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Biological Journal of the Linnean Sociely (1986), 29: 161-189. With 3 figures
Field observations and feeding experiments
on the responses of rufous-tailedjacamars
(Galbula ruficauda) to free-flying
butterflies in a tropical rainforest
PENG CHAI
Deparlmenl of <oology, Universily of Texas at Austin, Austin, Texas 78712, U.S.A.
Xeceiiied 12 Dertmber 1985, accepted f o r publication 12 June 1986
Wild rufous-tailed jacamars (Calbula rujcaudu) were shown to prey frequently, but selectively, upon
butterflies in a Costa Rican rainforest. Two individually caged birds (a male and a female) were
further tested with over 1000 butterflies of I14 morphs. Both wild jacamars and the two captive
individuals were able to capture and handle all kinds and sizes of local butterflies. These butterflies
(and other winged insects) were recognized by the jacamars as prey only through their movement.
l h e captive birds discriminated between an unacceptable group of butterflies, which generally fly
slowly or regularly, are warningly coloured and mimetic, with transparent, or white, orange, red,
and/or black coloration, and an acceptable group that generally fly fast or erratically, are cryptic
(on one or both sides), and have yellow, orange, green, blue, and/or brown coloration. These
different morphological and behavioural characteristics of butterflies presumably helped the
jacamars to assess their palatability.
Most individuals of unacceptable butterflies (e.g. Baffus and Purides (Papilionidae), some
Pieridae, Diaethria and Callicore (Nymphalinae), Heliconiinae, Acraeinae, Ithomiidae, and
Danaidae) were sight-rejected by the male jacamar (Jacamar 2), and many of the same were also
sight-rejected by the female (Jacamar 1). In cases when the above butterflies were attacked, they
were quickly released and usually unharmed. The captive female bird, after long periods without
food, consumed many pierid and heliconiine butterflies that were consistently rejected by the male
for their distasteful and dangerous qualities. I n contrast, palatable butterflies (e.g. Papilio,
Charaxinae, most Nymphalinae, Morpho, Brassolinae, and Satyrinae) were usually quickly attacked
and consumed. The captive jacamars were able to discriminate between the very similar colour
patterns of some Batesian mimics and their models, and could memorize the palatability of a large
variety of butterflies. The discriminatory abilities of specialized insectivorous birds such as jacamars
are likely to play a major role in the evolution of neotropical butterfly mimicry.
butterfly predator - rufous-tailed jacamar - discrimination and
learning capture and handling - neotropical butterflies - butterfly flight pattern - butterfly colour
pattern - warning coloration - mimicry - palatability.
KEY WORDS:-Specialized
~
CONTENTS
Introduction . . .
Materials and methods
Study species . .
Study site.
. .
Field observations.
Feeding experiments
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0 1986 The Linnean Society of London
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P. CHAI
Results . . . . . . . . . . . . . . . . .
Responses of wild birds . . . . . . . . . . .
Responses of caged birds . . . . . . . . . . .
Characteristics in colour patterns and flight patterns of local butterflies
Capture and handling of butterflies by caged birds . . . . .
Discriminatory and learning abilities ofcaged birds. . . . .
Discussion. . . . . . . . . . . . . . . .
Adaptations of butterfly predaton . . . . . . . . .
Adaptations of unpalatable butterflies . . . . . . . .
Conclusions . . . . . . . . . . . . . . .
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Acknowledgements
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References
Appendix. . . . . . . . . . . . . . . .
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INTRODUCTION
Birds are widely considered to be the primary selective agent for mimicry in
butterflies (e.g. Marshall, 1909; Swynnerton, 1915a; Carpenter, 1939; Jeffords,
Sternberg & Waldbauer, 1979; Bowers, Brown & Wheye, 1985). After
unpleasant experiences with an unpalatable ‘model’ insect or with artificial
prey, numerous species of birds (e.g. chickens, rollers, hornbills, wood-hoopoes,
tyrant flycatchers, jays, tits, starlings, blackbirds, grackles, tanagers and
sparrows) have learned to avoid other similar prey: ‘mimics’ which exhibit at
least some of the characteristics of the models (see reviews by Rettenmeyer,
1970; Ford, 1975; Turner, 1977; Brower, 1984; Huheey, 1984). Previous
butterfly feeding experiments recorded the responses of birds to dead or
immobilized specimens, with the implicit assumption that similar responses
would be elicited in these and other birds by live prey in nature. Although a
taxonomically diverse set of bird species has been tested with inactive butterflies,
except for European rollers (Corucius gurrulus) and fork-tailed flycatchers
(Muscivoru tyrunnus), aerial hawkers of flying insects, all are omnivorous, foliage
or ground gleaners, which seldom attack butterflies in the field. Different
specializations and foraging modes of predators should, however, impose
different selective pressures on their sensory and motor capacities, and such
predators should thus vary in relative discriminatory ability when sampling
novel prey (Alcock, 1971).
A predator’s tendency to learn prey attributes and to avoid similar prey after
an unpleasant experience with a potential prey species is the selective force
generating Batesian and Miillerian mimicry (Fisher, 1958). Moreover, predators
should reduce sampling of the model/mimic complex as the availability of
alternative prey increases (Holling, 1965; Dill, 1975; Luedeman, McMorris &
Warner, 1981). Two antagonistic selective forces have been proposed to operate
simultaneously on the predators: pressure to decrease sampling, thereby
reducing the possibility of poisoning or physical harm, us. pressure to sample
potential prey for palatable items (e.g. Batesian mimics), increasing feeding
efficiency (Fisher, 1958; Huheey, 1976; Nonacs, 1985). The first of these
selective forces may be important to opportunistic butterfly predators, which
feed mainly on fruits, less mobile arthropods, and small vertebrates. Having had
a bad experience with a model, these generalist predators should subsequently
avoid sampling from that mimetic group. O n the other hand, frequent sampling
may be more important for specialized predators, which ought to be able to
distinguish between unpalatable models and edible mimics, because adult
Lepidoptera are their major source of food, for at least part of the year.
RESPONSES OF JACAMARS T O BUTTERFLIES
I63
A predator’s discriminatory and learning abilities and its ability to capture
and handle a given prey are likely to be influenced by many other factors.
Particularly in tropical rain forests, a wide array of feeding behaviours may
evolve in predacious birds because of their sedentary life styles (Mayr, 1969;
Morse, 197 1; Willis, 1974), long periods of post-fledging parental care (Fogden,
1972; Skutch, 1976), long lifespans (Snow & Lill, 1974; Lopes, Sacchetta &
Dente, 1980) and specialized niches (Terborgh & Weske, 1969; Lovejoy, 1974;
Sherry, 1984). Moreover, tropical insectivorous birds encounter high levels of
insect species diversity and of aspect diversity (Ricklefs & O’Rourke, I975),
which should further reinforce selection for improved discrimination and
learning.
In tropical rain forest habitats, some predators have, in fact, become highly
specialized on certain groups of prey. Probably only exceedingly skilled
predators such as these could, by selective consumption of prey items, transform
incipient mimics into the astonishingly similar-looking morphs which are
frequently found among members of tropical mimicry complexes (Papageorgis,
1975; Gilbert, 1983). In addition, by eliminating the mutants which have only a
general similarity to other members of a mimicry complex, such predators may
suppress convergence among different Mullerian mimicry rings. The expansion
of colour patterns into new areas may also be restricted by the tendency of local
predators to sample prey with unfamiliar colour patterns (Benson, 1972; Smith,
1979; Turner, 1981). Different patterns may thus become locally isolated as a
result of the sedentary nature of tropical forest birds. The high degree of
development in insect mimicry in the tropics probably results from such tight
associations between local groups of predators and prey.
The responses of the rufous-tailed jacamar (Galbula ruficauda), to local, live
butterflies, was investigated in a Costa Rican tropical rainforest. Butterflies were
chosen for this study because they comprise a significant fraction of the
jacamar’s diet (Skutch, 1963), and because the relationships between their
colour patterns and palatability are generally understood (Brower, 1984). In
this initial study the responses of wild and caged birds to free-flying prey were
assessed by addressing the following questions: (1) which butterflies are
attacked, and which are avoided? (2) do these two groups of butterflies differ
from each other in colour or behaviour? (3) how consistent is the response of
any given jacamar to a particular butterfly morph? (4) do these responses reveal
discrimination and learning by the jacamars? (5) do the colour patterns of the
avoided butterflies conform to those of ‘aposematic’ or ‘warningly-coloured’
species identified in experiments with other birds?
MATERIALS AND METHODS
Study species
Jacamars are members of the neotropical family Galbulidae (Haffer, 1974).
The long, slender bill of these agile, aerial insectivores facilitates handling prey
with large bodies and/or wings, and helps them to avoid the sting of venomous
prey (Sherry, 1983). Consequently, their diet includes a high proportion of
insects that are generally avoided by other birds.
The black-chinned race of the rufous-tailed jacamar (C;.ruJicauda melanogenia)
is common in the lowland forests of Central America. Adults weigh 25-30 g and
I64
P. CHAI
have a bill length of 45-50 mm. Preferred habitat is open forests and older
second growth, especially along streams, where they perch on exposed branches
and sit and wait for passing insects. Upon sighting a potential prey item, the
bird takes flight, and often an elaborate, lengthy pursuit ensues. The bird
returns to its perch to handle any captured prey (Skutch, 1937, 1963). Although
they are often reported to attack butterflies as large as species of Morpho
(forewing length over 7 cm), jacamars are also known to ignore aposematic
butterflies (Belt, 1874; Sherry, 1983; Skutch, 1963, 1983). Moreover, the unique
mark left by its forcep-like bill has been found on the wings of many butterflies,
especially those known to be unpalatable (e.g. in Carpenter, 1939; Benson,
1972).
Study site
Corcovado National Park is a tropical rainforest on the Osa Peninsula of SW
Costa Rica (detailed in Hartshorn, 1983). The study site, Sirena, is located in
the lowland sector of the park (8"28'N, 83'37'W) and is largely surrounded by
second growth woods. This second growth is a result of agricultural activities in
the area before the establishment of the park in 1975, and is interspersed among
patches of forest which have been disturbed to different extents in the past. The
numerous forest edges and older second growth in this area have a moderately
high diversity of butterflies (DeVries, 1983), and support a large resident
population of Galbula rujcauda melanogenia, the only common jacamar in this
area.
Field observations
The foraging behaviour of breeding and non-breeding Galbula rujcauda
melanogenia (henceforth jacamars) was observed at Sirena for a total of 26 h
(accumulated over 17 days) in July 1980, and 94 h (20 days) from late June to
July 1983. The birds were located by their vocalizations, or by checking their
favourite hunting perches. They were generally unafraid of humans, and
tolerated approach to within 10-15 m of their perches. Observations of sallies
and attacks on prey items included the time, distance and success of each sally,
the identity of prey, and the way in which prey was handled after capture.
Large dragonflies, cicadas and butterflies could be identified with binoculars,
and smaller insects were classified to order whenever possible. In order to record
as many prey identities as possible, data were gathered as long as the jacamar
remained within sight. Jacamar bill size served as an approximate scale of prey
size. The wings of dragonflies and butterflies, which were usually removed by
the birds and fell below the perch, were collected for specific identification. I
also recorded the butterflies that passed the foraging jacamars (perching birds
that were actively looking for prey) but were not attacked. Most butterflies
could be identified to species, and all to genus.
Feeding experiments
The two birds used in the feeding experiments were captured with mist nets
in the Sirena forest. After 3-4 days in captivity each readily attacked insects
RESPONSES OF JACAMARS T O BUTTERFLIES
165
released into their cages under my observation. Jacamar 1, an adult female
observed with a fledgling in 1980, was held in a 0.6 m3 cylindrical cage (0.9 m
high) hung inside the forest for 35 days in July-August 1981. Two branches
were set across her cage about one-third of the way between top and bottom to
provide support and to serve as perches. Jacamar 2, a male, was maintained in
a 12 m3 aviary ( 3 . 6 1.8
~ x 1.8 m) under shade trees for 64 days in
August-October 1983. One long branch placed in the middle of the aviary
served as a perch. At the conclusion of the experiments, both birds were
released. Indeed, Jacamar 1, accompanied by another male, attended two
nestlings in a nearby nest tunnel throughout the 1983 study period. The
following year Jacamar 2 was found raising three nestling with another female.
These observations reinforce speculations that jacamars are highly sedentary.
Both birds were fed a diet of live insects, and did not show any signs of illness
throughout the experimental period. Their diet comprised locally caught
palatable insects, mostly dragonflies, cicadas and lepidopterans, but also
grasshoppers, katydids, wasps and flies. Each bird was maintained without a
strict feeding scheme, and was fed about five or six times a day (including the
feeding experiment) with varying amounts of food each time. All insects fed to
and/or eaten by the bird were recorded. The average weight of each insect
morph was obtained by measuring several individuals to the nearest 0.1 g. This
provided an estimate of the total mass of insects consumed by each bird each
day. Except for individuals of the abundant, palatable butterfly species. Anartia
fatima, A . jatrophae, and Junonia evarete, which were used as food when other
insects were not easily captured, butterflies were offered to the bird only during
feeding experiments.
A typical daily schedule went as follows: the bird was fed to satiation or
nearly so early every morning. Butterflies were netted in the morning from
around 08.00 hours. The feeding experiment, using butterflies caught that
morning, was begun at midday or in early afternoon. By then the bird, which
had not eaten for 3 or 4 h, was very hungry. If interrupted by bad weather, the
feeding experiment was postponed. Usually only one feeding experiment was
conducted each day. However, if the first feeding experiment was conducted
early, and weather permitted, a second feeding experiment was sometimes
conducted in the afternoon. The bird was always deprived of food for 3 or 4 h
before any feeding experiments.
Four different methods of presenting butterflies to the jacamars were used in
this study, each designed to investigate a different aspect of jacamar feeding
behaviour and responses to the various butterfly species. Method 1 tested the
general pattern of jacamar response to local butterflies. Jacamar 1 was tested
with this method only, and Jacamar 2 was tested exclusively with this method
for the first 31 days of its study period.
During each feeding experiment using method 1, a combination of different
butterflies, each representing a morph, was sequentially offered to the birds. (I
refer to butterfly morphs instead of species for two reasons: first, some species
contain two distinct colour morphs; secondly, some congeners are so similar that
they can be distinguished only with close examination, and are treated here as
one morph (see Appendix). Butterfly species combined as one morph for
analysis do not show any palatability difference to jacamars.) Although each
morph was tested only once in any given experimental period, whenever
I66
P. CHAI
possible other individuals of the same morph were used on different days. Some
rare, palatable butterflies could, however, only be tested once or twice.
Specimens of some uncommon, unacceptable species that survived rejection by
the birds were maintained in captivity for repeated testing. In such cases the
bird saw the same individual for two to four trials. In order to keep the bird
hungry and responsive as long as possible, unacceptable insects, or morphs
whose palatability was uncertain, were offered first, followed by palatable ones.
T o minimize the possibility that the bird learned this predictable sequence, the
number of butterflies offered during each feeding trial was varied greatly, from 2
to over 20 depending on the size and acceptability of butterfly morphs used.
More morphs could be offered if most of them were unacceptable, and the bird
therefore remained hungry. Contrarily, two large, acceptable butterflies like
Caligo (each weighs 0.8-2.0 g) could satiate the bird quickly.
In each feeding experiment, I held a butterfly between my fingers, and then
lifted my arm to release it. The birds soon learned to anticipate these
movements, and stared at my hands until the insect’s release. Butterflies were
presented one at a time. Jacamar 1 usually perched on the upper perch, and the
butterfly was passed through a slot at the bottom of the cage. I then sat beside
the cage to record her response. For Jacamar 2, I sat at the darker side of the
aviary to release the butterfly, and would stay there until the end of the feeding
experiment. Most butterflies when released would fly upward or toward the
opposite brighter side and across both birds’ field of vision. However, all satyrids
tended to fly downward and toward the shadier side, but the bird eventually
noticed their presence and initiated an attack.
I stopped offering butterflies to the bird when either all butterflies had been
tested, or when about 2 g of prey had been consumed. In the latter case, the
bird would often begin to show signs of satiation such as slow responses and
prolonged handling times. Because most butterflies, especially unpalatable ones,
continued flying or fluttering their wings while climbing along the wall as long
as they remained in the cage, I assumed that any unattacked insect had been
seen but was deliberately ignored by the bird. I sometimes beat the cage wall to
make motionless butterflies fly again. Uneaten insects were left in the cage for at
least 30 min. The feeding experiment usually lasted between 1 and 4 h from the
time I started offering butterflies until I stopped observing the bird and the
confined, uneaten butterflies. All uneaten butterflies were removed at the end of
each session. At this time the jacamar was given other insects (dragonflies,
cicadas and flies). At the end of each day, the bird was fed to satiation or nearly
so.
Method 2 was used to investigate the response of Jacamar 2 to butterflies
painted with artificial colours. I t was conducted after methods 1 and 3 had been
used, and the results will be published elsewhere (Chai, in press).
Method 3 investigated the ability of Jacamar 2 to discriminate among
butterflies with similar colour patterns. In 1983, after a long period of drought,
rains caused a sharp increase in butterfly abundance making many previously
uncommon mimetic butterflies available for experiments. Six feeding
experiments were carried out to test Jacamar 2’s discriminatory ability. I n each
experiment, two butterflies of different morphs from the same mimicry complex
were randomly selected and released together in front of the bird. The choice of
the bird was then recorded.
RESPONSES OF JACAMARS T O BUTTERFLIES
I67
Method 4 was conducted at the end of the study to determine if Jacamar 2
remembered the palatability of those butterfly morphs tested during previous
feeding experiments. In the morning on three separate days, a mixture of
previously acceptable or unacceptable butterflies was introduced into the
jacamar’s cage. These butterflies were left in the cage throughout the day. The
bird was free to attack, and the sequence of his attacks on and consumption of
butterflies was recorded until the end of the day.
The bird’s response to each butterfly individual was categorized according to
the scheme developed by Brower (1958a, b, c): N-not
touched = ignored,
rejected on sight. The bird did not attack ( = sample) the butterfly; Ppecked = rejected after tasting. The bird attacked, tasted and then dropped the
butterfly, which could still fly well; K-killed = rejected after tasting. The bird
attacked and seriously injured the butterfly, usually due to repeated beatings
against the perch, but did not eat it. Butterflies which survived these attacks
were unable to fly; E-eaten = accepted. The bird attacked and ate the
butterfly, usually after removing some or all of its wings.
In each experiment, the time to attack, or elapsed time in h : min from the
release of the butterfly until the attack, if any occurred, was recorded. Quick
attacks made within a minute (time to attack = 0 : 00) after the release of the
butterfly were noted. Since the butterfly was confined with the bird, if the
butterfly escaped from the initial attack, the bird could try again and might
make several thwarted attacks before a final success. The number of times that
butterfly escaped from the bird’s attack was also recorded.
RESULTS
Responses of wild birds
The entire diet of rufous-tailed jacamars observed in the field consisted of
winged insects that were either intercepted in the air or snatched from the
vegetation (Fig. 1). Jacamars always caught, and carried, a single item of prey
at a time. Small insects were taken most frequently. However, a large
proportion of the diet mass, especially of prey delivered to the young, was
composed of dragonflies (Odonata), cicadas (Homoptera), butterflies and
skippers (Lepidoptera), and other large, flying insects.
During the field observations, a total of 109 lepidopterans (28 butterflies
(Papilioidea), 49 skippers (Hesperoidea), and 32 moths) were captured and
eaten by wild jacamars. Many of these insects, including most butterflies within
the Charaxinae and Nymphalinae, and virtually all the skippers, are fast and
evasive fliers. Insect wings collected under jacamar perches suggest that they
can capture and consume very large butterflies, such as Morpho and Caligo
(butterflies of these two genera have forewing length of over 7 cm). O n three
occasions, the male jacamar which paired with Jacamar 1 in 1983 was seen
successfully capturing and handling Caligo butterflies (the genus containing the
largest neotropical butterfly). Also, numerous wings of this genus and of other
large butterflies were collected under his favourite perches. Other jacamars,
however, ignored Caligo in the field (Table 1).
In addition to the 28 butterflies eaten by the jacamars, 129 individual
butterflies were observed passing foraging jacamars but ignored (not touched),
and three were captured but released (pecked) (Table 1). The butterfly species
P. CHAI
168
20
Odonata Orttmptera HomoptemLepidoptem Diptem Hymenoptera Mix.
Figure I . Proportion of diet of wild rufous-tailed jacamars represented by insect classes.
Miscellaneous small insects ( < 1 cm), mostly Diptera and Hymenoptera, were immediately
consumed and could not be identified. A, Non-breeding birds, N = 306. B, Adults feeding young,
N = 309. C, Prey delivered to young, N = 270. m, Number of prey; 0,estimated weight; .
,
butterflies (Papilionoidea).
that wild jacamars were seen eating were also acceptable to the caged birds in
feeding experiments. However, wild foraging jacamars ignored many passing
palatable butterflies such as Phoebzs (Pieridae), nymphalids and satyrids, which
were readily consumed by the caged birds. Interestingly, Consul fabius
(Charaxinae), a semi-cryptic Batesian mimic, was captured and fed to the
young on three occasions in 1983 (once by the male bird, twice by the female,
i.e. Jacamar 1). The underside of Consul fabius resembles a dead leaf, and the
butterfly is cryptic at rest, but its upperside mimics the unpalatable Heliconius
ismenius to such an extent that it is warningly coloured in flight. The three
pecked and rejected butterflies, Battus polydamas (Papilionidae), Perrhybris pyrrha
female (Pieridae) and Eueides lybia (Heliconiinae), could still fly after their
RESPONSES O F JACAMARS TO BUTTERFLIES
169
release. Individuals of aposematic species such as Parides, Heliconius and
ithomiines were entirely ignored even though they sometimes flew very close to
foraging jacamars that were watching passing insects. Frequently I observed
jacamars sally out and return without prey in the bill. Such ‘missed’ attacks
account for about 40% of all attacks observed. Since it is extremely hard to see
the bird and its prey at the same time, only eight incidents in which the
butterfly actually escaped from a jacamar’s attack and/or was chased without
being captured were observed. Most observed captures occurred just after a
butterfly had landed close to a perching jacamar, or when a butterfly flew across
an open space in which the bird had room to manoeuvre.
Table 1. Responses of wild jacamars and two individually caged jacamars to
free-flying butterflies. Each number represents one individual butterfly in one
feeding experiment. The final fate of each individual butterfly is assigned to one
of four categories: N = not touch; P = peck; K = kill; E = eat. A butterfly
might be pecked and rejected before being killed or eaten. Such butterflies are
categorized under K or E. Total numbers are listed under each category
Birds’ responses
Butterfly taxa
Papilionidae
Baitus and Parides
Papilio
Pieridae
Ascia, Melete and Penhybris
Appias, Aphrissa and Phoebis
N ymphalidae
Charaxinae
N yrnphalinae
Hamadryas amphinome, H . arcthusa,
Diaelhria and Callicore
all other nymphaliines
Heliconiinae
Heliconiines excluding Philaethria dido
and D y a s iulia
Philaethria dido and Dryas iulia
Acraeinae
Actinote
Ithomiidae
Danaidae
Danaus and Lycorea
Satyridae
Morphinae
Morpho
Brassolinae
Caligo and Opsiphanes
Satyrinae
Lycaenidae
Eumaeus
Arawacus
Riodinidae
Euybia
Wild jacamars
Jacamar I
Jacamar 2
N P K EWings*
N P K E
N
2 3 1 - _ _
4
22--2--17
- 1 _ _ _
3
5
_ _
__
-
20--
9
83 1
I--
- -
-
2
-
1
2
3 - 52
3 - 1
-
I - -
- - -
-
-111
3 8 1 0 2 2 4 3 264
59
7
2 - - 3
3 - - 4
69
P K E
-
1
-
5
-
‘Wings = wings found under the jacamar perches. Each number represents one individual butterfly.
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P. CHAI
I70
Responses of caged birds
Feeding experiments showed that a jacamar’s attack was almost always
elicited by movement of the insect, especially flight. The two caged birds were
unable to detect motionless insects as prey. The average mass of insects
consumed by Jacamar 1 each day was 8.7f2.4 g (mass f 1 s . D . ) ; Jacamar 2
consumed 8.3 f 1.7 g. The food consumed was not significantly different
between the two birds (Mann-Whitney U test: Sokal & Rohlf, 1981).
A total of 218 butterflies representing 62 morphs were offered to Jacamar 1;
938 individuals of 103 morphs were offered to Jacamar 2 (Tables 2 & 3). Table
1 summarizes the response of the experimental jacamars to different butterfly
taxa. Both birds consistently rejected the Aristolochia-feeding Baths and Parides
(Papilionidae) as well as Solanaceae- and Apocynaceae-feeding ithomiines
(except for one individual of Ceratinia tutia eaten by Jacamar 1; larval host plant
information see DeVries, in press). Danaids (Lycorea cleobaea and Danaus gilippus)
which feeds on latex-rich plants of Asclepiadaceae, Apocynaceae, Caricaceae or
Moraceae were unacceptable to Jacamar 2; only one individual Danaus gilzppus
was tested and was also unacceptable to Jacamar 1. Jacamar 1 also rejected
three individuals of Actinote lapitha (Acraeinae) which uses Mikania sp.
(Asteraceae) as larval host plant. The palatability of the Pieridae appears to be
variable. With the exception of Appias drusilla, all crucifer- or caper-feeding
pierids (Ascia and Perrhybris) were rejected by Jacamar 2, but three individuals
of Ascia monuste were eaten by Jacamar 1. The legume-feeding pierids, Aphrissa
and Phoebis, were accepted by both birds. The palatability of the Heliconiinae
which use PassiJEra vines as host plant was also variable. Both Jacamar 1 and
Table 2. Summary of the responses of two caged jacamars to individual
butterflies
Jacarnar 2
Jacamar 1
Unacceptable
butterflies
Inconsistently
Inconsistently
accepted
Acceptable Unacceptable accepted
Acceptable
butterflies
butterflies
butterflies
butterflies
butterflies
~~
Total number of
individuals offered
Birds’ responses
N
P
K
E
Number of individuals
attacked (P, K or E)
Number of individuals
quickly attacked
(within I min)
37
54
127
369
59
510
17 ( 4 6 ~ ~ )24 (44%)
3 (6%)
17 (46%)
0
3(8%)
27 (50%)
0
337 (91%)
29 (8%)
3 (1%)
127 ( l O O ~ o )
0
4
3
6
46
(7%)
(5%)
(10%)
(78%)
(0%)
505 (99%)
20 (54%)
127 (lOOO/o)
32 (9%)
55 (93%)
509 (100%)
14 (4%)
38 (64%)
367 (72%)
3 (8%)
30 (56%)
7 (13%)
ns*(P > 0.3)
0
0
0
56 (44%)
P < 0.001
P < 0.001
P < 0.001
1
3
(0%)
(1%)
1
ns (P > 0.1)
P < 0.001
*Fisher’sexact test (one-tailed), ns = not significant; the significance level is reduced to 0.01 due to repeated
comparisons (Everitt, 1977).
RESPONSES O F JACAMARS TO BUTTERFLIES
171
Jacamar 2 consistently consumed all Philaethria dido and Dryas iulia offered to
them. However, Jacamar 2 rejected all other heliconiines, while Jacamar 1
consumed many more heliconiines, including Dione juno, Eueides aliphera, E. lybia
and six Heliconius species (Appendix). Except for Hamadryas amphinome,
H. arethusa (larva feed on Dalechampia sp., Euphorbiaceae), Diaethria marchalii
and Callicore ntacama (larva feed on Ulmaceae and Sapindaceae), most
nymphaliines were acceptable to both birds. Papilio, Charaxinae, Morpho sp.,
Brassolinae and Satyrinae were also acceptable to both birds. Very few species
of the Lycaenidae and Riodinidae were tested, so the palatability of these
groups is not discussed here.
Hence, overall the responses of both birds to local butterflies were very
selective and generally similar, though individual differences in feeding
behaviour did occur. Because of the behavioural differences between Jacamar 1
and Jacamar 2, the palatability of butterflies tested in this study was considered
separately on the basis of their treatment by each bird. For the purpose of this
study, each butterfly morph tested was classified into one of three categories,
based on the response it elicited from each bird: (1) unacceptable-uneatable,
all individuals rejected, including those morphs of which only one individual
was tested (see Appendix); (2) inconsistently accepted-some individuals eaten
individuals eaten, including those
while others rejected; (3) acceptable-all
morphs of which only one individual was tested.
Jacamar 2 (male) initially rejected some boldly patterned and/or mimetic
butterflies which it later accepted (Table 4). Although these butterflies were
accordingly categorized as inconsistently accepted, they were probably
palatable (see below). In contrast, Jacamar 1 (female) not only consumed all
butterflies considered acceptable or inconsistently accepted by Jacamar 2, but
also ate many morphs which Jacamar 2 rejected (i.e. 1 pierid, 9 heliconiines and
'Table 3. Summary of the responses of two caged jacamars to butterfly morphs
Jacamar 2
Jacamar I
Unacceptable
butterflies
Total number of
morphs offered
Number of morphs
attacked
Number of morphs
attacked within 30
min during their first
trial
Inconsistently
Inconsistently
accepted
Acceptable Unacceptable accepted
Acceptable
butterflies
butterflies
butterflies
butterflies
butterflies
21
7
34
50
5
48
15 (71%)
7 (lOOo/o)
34 (100%)
16 (32%)
5 (100%)
48 (100%)
2 (29%)
30 (88%)
9 (18%)
2 (40%)
43 (90%)
6 (29%)
\ns*
uu
P<O.Ol /
(P>0.6)
\
I
P < 0.001
u
(P> 0.2) (P> 0.02)
\u
ns
\
ns
P < 0.001
Number of morphs
attacked quickly
(within I min) during
their first trial
*Fisher's exact test (one-tailed), ns = not significance; the significant level is reduced to 0.01 due to repeated
comparisons.
P. CHAI
I72
1 ithomiine, see above). However, Jacamar 1 did not eat the latter butterflies
quickly when they were offered, but consumed most of them only after long
periods without food, indicating its reluctance. Many of these species were
consumed by Jacamar 1 inconsistently (Table 4). During any given feeding
trial, Jacamar 1 sampled these butterflies in direct proportion to the time it had
been without food; i.e. initially they were tasted and rejected but eventually
many were consumed. In two cases, Jacamar 1 ate four Heliconius butterflies
within an hour without subsequent vomiting or other signs of sickness. Unlike
Jacamar 1, Jacamar 2 was very reluctant to sample butterflies unacceptable to
it, even after long periods of food deprivation. Overall, Jacamar 1 sampled and
consumed a significantly larger proportion of butterflies offered to it than did
Jacamar 2 (butterflies sampled: 177/218 or 81% us. 596/938 or 64%, P < 0.001;
butterflies consumed: 154/218 or 71% us. 551/938 or 59%, P < 0,001; one-tailed
Fisher's exact test: Everitt, 1977).Jacamar 1 also sampled proportionately more
unacceptable butterfly morphs than Jacamar 2 (15/21 or 71% us. 16/50 or 32%,
P < 0.01, one-tailed Fisher's exact test). Many unacceptable morphs were never
touched by Jacamar 2 in any of the feeding experiments.
Characleristics in colour patterns andjight patterns of local buttegies
Local butterflies show many easily noticeable characteristics in both colour
patterns and movement patterns, which tend to be correlated with their
acceptability. In general, unacceptable butterflies are brightly coloured
(aposematic) on both upper- and undersides of wings, and are mimetic. Major
portions of their wings are transparent, white, orange, pink, red and black. In
Table 4. Butterfly morphs inconsistently accepted (some individuals eaten, but
others rejected) by the two jacamars in feeding experiments. Observed responses
to a given morph are shown and arranged according to the order in which
individuals of this morph were offered to the bird
Butterfly species
Jacamar I
Heliconiinae
Eueides lybia
Heliconius ismcnius
Hcliconius hecale
Heliconius melpomene
Hcliconius erato
Hcliconius hcwitsoni
lthomidae
Ceratinia tutia
Sequence of trials
N, N, E, E
P, E, N, E, N, E, N
PE*, N, E, N, E, E, E, N, N , N
E, PE, PE, N, N
N, N, N, E, PE, E, PE, PE, E, E, PE, N, P, P, PE, E, N
N, PE, E, PE
N, PE, N, N, N, N, N
Jacamar 2
Pieridae
Appiar drusilla (6)
Nymphalidae
Hamadyas feronia
Calonephclc nyctirnus (d)
Siproela stelmes
Satyridae
Cithaerias mmandcr
~
*PE: the butterfly was fint pecked and released unharmed, but later the bird attacked again and ate it.
RESPONSES O F JACAMARS TO BUTTERFLIES
Jacamar
173
1
F
S
33
l5 7
111
N
j5
A
N
C
6
7
A
C
19
l4
111 0 0 0 120 0 0 0
b
U
.
A
B
A
U
B
B
h
P
Jacamar 2
S
Figure 2. Corcovado butterflies tested with two caged jacamars categorized according to their flight
pattern, colour pattern and palatability to each bird. Flight pattern: S,slow and fluttering fliers; F,
fast fliers. Colour pattern: C, cryptic on at least one side (usually the underside); N, not cryptic; U,
most wing areas transparent, or white, orange, pink, red or black colours often shown in
unpalatable butterflies; P, most wing areas yellow, green, brown or blue colours often shown in
palatable butterflies; B, colours from both groups are present. Palatability: .
,
unacceptable
butterfly morphs; m, inconsistently accepted morphs; 0 , acceptable morphs.
contrast, a great variety of wing patterns from very conspicuous to highly
cryptic are found among the acceptable butterflies, whose wings usually contain
yellow, orange, green, blue and brown colours. In most of the latter, including
almost all species of the Charaxinae, Nymphalinae and Satyridae, at least one
side of the wings is cryptic and resembles the substrate on which these butterflies
usually land.
About 60% of the unacceptable butterflies, such as Heliconius, Actinote,
ithomiines and danaids, have slow and fluttering wing beats, and usually fly in a
straight, regular path. In addition, almost all have long and slender bodies.
Most acceptable butterflies, on the other hand, are fast and irregular fliers with
short, stout bodies. Some unacceptable butterflies, such as Battus and Parides as
well as most non-Heliconius heliconiines, seem to fly as fast as most acceptable
butterflies, but their flight pattern is straighter and more regular than the
erratic flight path of the acceptable group. Among the butterflies found to be
unacceptable to jacamars, only the pierids and nymphaliines are truly fast,
irregular fliers with fluctuating flight paths (i.e. with flight patterns very similar
to those of most acceptable butterflies). Interestingly, the presumed Batesian
mimics, Papilio anchisiades female, P . androgeus female, Consul fabius and Phyciodes
P. CHAI
I74
(Eresia) eutropia (Nymphalinae), all fly like their presumed models (Bullus sp.,
Parides females, Heliconius ismenius and Mechanitis sp. (Ithomidae), respectively).
Figure 2 categorizes the butterfly morphs tested in feeding experiments with
Jacamar 1 and Jacamar 2 according to their major flight pattern and colour
pattern differences. It can be seen that jacamars chiefly attacked and consumed
cryptic and/or fast-flying butterflies that are harder to detect and/or to catch,
and tended to avoid conspicuous and/or slow-flying butterflies that are easier to
detect and/or to catch. This response tendency with respect to butterfly
morphological and behavioural characteristics was more stongly expressed in
Jacamar 2 than Jacamar 1. Jacamar 1, after long periods without food, attacked
and consumed many heliconiines which are both slow-flying and conspicuous,
mimetically coloured.
Capture and handling of buttegies by caged birds
Caged jacamars were able to capture and handle all butterflies offered
(except some unacceptable morphs which were never touched), but handling
time depended on butterfly size. Small acceptable butterflies (forewing length
less than 3 cm) were often immediately ingested whole while still living.
Medium and large butterflies were first seized by the head, thorax, junction
between head and thorax, or wing base, then weakened by knocking their head
and thorax against the perch. When the butterfly reduced struggling, the bird
removed the wings, a process which accounted for most of the handling time.
Each wing was removed by holding the insect a t the base of one forewing and
repeatedly beating it against the perch until the wing was broken off. This
procedure was repeated until all four wings were gone. Unless the butterfly was
very big, the bird often did not complete its handling and ingested some wings
(usually the softer hindwings) along with the body, After handling the butterfly,
the bird positioned it and swallowed it head first. Handling time for the large,
Table 5. Total number of times that butterflies escaped from the attack or were
taste-rejected by two caged jacamars
Jacamar I
Jacamar 2
Inconsistently
Inconsistently
Unacceptable accepted
Acceptable Unacceptable accepted
Acceptable
butterflies
buttertlies
butterflies
butterflies
butterflies
butterflies
~~
Total number of
butterflies offered
Total number of times
that the butterflies
escaped
Total number of times
that the butterflies
were taste-rejected
Rejected after one peck
Rejected after further
handling
~~
~
31
54
127
369
59
510
0
0
80
2
20
303
33'
28
21
17
0
0
47
10
36
6
0
0
5
4
0
11
4
0
~
*Some individual butterflies were tasted and then rejected more than once during the same feeding
experiment; thus more than one taste-rejection of a given butterfly was possible. This number is different from
those for P and K, which represent the final fate of an individual butterfly in a feeding experiment.
RESPONSES OF JACAMARS T O BUTTERFLIES
175
strong fliers like Archaeoprepona, Historis (Nymphalinae), Caligo and Morpho
butterflies averaged 9 min with a maximum of 40 min. The tough body of these
large butterflies made it hard for the birds to kill them and to remove their
wings.
Even in the cage, many individual butterflies, almost entirely representing
acceptable morphs, were able to escape the bird’s attack (Table 5) if they flew
just before being seized, if the bird bit at the wrong place (such as the wings), or
if they struggled strongly and slipped out of the bird’s bill. The previously
mentioned large and strong butterflies were also very difficult for the birds to
catch. Because of their size and strength, these butterflies usually had to be
attacked and handled repeatedly before they finally wore out and could not
escape any more. After several missed attacks and/or unsuccessful handling, the
bird often waited a while before initiating another attack. Presumably due to
the difficulty of subduing this type of butterfly, except after long periods without
food the jacamars did not attack these species quickly, thus treating them like
unacceptable ones, at least initially. As a result, some individuals were not
consumed during the feeding trials (1P for Morpho peleides, and lN, 2P, 1K for
two Caligo species; see Appendix). All of them were, however, eventually
subdued and eaten when I offered them again to make sure of their palatability.
These butterflies were therefore considered acceptable butterflies.
Unacceptable butterflies seldom escaped if the bird initiated an attack, but
they were quickly rejected if captured (Table 5 ) . My preliminary results
indicate that a bird could detect an unacceptable butterfly after a single peck.
Even if the bird continued to handle the butterfly by biting it several times, or
beating it against a perch, this behaviour only lasted a few seconds. Thus
butterflies were seldom killed after taste rejection. Indeed, the large,
unacceptable Parides species and danaids appeared to be especially tenacious,
and could still fly well after several days of multiple attacks.
In those cases where the capture and handling of butterflies by wild jacamars
were actually observed, although the handling time was not recorded, no
substantial differences in handling behaviour between wild and caged jacamars
was detected.
Discriminatory and learning abilities of caged birds
In general, both birds ignored or delayed their attacks on butterflies which
they considered to be unacceptable, whereas acceptable butterflies were usually
attacked quickly (Table 2). This very distinct response was shown from the first
time a given morph was tested (Table 3).
A few unacceptable morphs, however, were quickly and/or repeatedly
attacked in feeding experiments even though they were rejected after tasting:
Diaethria marchalii, Actinote lapitha, Melinaea scylax and Mechanitis lysimnia for
Jacamar 1; Melete florinda (Pieridae), Hamadryas amphinome, H. arethusa, Diaethria
marchalli, Agraulis vanillae, Eueides aliphera, Lycorea cleobaea and Danaus gilippus for
*Jacamar 2. Melete florinda, Diaethria marchalii and the two Hamadryas species fly
fast and erratically like most acceptable butterflies. The colour on the wings of
Actinote lapitha, Lycorea cleobaea and Danaus gilippus is brownish and somewhat
cryptic. Agraulis vanillae, Eueides aliphera, Melinaea scylax and Mechanitis lysimnia
are members of large mimicry complexes which are invaded by many Batesian
P. CHAI
176
Figure 3. Wing patterns of mimetic butterflies tested with a caged jacamar (Jacamar 2), see Table 6
for results.
mimics such as Dryas iulia, Consul fabius and Phyciodes (Eresia) eutropia. Each of
these butterflies, then, shares some characteristics with edible butterflies which
probably confused the birds and rendered them prone to attack.
In the feeding experiments using method 3, which tested Jacamar 2’s ability
to discriminate between a pair of similar mimetic butterflies (Fig. 3 & Table 6),
it clearly discriminated between the edible Consul fabius and the unacceptable
RESPONSES OF JACAMARS TO BUTTERFLIES
177
members in the Tiger mimicry complex (see Papageorgis, 1975; DeVries, in
press, for general descriptions of neotropical butterfly mimicry complexes). It
also appeared to differentiate between Lycorea cleobaea and Heliconius ismenius, for
it attacked the danaid immediately and continuously (seven times) when it was
first presented, while H . ismenius, with which the bird was already familiar, was
ignored. Jacamar 2 also quickly attacked and consumed Dryas julia while almost
entirely ignoring the other two heliconiines (Dione juno and Eueides aliphera) of
the Orange mimicry complex. Among bright, uniformly coloured pierids, all
pure white forms (genus Ascia, male Appias drusilla and male Perrhybris pyrrha)
were rejected, b u t the partially white female Appias drusilla (see below) and the
creamy white Aphrissa boisduvalii were readily consumed.
Papilio androgeus females that mimic unacceptable Battus species (e.g. B. belus)
were quickly attacked and eaten in all trials (Appendix). The presumably edible
Papilio anchisiades female, which mimics unacceptable Parides females, was
untouched. The bird also did not touch Phyciodes (Eresia) eutropia, a presumed
Batesian mimic in the Tiger mimicry complex. Females of the sexually
dimorphic Appias drusilla, greyish-white with darker margins and yellow patches
on the wings, were quickly eaten upon first presentation. Conversely, pure white
males, resembling the unacceptable Ascia monuste, were rejected by Jacamar 2 for
the first four presentations. After that, all five males presented were eaten
(Table 4).
Three lines of evidence, all from the more extensively tested Jacamar 2,
suggest that the palatability of some local butterflies was learned by sampling.
First, most unacceptable butterflies rejected by Jacamar 2 were tested
Table 6. Response of a rufous-tailed jacamar (Jacamar 2) to similar mimetic
butterflies. In each feeding experiment, two individuals of different species in
the same mimicry complex were randomly selected and released together
(method 3 )
Response within
I min after the release
N
P
K
Tiger mimicry complex
Perrhybrzs pyrrha ( 0 )
Heliconius ismenzus
Melinaea sglax
Lyrorea rleobaea
Consul fabius
1 7 - - 1 1 - - 4 I
-
Orange mimicry complex
Agraulis uanillae
Dione juno
Eueides aliphera
Dryas iulia
1
1 1
12
9
White mimicry complex
Asria limona
Ascia monuste
Perrhybris pyrrha (3)
Appias drusilla ( 8 )
Appias drusilla ( 0 )
Aphrissa boisduoalii
2
2
-
-
-
E
N
P
K
E
I
16
10
1
1
1
-
-
-
-
-
-
-
4
I
-
14
-
.-
-
-
-
1 - - - 1
- -
Response observed
within the 30 min trial
16
-
-
9
2 - 1 1 - - 1 1 1
1 -
-
-
-
18
P. CHAI
I 78
repeatedly. Each of the 16 taste-rejected morphs was offered 3-20 times
(mean = 10). But 14 out of these 16 morphs were sampled only once (eight) or
twice (six). Of the eight sampled once, six were sampled at the first trial.
Therefore, after one or two sampling trials, Jacamar 2 learned to avoid most of
these unacceptable morphs.
Secondly, Jacamar 2’s consumption of certain boldly patterned and/or
mimetic morphs was inconsistent (Table 4). It initially rejected male Appius
drusilla, Hamadryas feronia, male Catonephele nyctimus, Siproeta stelenes
(Nymphalinae) and Cilhuerius menunder (Satyrinae), but over time learned to
accept them. Jacamar 1 showed no such uncertainty, and attacked and
consumed the last three butterfly species immediately (no individuals of the first
two species were available during the period Jacamar 1 was held in captivity).
Thirdly, the three modified feeding experiments (method 4: simultaneously
offering a mixture of acceptable and unacceptable butterflies) conducted at the
end of my study showed that Jacamar 2 still remembered the palatability of
those butterfly morphs tested during previous feeding experiments. It made no
mistakes (i.e. it did not attack unacceptable butterflies as long as acceptable
ones were available), and showed good discriminatory ability and memory
(Table 7). The three attacks on unacceptable butterflies occurred only after it
had consumed all the acceptable ones.
DISCUSSION
Adoption of a specialized niche by a tropical insectivorous bird requires a
series of adaptations with respect to its sensory, motor and physiological
capacities. Previous studies of other avian insectivores or omnivores suggest
differential adaptations of these predators with respect to sampling strategies
(Alcock, 1973; Barrows et al., 1980), discriminatory and learning abilities
(Rothschild, 1964; Wilcoxon, Dragoin & Kral, 1971), prey capture and
handling abilities (Swynnerton, 1915b, 1919; Brown & Neto, 1976; Evans,
1984), and abilities to tolerate toxic prey items (Swynnerton, 1915b; Rothschild
& Kellett, 1972; Marsh & Rothschild, 1974; Fink & Brower, 1981).
In this study, the general pattern of jacamar response to local butterflies, i.e.
Table 7. Response of a rufous-tailed jacamar (Jacamar 2) to a combination of
unacceptable and acceptable butterflies. I n each feeding experiment, a variety
of butterflies, each a different morph previously tested with this bird, were
offered simultaneously, and the bird was free to attack for the whole
experimental period (method 4)
Previously unacceptable
butterflies
Number of
morphs
offered
Experiment 1: 10.13 to 17.00 hours
Experiment 2: 9.15 to 17.00 hours
Experiment 3: 10.39 to 17.00 hours
24
21
24
Previously acceptable
butterflies*
Response of bird
N
P
K
2 4 - - 18 3 2 4 - - -
*Including inconsistently accepted butterfly morphs.
E
-
Number of
morphs
offered
14
16
10
Response of bird
P
K
E
-~~
14
16
10
N
_
-
-
_ _ _
RESPONSES OF JACAMARS TO BUTTERFLIES
179
some of their behavioural adaptations and physiological capacities, was
indicated. Many butterfly morphs were insufficiently tested with only one or few
individuals; in such cases their palatability assignment is suggestive only.
Nevertheless, when considering the palatability of genus or family, the overall
results are consistent with other studies. Most of the butterfly taxa which were
unacceptable to jacamars-Battus
and Parides, Asciu, most heliconiines,
acraeines, ithomiines and danaids-are also known to be unpalatable to other
birds. By the same token, the acceptable butterflies-Papilio, Charaxinae, most
Nymphalinae, Morpho, Brassolinae, and Satyrinae-are also palatable to other
birds (Brower, 1984). Almost all Battus and Parides, ithomiines and danaids were
rejected by jacamars, but pierids and heliconiines showed a range of
acceptability to jacamars; this too is consistent with other studies (Brower,
1984).
All the butterfly taxa unacceptable to jacamars specialize on restricted plant
taxa as larval host plants (see Results). The chief deterrent quality of the large
white (Pieris brussicae) and the monarch butterfly (Danaus plexippus) to birds has
been shown to be host-plant derived (Marsh & Rothschild, 1974; Brower et al.,
1982). However, toxins and/or repellent factors sequestered from host plants are
not the only chemical defensive mechanism in butterflies (Rothschild & Kellett,
1972; Marsh & Rothschild, 1974). Recent evidence suggests that adult
ithomiines and danaids need to suck up fluids from plants (such as Boraginaceae
and Asteraceae) rich in pyrrolizidine alkaloids (PAS) which are stored as
defensive chemicals in the butterflies’ bodies. Although the jacamars rejected all
but one ithomiines and danaids, the deterrent quality of these butterflies may
range across a broad spectrum (Bopprt, 1984; Brown, 1984).
Although the responses of the two caged birds to local butterflies were
generally similar, they clearly showed individual feeding differences. Jacamar 1
was more likely to sample and consume butterflies (Table 2). After long periods
without food, Jacamar 1 consumed pierid and heliconiine butterflies that were
consistently rejected by Jacamar 2. This individual difference was unlikely to be
a result of different amounts and types of food offered to the birds since both
birds were maintained in very similar ways. Such individual variation has also
been found in other bird species in controlled experiments (e.g. Swynnerton,
1919; Brower, 1958a, b, c, 1960; Brower, Brower & Collins, 1963; Brower &
Brower, 1964).
The Heliconius butterflies consumed by Jacamar 1 are known to be
unpalatable to other birds (Brower, Brower & Collins, 1963) and to contain
cyanogenic glycosides (Nahrstedt & Davis, 1983). Insect unpalatability to birds
is often relative (Rothschild & Kellett, 1972; Marsh & Rothschild, 1974). A
variety of African bird species tested by Swynnerton (1915a, b, 1919) were
found, when hungry, to consume usually unacceptable insects such as danaid
and acraeine butterflies without showing any ill effects. Some birds even
‘specialize’ on aposematic butterflies (e.g. black-eyed bulbuls, Pycnonotus barbatus,
on danaids and acraeines, Swynnerton, 1915b; black-eared tanagers, Pipraeidea
melanonota, on ithomiine butterflies, Brown & Neto, 1976; black-backed orioles,
Icterus galbula, and black-headed grosbeaks, Pheucticus melanocephalus, on
overwintering monarch butterflies, Danaus plexippus, Fink & Brower, 1981), or
quite readily accept them (European rollers, Coracias garrulus, and hornbills,
Tockus (Lophoceros) species, on danaids and acraeines, Swynnerton, 1915b,
P. CHAI
180
1919). However, these are probably special cases. Past feeding experiments with
African birds (Swynnerton, 1915b, 1919) and North American birds (Jones,
1932, 1934) indicate that most birds do show a consistent agreement in the
order of preference for local insects, though readiness to consume such insects is
variable among birds. The experimental jacamars’ preference for different
butterfly taxa is also consistent with other studies using different bird species
(Brower, 1984).
Jacamars are potentially able to capture and handle the entire range of
butterflies in their environment, but, judging from the number of missed attacks
and the very different handling times on different butterfly species by caged
jacamars, butterflies are probably highly variable in terms of easiness of capture
and handling (Swynnerton, 1915b). This suggests that some butterflies probably
gain protection by means of effective escape behaviour (Gibson, 1980) or high
costs of handling (Pyke, Pulliam & Charnov, 1977; Sherry & McDade, 1982).
This may explain why wild jacamars frequently ignored passing butterfly species
that both caged birds readily attacked (see also Swynnerton in Carpenter, 1942
on other wild birds).
Adaptations of butte& predators
A predator may reject noxious prey (1) on sight, (2) after capture and tasting
(Jarvi, SillCn-Tullberg & Wiklund, 1981; Wiklund & Jarvi, 1982), or (3) after
consumption, subsequent vomiting, and learning by latent association
Table 8. A comparison of the responses of four species of birds: rufous-tailed
jacamars (two birds), blue jays (six birds), silverbeak tanagers (Rhamphocelus
carbo, seven birds) and Parson’s tanagers (Tuchyphonus ~ufus, six birds) to
butterflies in feeding experiments. The jay and tanager data are from Brower
(1984)*
Percentage of birds’ responses
N
P
K
E
Jacamar I
Jacamar 2
Blue jays
19
9
I
71
36
4
1
59
15
18
20
46
Rejected but survived
(N P/N P+ K)
+
+
Silverbeak
tanagers
30
6
16
48
Parson’s
tanagers
56
8
14
22
82
P < 0.001
P < 0.001
*Each bird was simultaneously offered 10 dead butterflies representing 10 species of different taxa on a tray
for 2 h for each of 10 consecutive days. Birds’ responses suggest that Paridcs, Hcliconius, Bhomia, Danaus and
Lycorea are relatively unpalatable, and Biblas, Siprocfa, Anortia, Agruulis and Euplychia relatively palatable.
?Fisher’s exact test (one-tailed), ns = not significant; the significance level is reduced to 0.005 due to
repeated comparisons.
RESPONSES OF JACAMARS TO BUTTERFLIES
181
(Swynnerton, 1915b; Brower, 1969). Both the predator and noxious prey pay
more in terms of time, energy, and physical harm as their interaction rises from
step 1 to step 3 (Boyden, 1976). Consequently, natural selection should favour
rejection occurring as early as possible, at step 1 or 2 (Endler, 1986). Indeed,
distasteful butterflies used in past feeding experiments were mostly sight- or
taste-rejected by experimental birds (Swynnerton, 1915b, 1919; Jones, 1932,
1934; Lane, 1957; Brower, 1958a, b, c; Brower et al., 1963; Brower & Brower,
1964; Brower, Alcock & Brower, 1971; Platt, Coppinger & Brower, 1971;
Bowers, 1980, 1981 ; Brower, 1984).
In the feeding experiments reported here, all rejections observed were by sight
or by taste, not by vomiting (Jacamar 2 was observed vomiting in response to
ingested artificially painted butterflies; Chai, in press). Sight-rejections
especially account for most rejections. Of the butterflies tested with Jacamar 1
19% were sight-rejected compared to 10% taste-rejected by it; for Jacamar 2,
36% of the butterflies were sight-rejected compared to 5% taste-rejected (Table
8). Efficient sight-rejection requires an ability to discriminate between
unpalatable and palatable prey. Sampling behaviour of the two jacamars
indicates that learning and memory play a role in enabling them to make the
right decision. The role of instinct in jacamar feeding behaviour is still not clear.
In other birds, there is some evidence suggesting an innate tendency to avoid
warningly coloured prey (Coppinger, 1970; Schuler, 1982).
Whether or not the sight-rejected butterflies actually contain noxious
chemicals is unknown. It is probable that some are edible mimics, such as Papilio
anchisiades and Phyciodes (Eresia) eutropia. Jacamar 2 attacked and consumed
P. androgeus females but ignored P. anchisiades females. Parides females (model of
P . anchisiades females) were many times more common than Battus species
(model of P. androgeus females), and thus presumably served as a better model.
As seen in Table 4, Jacamar 2 rejected conspicuously coloured male Appias
drusilla (mimic of Ascia monuste) , Hamadryas feronia, male Catonephele nyctimus,
Siproeta stelenes and Cithaerias menander (a mimic of transparent winged
ithomiines) initially, but over time learned to accept them. The initial rejections
are thus interpreted as the result of the bird’s uncertainty, rather than
distastefulness of the butterflies. In these experiments, some boldly patterned
and/or mimetic palatable butterflies appeared to enjoy at least temporary
protection from jacamar attacks.
It is also unknown whether or not the ‘taste-rejections’ observed are actually
caused by noxious olfactory or gustatory stimulation from defensive chemicals in
the butterfly or are due to other cues such as close viewing of the butterfly,
behaviour of the butterfly after capture (most unacceptable butterflies ceased
struggling when held by the thorax), or feeling the body texture in the bill (most
unacceptable butterflies have a tough and flexible thorax; on post-capture
defences by aposematic insects, see Rothschild, 1971).
If a predator must taste its prey to assess palatability, selection is likely to
favour the most rapid and least costly assessment possible. The jacamar’s ability
to reject an unacceptable butterfly rapidly, usually after a single peck, makes
sampling less time consuming. Jacamars have long bills which allow them to
keep noxious insects away from their face. They can also vomit ingested prey
easily (Chai, in press), and can tolerate certain kinds of noxious prey such as
Heliconius butterflies. All these characters make sampling less dangerous. This
182
P. CHAI
relatively inexpensive learning process should encourage a predator to sample
(Huheey, 1980). Indeed, jacamar beak marks are the most common beak marks
found on the wings of wild Heliconius butterflies at Corcovado (P. Chai & L. E.
Gilbert, unpubl. obs.).
Adaptations of unpalatable butterjlies
It is to the advantage of unpalatable butterflies to warn potential predators
from attacking them. Unpalatable butterflies, by evolving away from palatable
butterflies in appearance and behaviour, increase the probability that predators
will discriminate and reject them on sight (Fisher, 1958; Turner, 1975;
Matthews, 1977; Gittleman, Harvey & Greenwood, 1980; Harvey et al., 1982).
The distinct morphology and behaviour of unpalatable butterflies then serve as
warning signals to visually hunting predators to indicate their distastefulness. In
contrast, except for Batesian mimics for obvious reasons, palatable butterflies are
protected by camouflage, escape behaviour and/or large size. Their
morphology, behaviour and colour patterns are primarily designed not to
educate but to avoid and distract predators by being hard to detect, capture
and/or handle (Edmunds, 1974; Endler, 1986; DeVries, in press; but see Gibson,
1980). Because of these diverse selective forces exerted by visually hunting
predators, the morphological and behavioural attributes of butterflies tend to be
correlated with their palatability. Among the butterflies at Corcovado,
unpalatable and palatable species are very different in morphology, colour
patterns and movement patterns, and these differences can be easily noticed
even from a distance (Fig. 2 and Chai, in prep.). It is anticipated that
specialized butterfly predators will use these differences as cues to select butterfly
prey. In this study jacamars actually tended to attack and consume
camouflaged (at least on one side) and/or fast-flying butterflies while avoiding
boldly patterned, mimetic and/or slow-flying ones.
Because the prey behaviour itself can signal predators such as jacamars, it is
more realistic to use live butterflies to conduct feeding experiments with this
type of predator. In addition, since the bird was offered live butterflies, it was
possible to determine directly whether or not the butterflies were killed. Previous
studies have attempted to judge whether or not a butterfly would have been
killed from the extent of damage inflicted on butterflies that were already dead
(Brower, 1958a, b, c; Brower et al., 1963; Coppinger, 1969, 1970; Bowers, 1980,
1981).
Unpalatable butterflies also possess adaptations which help them to survive if
they are captured. Many have unpleasant odours (Rothschild, 1961), a tough
and flexible body (Fisher, 1958; Rothschild, 1971) as well as higher
concentrations of distasteful substances in the wings (Brower & Glazier, 1975).
Most cease to struggle when captured. These characteristics help the
unpalatable butterflies to survive a predator’s tasting and handling. Indeed, the
survival rate of butterflies rejected by Jacamar 1 and Jacamar 2 was significantly
higher than that of butterflies rejected by generalized predators such as jays and
tanagers (Brower, 1958a, b, c; Brower et al., 1963; Brower & Brower, 1964;
Bowers, 1980, 1981; Brower, 1984). Table 8 shows that 438/451 or 97% of
butterflies survived after being rejected (by sight or taste) by the two jacamars
us. 836/ 1 154 or 72% by the three omnivorous bird species. This is partly because
RESPONSES OF JACAMARS T O BUTTERFLIES
I83
the jacamar’s long thin bill is too weak to exert a crushing force (Lederer, 1975),
and its tasting process is usually very brief (Table 5). Although predators must
continue to sample potential prey items, both the specialized predators and
unpalatable prey have characteristics to reduce the cost of such sampling.
Both jacamars used in this study generally ignored, or delayed their attacks
on, butterflies which they considered to be unacceptable, whereas acceptable
butterflies were usually attacked quickly (Table 2). Jacamar 2 made clear
distinctions between very similar mimetic butterflies (Table 6). Relatively few
morphs were consumed inconsistently (Table 4), and the percentages of tasterejections (Peck+Kill) compared with Not touch and Eat were low (Table 8).
These facts imply that in most cases when the birds saw a given butterfly, they
somehow ‘guessed’ its palatability. They were only uncertain about a small
proportion of the total butterfly morphs tested, and those they tended to sample.
Such accurate discrimination in butterfly predators such as jacamars can further
drive incipient mimics toward an improved resemblance of their model.
Variation in the responses of predators affects the intensity of selection on
prey that use mimicry as an antipredatory strategy. Consequently, the
distributions of predator species, and of variable (territorial) individuals within
predator species, which adopt different feeding strategies, create a selective
landscape which determines the effectiveness of mimicry in a dynamic local
scale. This can lead to initial protection of incipient mimics having a crude
resemblance to a model, from less specialized predators in one area; subsequent
sampling by more specialized predator species or individuals in other areas
further selects for an enhanced degree of resemblance. More detailed
comparative studies of the adaptations and responses of different predator
species and individuals to a variety of prey types are clearly needed.
CONCLUSIONS
Rufous-tailed jacamars show preference toward certain butterfly taxa while
rejecting others, and do not ‘specialize’ on any aposematic butterflies. Their
preferences are very similar to those shown by a variety of bird species tested in
past feeding experiments. In this study, Jacamar 2 was less prone to attack and
consume butterflies than Jacamar 1. This difference among individuals of the
same species has also been demonstrated in past studies.
However, as a more specialized predator on butterflies, jacamars show many
unique characteristics. First, they only consume winged insects and do not
recognize insects as prey unless the insects are moving. Secondly, they are
capable of capturing and handling the entire range of local butterflies. Thirdly,
they can discriminate between butterflies with very similar colour patterns.
Lastly, they tend to ignore (sight-reject) uneatable (unacceptable) butterflies,
while quickly attack eatable (acceptable) ones. Of the butterflies tested with
Jacamar 1 190; were sight-rejected compared to 10% taste-rejected by it; for
Jacamar 2, 367, of the butterflies were sight-rejected compared to 5% tasterejected. The taste-rejection process is usually very brief; thus very few tasterejected butterflies are killed. Local butterflies unacceptable to jacamars are
generally conspicuously coloured and mimetic, have long, slender bodies, and
fly slowly and regularly. Acceptable butterflies are generally cryptic (on at least
one side), with short, stout bodies, and fly fast and erratically. Jacamars
184
P. CHAI
presumably use these morphological and behavioural characteristics of
butterflies as cues to assess their palatability.
ACKNOWLEDGEMENTS
I thank T. C. Moermond, M. Rothschild and anonymous reviewers for their
suggestions and critical comments. I am grateful to P. J. DeVries for teaching
me to identify butterflies and for commenting on this paper, to S. S. Bramblett
for commenting on and re-typing this paper, and to C. D. Thomas and N. Greig
for discussing and greatly helping me at a late stage of revision. I wish to express
my profound gratitude to J. C. Lang who critically and painstakingly helped me
to revise and commented on the entire paper. Special thanks are due to L. E.
Gilbert for inspiration and assistance during the course of this study and for
improving the manuscript. The National Park Service of Costa Rica, especially
the staff of Corcovado National Park, are acknowledged with many thanks.
Lastly, I thank my wife, C. Hu, for her continuous support in numerous ways.
This work was supported by research grants from Sigma Xi, Chapman
foundation of the American Museum of Natural History, Tinker Foundation of
the Institute of Latin American Studies, and the Graduate School of the
University of Texas at Austin. Cage facilities and logistic support were made
possible by NSF grants (DEB-79060332) and (BSR-8315399) to L. E. Gibert.
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Appendix. Free-flying butterflies offered to two individually caged rufous-tailed
jacamars listed by morph. Each number represents one individual butterfly in
one feeding experiment. The final fate of each individual butterfly is assigned to
one of four categories: N = not touch; P = peck; K = kill; E = eat
Butterfly morphs*
Papilionidae
Battus belus uarus
Battur crassus
B a t h polydamas
Parides childrenae (J)
Parides childrenae (9)
Parides erithalion (6)
Parides erithalion (9)
Parides lycimenes (6)
Parides lycimenes ( 0 )
Papilio anchisiades idaeus (9)
Papilio androgeus epidarus (9)
Papilio thoas nealces
Pieridae
Aphrissa boisduvalli
Appias drusilla (d)
Appias drusilla (9)
Asria limona
Ascia monuste
Melete jorinda
Perrhybris pyrrha (6)
Perrhybris pyrrha (9)
Phoebis argante
Phoebis sennae
Phoebis trite
Flight
pattern
and
colour
pattern7
F,N, U
F,N,U
F,N,U
F,N,U
F,N,U
F,N,U
F,N,U
F,N,U
F,N,U
F,N,U
F,N,U
F,N,B
F,N,B
F,N,U
F,N,B
F,N,U
F,N,U
F,N,B
F,N,U
F,N,U
F,C,P
F,C,P
F,C,P
Jacamar I
Jacamar 2
Response
Time of
Response
Time of
first
first
N P K E attack: N P K E attack
I
--
- -
0:45
-
-
X
- - - -
-
X
x
X
-
1
-
-
1
-
-
-
-
- 2 - I --
- - - -
-
-
----
-
-
~
-
X
1:13
X
x
X
-
X
~
X
~
-
X
0 : 00
0:Ol
~
-
--- 4
0:oo
- - - -
-
- _ -
3 - 1
- _ _
- - - 16--- - - 3
0:02 3 0 - - ---- 4 2 - - - 16--- I - 0:02 3 1 - - - -
~
-
- - -
-
- -
5
- - - -
-
-
0:05
- - -
-
- - -
16
5
6
0 : 00
X
0 : 00
X
X
-
0 : 00
X
2 : 22
13 ~
0 : 15
10 0 : 17
2
0 : 00
-
P. CHAI
188
Appendix Continued
Butterfly morphs*
Nymphalidae
Charaxinae
Archaeoprepona demophon
Zaretis ellops
Consul fabius
Memphis eurypyle confusa, M . gbcerium or M.
chrysophana
Memphis artacama
Memphis forreri
Memphis pittyusa
Memphis sp.
N ymphalinae
Colobura dirce
Historis acheronta
Historis odius
Hamadryas amphinome mexicana
Hamadryas arelhusa saurites (d)
Hamadryas arethusa saurites (9)
Hamadryas feronia farinulenta, H. februa or
H. ipthime
Marpesia berania
Marpesia iole
Marpesia chiron
Temenis laothoe a g a h
Nica Javilla canthara
Catonephele numilia esite (d)
Catonephele nyclimus (6)
Catonephele nyctimus ( 9 )
Diaethria marchalii
Callicore atacama manoua
Pyrrhogyra crameri or P. otolais
Adelpha boeotia
Adelpha celerio or A. iphiclus
Adelpha cytherea marcia
Adelpha heraclea
Adelpha lerna aeolia
Adelpha naxia
Siproeta stelenes biplagiata
Anartia fatima
Anartia jatrophae
Junonia evarete
Phyciodes (Eresia) eutropia
Heliconiinae
Philaelhria dido
Dione juno
Agraulis vanillae
DIyadula phaetusa
Dryas iulia
Eueides isabella
Eueides aliphera
Eueidus bbia libioides
Heliconius doris (green morph)
Heliconius doris (red morph)
Heliconius ismenius clarescms
Heliconiu hecale zuleika
Heliconius melpomene rosina
Flight
pattern
and
colour
pattern?
F, C, P
F,C,B
S,C,B
F,C,B
F,C,P
F,C,P
F,C,P
F,C,P
F,C,P
F,C,B
F,C,B
F,C,B
F,N,U
F,N,U
Jacamar I
Jacamar 2
Time of
Response
N P K E attack:
- ~ --
- -
- - - -
Time of
N P K E
attack
lint
----
-
0 : 00
0 : 00
0:lO
-
- - - -
-
- - - -
-
- - - -
-
- - - -
-
- - - -
-
0 : 00
0 : 00
0 : 00
0 : 14
0 : 00
----
-
--_
- - - -
-
- - _
1
- - -
-
-
- - - - - - -
0 : 00
~
-
-
0:07
0 : 00
1
0 : 00
-
-
0 : 00
5 : 55
0 : 00
0:Ol
-
-
-
0 : 00
-
0 : 00
0 : 00
0 : 06
0 : 00
-
- - - 1 0 : 08
- - - 1
0 : 53
---- - - - -
-
--- 3
0 : 29
-4
X
0 : 00
0:Ol
~
145 2 3 2 -6 2 --
0 : 00
0 : 00
0 : 00
0 : 00
0 : 00
-
0 : 00
-
- - -- -
- - -
I
9
5
0 : 00
0 : 00
0 : 00
-
___
F,N,B
F,N,U
F,N,U
F,N,U
F,N,U
S, N, U
S,N,U
S,N,U
S,N,U
S,N,U
S,N,U
S, N, U
S,N,U
Response
fint
0:Ol
X
0 : 00
0 : 00
0:Ol
0 : 10
0 : 00
0 : 02
0 : 00
0 : 32
?
?
?
X
0 : 00
X
0 : 00
0 : 15
0 : 00
X
X
0 : 15
2 -- 2
1 2
X
X
- - - -
-
X
4 : 55
0:11
0:Ol
X
-
3
5
2
1
-
-
- ~-
-
3
5
3
X
X
X
RESPONSES O F JACAMARS TO BUTTERFLIES
Butterfly morphs*
Heliconius pachinus
Heliconius erato petiverana
Heliconius hewitsoni
Heliconius sara theudela
Heliconius charifonius
Acraeinae
Artinoie lapitha
1 thomiidae
Tithorea tarricina pinthias
Melinaea scylax
Thyridia psidii melantho
Mechanitis polymnia isthmia
Mechanitis hsimnia doyssus
lthomia patilla
Aeria eurimedia agna
Hyposcada virginiana euanides
Oleria paula
Callithomia hrzia
Ceratinia tutia dorilla
Godyris U g i a
Hypoleria cassotis
Pteronymia agalla obscurata
Danaidae
Lycorea cleobaea atergatis
Danaus gilippus or D. eresimus
Satyridae
Morphinae
Morpho amathonte
Morpho peleides
Brassolinae
Caligo atreus
Caligo eurilochus sulanus
Caligo memnon
Opsiphanes tamarindi sikyon
Satyrinae
Cithaerias menander
Pierella heluetia incanescens
Pierella luna
Tcygetis andromeda
Euptychia hermes
Euptychia metalmca
Eupychia arnaea
Cissia confusa
Cissia libye
Lycaenidae
Arawacus aetolus
Eumaeus minyas
Riodinidae
E u y b i a patrona persona
Eurybia lycisca
Flight
pattern
and
colour
pattern7
189
Jacamar 2
Jacamar 1
Time of
Response
first
N P K E attack: N P K E
Response
Time of
first
attack
X
X
X
X
X
X
X
X
0:10
X
0:Ol
-
1 :39
0 : 00
-
3 : 38
X
X
X
0:Ol
X
X
X
X
X
-
3: I1
0 : 14
X
X
X
X
X
X
0 : 48
X
X
5 I
5 2
- -
0 : 00
0 : 00
0 : 00 _ _ _ 3
1 :41 - I - 12
0 : 00
0 : 00
1 :25
0 :10
-
1 :42
0 : 23
0 : 00
0 : 00
0 : 00
0 : 00
0 : 00
0 : 00
0 : 00
0 : 00
0 : 00
0 : 00
0:Ol
0 : 00
0 : 00
0 : 00
0 : 00
0 : 08
-
0 : 36
X
0 : 03
0 : 00
- -
-
0 : 33
-
0 : 00
0 : 00
*The taxonomical order and butterfly names are according to DeVries (1983).
tFlight pattern: S, slow and fluttering fliers; F, fast fliers. Colour pattern: C, cryptic on at least one side
(usually the underside); N, not cryptic. U, most wing areas transparent, or white, orange, pink, red or black
colours often shown in unpalatable butterflies; P, most wing areas yellow, green, brown, or blue colours
often shown in palatable butterflies; B, colours from both groups are present.
:Time of first attack is the time of attack during the first feeding trial of a given morph ( h : min; x = no
attack ever observed).