of sampling would allow
better modeling of Heliconius systems, in particular, by determining the effective sampling population and rates of sampling novel prey over time.
Prevalence of Mullerian mimicry among butterflies strongly
suggests avian-driven selection because birds are common
visual predators. That some birds do learn to avoid aposematic
patterns after only a few encounters is well documented in
jays, Corvidae (e.g., Brower et al., 1964, 1968). This generalized pattern avoidance may explain the existence of Batesian
mimics and the relatively high frequency of imperfect mimicry. The motivation for predators to attack palatable prey like
cryptic moths or nontoxic mimics is obvious—they are consumed. However, less obvious is why predators would repeatedly attack aposematic prey. In a simple Mullerian mimicry
system, relatively low rates of selection can explain convergence of two or more species on a single pattern. The H. eratomelpomene system is regionally polymorphic, so that local forms
must face constant migrations for adjacent forms. The stability
of these systems is more difficult to explain from a predator’s
perspective, yet relatively higher rates of selection are necessary in order for Heliconius wing-pattern polymorphism to
remain stable. Direct empirical evidence that explain the
mechanisms of predatory behavior that result in frequencydependent selection would aid our understanding of how and
why avian predators are driving Mullerian mimicry complexes.
Behavioral Ecology
286
Few neotropical bird species are known to regularly attack
brightly colored butterflies. Jacamars are the best-known example. Rufous-tailed jacamars, Galbula ruficauda, excel at capturing fast-flying insects, such as dragonflies and wasps, and,
more importantly, at discriminating among numerous butterfly wing patterns (Burton, 1976; Chai, 1986; Skutch, 1983). In
contrast to the generalized aversion to aposematic butterflies
exhibited by jays, jacamars develop highly specific pattern
aversion but also constantly sample novel butterfly morphs
to find palatable mimics (Brower et al., 1963; Chai, 1986).
Although other bird families (e.g., Tyrannidae, Cuculidae,
and Momotidae) likely play some role in the evolution of
aposematic mimicry, jacamars represent important agents in
neotropical habitats because they feed on butterflies regularly
and have demonstrated skill at discrimination of butterfly
wing patterns (Chai, 1996).
Demonstrating that avian predators possess the ability to
play a role as a selective agent in the maintenance of regionally polymorphic mimicry requires two steps. First, experimental evidence that an important butterfly predator species is
capable of positive frequency-dependent selection must be
provided (e.g., Langham, 2004). Second, discovering predictable sampling patterns among predators would facilitate our
understanding of whether attacks are based on learning,
forgetting, mistakes, or attempts to discover Batesian mimics.
Because Heliconius are unpalatable, avian predators have little
motivation to attack these butterflies once, much less repeatedly over time. This second step is the focus of this study and
is especially important if Heliconius mimicry polymorphism is
enforced over time by long-lived, relatively sedentary birds,
like jacamars.
METHODS
Experimental design
I tested assumptions of predator behavior needed to maintain
Heliconius polymorphism and looked for significant patterns
of attack behavior and repeatability as a function of adult age
and morphology. I investigated patterns of sampling behavior
by presenting three aposematic butterflies to wild-caught
jacamars in cage trials in Venezuela. I presented 80 jacamars
(40 males and 40 females) with three Heliconius butterflies: an
unaltered wing pattern (local morph) and two altered wing
patterns (novel morphs).
Site
Los Cerrajones (225-m elevation; 09 12# N, 69 43# W) is
a working cattle ranch of approximately 650 ha located in
the llanos (savannas) of western Venezuela, in the state of
Portuguesa. I conducted experiments over three seasons:
the first season (two birds) from 10 February 1998 to 4 March
1998; the second season (38 birds) from 6 December 1999 to
18 February 2000; and the third season (40 birds) from 6
December 2000 to 17 April 2001. These dates fell within the
dry season (November–May) and overlapped most of the
breeding season of jacamars at the site. The breeding season
began soon after the rainy season ended in late October and
continued through late April, so that for some birds breeding
continued for up to 6 months. Stable pairs often started nest
building as early as 15 November and reared second broods
through early May. Breeding throughout the season as a whole
is quite staggered. However, by late February through mid-May
most free-living pairs were feeding young in the nest.
Jacamars
Individual birds were captured in nylon mist nets by attracting
them using conspecific playbacks. I took standard measure-
ments (e.g., mass, wing length, and tail length) from each
bird. After tail length was shown to be a predictor of attack
behavior in cage experiments, I recaptured as many of the 180
banded individuals on the study site as possible. Note that
these birds are not necessarily the same as those used in cage
experiments. However, these birds were only used to determine if tail length increased with age. I captured jacamars
before 1300 h and placed them (one bird per cage) in outdoor cages containing 15 free-flying, large dragonflies (total
8–11 g). Most birds began to forage on the dragonflies within
15 min and usually consumed all dragonflies by 1800 h. Individuals appearing to be severely stressed (e.g., puffed, not
foraging, or lethargic) were immediately returned to the wild
and not included in any experimental trials. Outdoor cages
(2 3 2 3 4 m) were supported by a wooden frame and covered
in a Lumite mesh. Cages, with dirt floors and one perch across
center, were shaded by trees directly behind and above cages.
Heliconius
I housed locally captured H. erato hydara in cages identical to
those described above and fed them a 2% sucrose solution ad
libitum. Some butterflies survived over 3 months under these
conditions. I captured butterflies using butterfly nets and
carefully marked them by hand, so as not to remove wing
scales. Butterflies were marked ventrally and dorsally on the
forewing patch with Sharpie pens that reflect little to no UV
applied to the bright red wing patch (see Langham, 2004;
Figure 1). After drying, this ink showed no visible sign of
altering normal activity or lifespan. The method of marking
wings was modified (after Benson, 1972) and required approximately 2 min of handling. Butterflies were only used in
trials if they were in good condition, showed little to no wing
damage, and appeared to have normal flight behavior. Although experimental handling of butterflies was similar and
they appeared to be undamaged, all butterflies are wild
caught and thus could have had varying rates of handling by
birds prior to this study.
Trials
Three H. erato (an unaltered local morph, an altered red
morph, and an altered black morph) were presented to individual jacamars simultaneously the morning after capture starting between 0900 and 1000 h for 2.5 h. Observers watched
from 25 m with 10 3 42 binoculars. Butterflies were captured
after each trial and examined closely for wing damage and bill
marks. Usually birds took the butterfly and returned to the
perch before releasing it, but sometimes they released the prey
even before returning to the perch. A sampling event was recorded when (1) a bird captured a butterfly with its bill and
brought it to the perch or (2) aerial sampling and release was
suspected and the butterfly showed clear wing damage or bill
marks. After each test, I returned the birds to the capture site
on the same day. Jacamars were kept under Cornell University
Institutional Animal Care and Use Committee protocol #98-96.
RESULTS
Cage trial
A novel (red or black) morph was attacked by 29 of 80 jacamars during the cage trial, while the local morph was never
attacked (0 of 80; see also Langham, 2004). I detected no
difference in sampling behavior among breeding seasons
(homogeneity of odds-ratio test among breeding seasons,
p ¼ .48), and results were combined in all subsequent analyses. Julian date was standardized for all three seasons to the
Langham • Do older birds attack aposematic butterflies?
287
Figure 1
Boxplots of (a) wing length
and (b) tail length for male
and female rufous-tailed jacamars. Both morphological
traits show moderate sexual
dimorphism (Table 1).
earliest experimental date (6 December). Julian date was not
a significant predictor of sampling behavior (logistic regression: R2 ¼ .003, p . .5).
Morphological variation
Among males and females, wing length and tail length were
the only morphological traits to show significant sexual dimorphism (Table 1). Despite considerable overlap, wing length in
males (range 75–84 mm) was significantly greater than in
females (range 75–82 mm) (F1,78 ¼ 5.41, p , .05) (Figure 1a).
Tail length in males (range 95–120 mm) and females (range
93–116 mm) differed significantly (F1,78 ¼ 42.1, p , .001)
(Figure 1b). Wing length and tail length were positively correlated for both males (r2 ¼ .16, p , .01) and females (r2 ¼ .23,
p ¼ .01) (Figure 2). Although tarsus is a good univariate measure of comparative body size in birds (Rising and Somers,
1989), tail length was not correlated with tarsus length or
any other morphological trait except wing length (Table 2).
Morphology and sampling
The only significant morphological predictor of attack behavior in the cage trial was tail length. A logistic regression model
(Table 3) was based on data from the cage trial, using a simplified description of sampling behavior (i.e., attack or avoid)
as the predictor variable, with six covariates and two interaction terms. The regression was highly significant overall (log
likelihood ¼ 40.39, df ¼ 6, p ¼ .0008) and supplied an adequate fit to the data (goodness of fit ¼ 80.78, df ¼ 6, p ¼ .22).
The model indicated a strong positive relationship of tail
length on the predicted probability of attacking a novel (red
or black) morph (estimated odds ratio ¼ 0.004). Two interactions with tail length were also investigated: sex and wing
length. Tail length was correlated with both sex (Figure 1b)
and wing length (Table 2), but interactions showed no significant effect in the model (Table 3). There was no significant
difference in tail length for birds that attacked a red or black
morph (r2 ¼ .08, p ¼ .14, n ¼ 29). A univariate logistic regression of tail length predicted a 50% or greater probability
of attacking a novel morph at tail lengths of .110 mm
(r2 ¼ .20, p , .001, n ¼ 80).
Tail length change
From the overall population of birds banded at the study site
(180 birds), 47 were captured multiple times from one to four
breeding seasons later. For these birds, tail length increased
between captures (Figure 3). Mean tail length of recaptured
birds increased 1.82 mm in males (SD ¼ 4.42, paired t ¼ 1.66,
df ¼ 24, p ¼ .11) and 2.0 mm in females (SD ¼ 3.28, paired
t ¼ 2.91, df ¼ 21, p , .01). Number of molts was not a significant predictor of tail length change (least squares regression:
R2 ¼ .08, F4,42 ¼ 0.10, p . .28), suggesting that tail length
reached an asymptote. In both sexes, there was a significant
negative relationship between initial tail length and magnitude of change in tail length between years (males: R2 ¼ .43,
F1,23 ¼ 17.4, p , .001; females: R2 ¼ .48, F1,20 ¼ 18.3, p , .001).
Long-tailed birds showed little change in tail length, while
short-tailed birds showed marked change.
Table 1
Means and coefficients of variation for morphological traits of male and female rufous-tailed jacamars
Males (n ¼ 40a)
Females (n ¼ 40)
Morphological trait
Mean
SD
CV
Mean
SD
CV
Sexual dimorphism
(male/female)
Body mass (g)
Wing length (mm)
Tail length (mm)
Tarsus length (mm)
Toe length (mm)
Bill length (mm)
23.5
79.2
110.3a
14.3
13.4
45.6
1.41
1.76
4.80
0.91
0.80
4.90
5.9
2.3
4.4
6.3
6.0
10.7
23.8
78.3
103.3
14.2
13.5
43.8
2.77
1.63
4.76
1.44
0.95
3.69
11.8
2.0
4.6
9.9
6.7
8.5
0.99
1.01*
1.07**
1.01
0.99
1.04
One male tail measurement is excluded due to missing feathers.
n ¼ 39 for tail.
* p , .05, **p , .001.
a
Behavioral Ecology
288
Figure 2
Association between tail length and wing length in male and female
rufous-tailed jacamars. Filled circles denote males (n ¼ 39) and
open circles denote females (n ¼ 40). Tail length and wing
length were correlated for both males (solid line) and females
(dashed line).
DISCUSSION
Results from this study have implications for the H. eratomelpomene system, Mullerian mimicry in neotropical butterflies, and our understanding of a predator’s perspective in
attacking potentially toxic prey. From a predator’s perspective,
Heliconius polymorphism is perhaps the most demanding
case of Mullerian mimicry to maintain. Predators must attack
brightly colored butterflies, memorize local wing patterns,
recognize novelty, and continue to attack bright, rare butterflies even though they may have experienced bright, toxic
butterflies in the past. Compounding the problem, Heliconius
butterflies are toxic and, therefore, provide no apparent
foraging benefit to sampling behavior in this system. These
factors have led previous investigators to suggest that naive
birds are the most likely predators in Heliconius mimicry complexes (e.g., Turner and Speed, 1996). Because toxic prey, like
Heliconius, provide no obvious foraging benefit, selection in
the Heliconius system was predicted to arise from younger
birds still learning the local butterflies and perhaps more
prone to attacking risky prey. Of the morphological variables
measured, however, tail length was the only significant predictor of attack behavior in each trial. Tail length tended to
increase with time, suggesting that longer tailed individuals
are older birds. This result supports the new hypothesis that
jacamars become increasingly adept at tasting and rejecting
toxic prey through reduced handling time or improved taste
discrimination. Among long-lived, sedentary birds, like jacaTable 2
Correlations between tail length and other morphological traits in
male and female rufous-tailed jacamars
Males (n ¼ 39)
Females (n ¼ 40)
Morphological trait
r
p
r
p
Weight (g)
Wing length (mm)
Tarsus length (mm)
Bill length (mm)
.223
.489
.259
.081
.17
,.01
.11
.06
.097
.400
.122
.161
.55
.01
.45
.32
One male tail measurement is excluded due to missing feathers.
Boldfaced type indicates significant p value.
mars, overall selection pressure is much higher if adults rather
than juveniles are the important agents, suggesting that most
adult birds will eventually play a role in selection against rare
aposematic morphs. Under the juvenile selection model,
a constant, but short-lived, selection pressure would exist each
season with most of the individuals leaving the population due
to dispersal or mortality.
Because birds have no obvious reason to attack aposematic
prey, the high proportion of adult birds attacking novel
Heliconius in each trial is surprising. Potential explanations
for this predator behavior include low sampling costs and
the search for Batesian mimics. Laboratory and field experiments using several bird species suggest that dietary conservatism either may be based on prior experience with novelty or
be a function of age. Domestic chicks (Roper, 1993) and blue
jays Cyanocitta cristata (Schlenoff, 1984) were more likely to
avoid novel prey after a previous negative experience with
unpalatable novel prey. In a study of wild blackbirds, Turdus
merula, Marples et al. (1998) found that one-third (of 27)
birds were willing to sample novel colored baits after prior
familiarization with a different colored bait. The remaining
birds needed varying amounts of exposure to sample the
novel baits. Thus, the results presented here could reflect
the most recent experience each bird had with novel prey.
Those individuals encountering a palatable novel prey type
may have been more willing to sample during this experiment. However, this should not be related to age and thus
seems unlikely. Lindstrom et al. (1999) found that great tits,
Parus major, were more likely to avoid aposematic prey than
cryptic prey. Importantly, wild-caught birds in their hatch year
were more likely to avoid novel aposematic than laboratoryreared juveniles or adults. If jacamars behaved in the same
way, we would predict more sampling in juveniles and less in
hatch year birds. If so, avoidance of novelty in young birds may
prevent foraging events that cause them to lose all crop contents. Established birds, especially ones with permanent territories, may benefit from expanding to new prey types while
being confident of feeding themselves. This behavior could
uncover Batesian mimics or other prey that might help if the
normal prey base decreases. Jacamars taste reject prey so the
foraging costs are lower than a bird that must ingest prey to
determine toxicity. Jacamars might then be better able to associate a particular predation event with toxicity of the prey
just handled, whereas other birds may not know which prey
type consumed was toxic.
I suggest that jacamars have evolved specialized capabilities
of taste discrimination associated with a diet high in butterflies and, therefore, have low energetic costs associated with
capture and sampling of novel prey relative to the costs likely
to be incurred by most other insectivorous bird species. Taste
rejection of toxic prey by jacamars was found in this and other
studies (Chai, 1986, 1988, 1996). Taste rejection is defined
here as release of prey after returning to the perch. After taste
rejection, jacamar behavior included vigorous bill wiping and
head shaking. The costs associated with taste rejection are
presumably much lower than vomiting crop contents, as
found by Brower et al. (1968).
Taste rejection by jacamars presents a problem for the interpretation of the role of jacamars in any mimicry system
because many attacks on toxic prey are followed by the release
of the prey. Even high rates of attack on prey would have little
selective effect if most prey escaped unharmed. In contrast,
generalists are likely to kill any captured prey, but if attack
rates are low the result is also low.
The existence of Batesian mimics may provide an incentive
to sample unfamiliar brightly colored prey but also suggests
that Batesian mimicry is targeting different generalist insectivores rather than specialists, like jacamars. Batesian mimics
Langham • Do older birds attack aposematic butterflies?
289
Table 3
Multivariate logistic regression of rufous-tailed jacamars sampling behavior (attack or avoid) as
predicted by sex and morphological traits
Variable
Parameter
estimate
Wald v2
Probability . v2
Likelihood
ratio v2
Odds ratio
Intercept
Tail length
Bill
Tarsus
Sex (f)
Mass
Wing length
Tail 3 sex
Tail 3 wing length
31.049
0.203
0.059
0.211
0.150
0.034
0.028
0.054
0.029
3.96
7.22
0.79
0.78
0.22
0.04
0.02
0.40
0.37
0.047
0.007
0.374
0.377
0.639
0.835
0.899
0.523
0.544
—
8.793
0.818
0.804
0.219
0.016
0.042
0.407
0.375
—
0.004
0.247
0.254
1.351
0.613
0.775
4.030
14.826
Results are for the first trial (n ¼ 80). Bold indicates p , .01.
are nontoxic butterflies that have wing patterns similar to
those of toxic models, occur at low frequencies, and are often
quite imperfect mimics. Because many aposematic patterns
occur in any lowland tropical locale, predators must also learn
to avoid local models while still attacking novel models or
hybrids in sufficient numbers to counter variation arising
through dispersal and mutation.
There is little evidence that neotropical bird families, with
the exception of jacamars, attack adult butterflies with any
regularity. Of those insectivorous species that do, most seem
to attack opportunistically or focus on mainly palatable species or larval stages of butterflies (e.g., Fitzpatrick, 1985;
Sherry, 1984). Jacamars are the only family known to regularly
consume brightly colored butterflies (Burton, 1976; Chai,
1986, 1996), but Myiarchus and Tyrannus tyrant flycatchers
are prime candidates among the flycatchers for some role in
mimicry evolution (e.g., Pinheiro, 1996, 2003). There are
many common, brightly colored butterflies in the tropics that
are not toxic, yet very few bird species seem to eat these abundant prey (but see Burger and Gochfeld, 2001). Among 16
species of tyrant flycatchers in lowland Costa Rica, Sherry
(1984) found that stomachs contained an average of 1.8%
adult lepidopterans. In contrast, jacamars are frequently observed attacking butterflies, have many butterfly wings under
perches and near nests, and have diets containing up to 30%
adult lepidopterans (Burton, 1976; Tobias, 2002; Langham,
personal observation).
The hypothesis that all insectivorous birds contribute
equally to the maintenance of warning-color mimicry predicts
highly acute, pattern-specific aversion in all insectivores. This
prediction contrasts with the generalized pattern aversion
shown for birds fooled by Batesian mimicry. Indeed, the main
conclusion of the experiments with blue jays (C. cristata) was
that generalized aversion to warning-color patterns allows
Batesian mimicry to exist (Brower et al., 1963). Furthermore,
many Mullerian mimics often have only broad pattern convergence, such that the wing patterns are both orange and black
overall but differ in the specific placement of each wingpattern element. Generalized aversion to warning-color patterns also allows broadly similar mimicry without fine-scale
convergence to operate as an effective antipredator strategy.
The existence of both broad and fine-scale mimics, even
within the same habitat, suggests that these mimicry complexes may target different predators. It is possible that some
birds have fine discrimination and pattern-specific aversion
while others have generalized aversion. Jacamars clearly belong to the former group while jays belong to the latter. Less
clear is where flycatchers and other insectivores lie on the
spectrum. Pinheiro (1996, 2003) showed that tropical kingbirds, Tyrannus melancholicus, were willing to attack many kinds
of butterflies, but whether these kingbirds just attacked all
butterflies or showed discrimination is critical to the question
of mimicry. Birds that attack and kill every butterfly that passes
by have the same selective effect as birds that never attack
butterflies.
I thank D. Winkler, J. Fitzpatrick, G. Hume, J. Schuetz, and S.
Beckwith for valuable discussion and review of the manuscript and
J. Hite, J. DaCosta, B. O’Shea, K. Belinski, S. Baldwin, and J. Martin
for field assistance. This research was supported by a National Science
Foundation dissertation improvement grant (DEB-9903715).
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Relationship between initial tail length of male and female rufoustailed jacamars and subsequent change. Filled circles denote males
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