Download Palatablility and escaping ability in Neotropical butterflies: tests with

Biologicaljournal of the Linnean Society (1996), 59: 351-365. With 2 figures
Palatablility and escaping ability in N eotropical
butterflies: tests with wild kingbirds (Tyrannus
rnelancholicus, Tyrannidae)
CARLOS E.G. PINHEIRO
Department qf Zoology, South Parks Road, Oxford, OX13PS and
Departamento de Zoologia, Universidade de Brasilia - UnB. 70910-900 Brasilia, DF, Brazil
Received 29 August 1995, accepted for publication 12 January 1996
The palatability and the ability of neotropical butterflies to escape after being detected, attacked and
captured by wild kingbirds (Tyrannus melancholicus Vieillot), was investigated by the release of 668
individuals of 98 butterfly species close to the birds, during their usual feeding activities. Most of the
butterflies were attacked and eaten. Only the troidine swallowtails (Parides and Battus; Papilionidae) were
consistently rejected on taste and elicited aversive behaviours in birds. Most other aposematic and/or
mimetic species in the genera Danaus and Lycorea (Danainae), Dione, Eueides and Heliconius (Heliconiinae),
Hypothyris, Mechanitis and Melinaea (Ithomiinae), Biblis, Callicore and Diaethria (Limenitidinae) were
generally eaten. Cryptic and non-mimetic species were always attacked and, if captured, they were also
eaten. All Apaturinae, Charaxinae, Nymphalinae, Hesperidae, most Limenitidinae, Heliconiinae
(Agraulis, Dryas, Dryadula and Philaethria) and Papilionidae (Eurytides, Heraclides and Protesilaus) were in this
group. Results indicate that the learning process in kingbirds may demand a large mortality in prey
populations, even among species generally accepted as unpalatable and aposematic. They also support
the assertion that escaping ability and unpalatability evolved in butterflies as alternative strategies to
avoid predation by birds. Mimetic relationships among several species are discussed. Evidence for the
evolution of aposematism not related to unpalatability, but to escaping ability, was found for two hardto-catch Morpho species.
© 1996 The Linnean Society of London
ADDITIONAL KEY WORDS: -tyrant-flycatchers - predation - butterfly defences - aposematismcrypsis - mimicry.
CONTENTS
Introduction . .
Material and methods
Study species
Study site
Field experiments
Results. .
Unpalatability .
Relationships between palatability, escaping ability and wing size
Discussion .
Birds' reactions
Chemical defences and Fisher's Dilemma
Mimicry . . .
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© 1996 The Linnean Society of London
C. E. G. PINHEIRO
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Escaping. .
Acknowledgements
References .
Appendix . . .
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INTRODUCTION
The evolution of coloration patterns in prey insects is in large part determined by
the selective pressure of visually hunting predators (Fisher, 1930; Cott, 1940;
Edmunds, 1974; Endler, 1991). In butterflies, especially, different colour patterns are
associated with distinct defensive strategies. Thus, unpalatable species are generally
aposematic, fly slowly and regularly, and exhibit tough wings. These characteristics
are believed to help learning by predators and provide protection against sampling.
Mullerian mimicry is common in several species that can be also used as models by
palatable, Batesian mimics. On the other hand, palatable butterflies are predominantly cryptic, fly fast and erratically, and are expected to show a higher ability to
escape predator attacks than unpalatable species (see Poulton, 1890; Fisher, 1930;
Chai, 1990; Chai & Srygley, 1990; Endler, 1991; Malcolm, 1992; Srygley, 1994).
However, escaping ability in butterflies has been only rarely tested in natural
conditions.
In recent years many different types of chemical compounds have been detected
and identified in several butterfly taxa (see Brower, 1984; Brown et al., 1991).
However, we still do not know how unpalatability and/or aposematism evolved in
butterflies, or in prey insects in general. Fisher (1930) reasoned that predators need
to sample prey to assess its palatability, and many prey were assumed to die in the
learning process. As a consequence, unpalatability and/or aposematism should
evolve better through kin selection (see also Benson, 1971; Turner, 1981; Krebs &
Davies, 1981; Harvey & Paxton, 1981). However, some data suggest that aposematic
species generally survive predator sampling, and aposematism and/or unpalatability
could evolve by individual selection (Wicklund &Jarvi, 1981;Jarvi, Sillen-Tullberg
& Wicklund, 1981).
In the neotropics, butterflies face a variety of predators whose abilities to capture,
handle, and tolerate butterfly defensive chemicals differ greatly from each other
(Alcock, 1971; Rothschild & Kellett, 1972; Brower, 1984; Turner, 1984). A
significant amount of palatability data is now available for the bird Galbula nificauda,
one of the most specialized butterfly predators (Benson, 1972; Sherry, 1983; Mallet
& Barton, 1989; Chai, 1986, 1990). Most other presumed important predators
remain uninvestigated and the relative importance they might have played in the
evolution of butterfly defences has not been assessed. This is the case for tyrantflycatchers (Tyrannidae), which form one of the largest and most diverse bird families
of the New World (Schauensee, 1970; Sick, 1993). Most species are predominantly
insectivorous and attacks on adult Lepidoptera are well known (e.g. Cook, Brower &
Alcock, 1969; Collins & Watson, 1983; Sherry, 1984; Pinheiro & Martins 1992;
Poulin, Lefebvre & McNeil, 1994).
In this paper the palatability and escaping ability of butterflies to one of the most
common and widespread tyrant-flycatchers, the neotropical kingbird, were tested.
The following questions were investigated: (1) Do kingbirds attack butterflies in. the
field? (2) Are they able to capture and handle butterflies of different sizes and
escaping strategies? (3) Is there a high mortality of aposematic butterflies resulting
PALATABILITY AND ESCAPING IN BUTTERFLIES
353
from bird sampling? (4) Is there any relationship between unpalatability, escaping
ability and body size (wing length) in butterflies?
MATERIAL AND METHODS
Study species
Tyrannus melancholicus occurs throughout Central and South America. These birds
are commonly found in forests, especially in the edge or on higher perches above the
canopy, where they get an excellent view for hunting and find the necessary space for
their aerial manoeuvres. They may also occur in many other natural and disturbed
habitats, including urban areas. Kingbirds are among the largest birds in the family
Tyrannidae, adults weighing 38-45 g. The bills are relatively long (up to 26 mm), flat,
with a large base and hooked at the tip of the upper jaw (see Sick, 1993).
A large part of kingbirds' diet consists of winged insects such as flies,
hymenopterans, and termites intercepted in flight (see also Sherry, 1984 for a survey
of tyrant-flycatchers' diet). Very small insects are generally seen against the sky and
captured after a direct flight within a small distance from the perch. Large
insects - and the butterflies offered to birds - are predominantly seen against the
ground or the vegetation below. Birds must dive and perform a previously studied
flight to intercept and catch prey in the air. Prey is often carried to the perch to be
consumed. They generally use a small number of preferred perches to which they
return day after day (see also Fitzpatrick, 1980).
A list of the butterflies (Papilionoidea) used in the experiments and the mimetic
complexes investigated are given in the Appendix (see also Brown & Benson, 1974;
Papageorgis, 1975; Brown, 1988). The classification of butterflies into subfamilies of
Nymphalidae follows Harvey (1991).
Study site
Field work was conducted in June-July 1994 in the Serra dos Carajas in the
southern portion of the State of Para, Brazil (5°54'-6°33'S; 49°53'-50 034'W). Tests
with kingbirds were carried out in the city of Carajas, The city is relatively small and
surrounded by natural rain forest. Birds were very abundant and commonly found
on the wires along the streets, generally in groups of two or three individuals that
were always present at the same time and sites during the experiments. Unlike birds
in more wild areas, they were relatively unafraid of humans.
Field experiments
Butterflies were netted or trapped in different sites in the Serra dos Carajas,
especially the Represa do Esteril SuI, the Horto Florestal, and near the rivers Pojuca
and Salobo. After capture, they were kept in entomological envelopes or inside a
small cage until released to birds (> 25 km away) in the city of Carajas, Most of the
tests were conducted in the afternoon of the same day of capture (between one and
five hours later), but on a few occasions they were carried out on the following
354
c. E. G. PINHEIRO
morning. Species and the number of butterflies offered were in large part determined
by their abundance and ease of capture in the field. With few exceptions, most of the
butterflies were of medium to large size (wing length > 25 mm). All individuals were
previously checked for damage and were active before being offered to the birds.
Six groups of birds (18 individuals) more than 250 m apart were used in the
experiments. Groups were sequentially visited on the same day and a set of butterflies
(no more than ten individuals) was offered to an individual bird. Butterflies were
released 2 m above the ground within a distance of 8-12 m of a previously chosen
bird. If a butterfly was rejected on sight I always offered a palatable species
(previously tested by Pinheiro & Martins 1992; or Chai, 1986; 1990) to test the
possibility of satiation. Each butterfly species was offered to birds until ten individuals
had been tested for palatability (eaten or taste-rejected) to different birds.
Birds' responses were pooled into the following categories (also used by Chai,
1990): (1 )'Rejected on sight' (= SR), when a butterfly was detected but not attacked
by birds. On most occasions birds remained on the perch and only moved their
heads to observe the butterflies, but on a few occasions they flew towards a butterfly
for closer observation, and did not attempt to capture it; (2)'rejected on taste'
(= TR), when a butterfly was captured, but afterwards released by the bird, and
(3)'eaten' (= E), when a butterfly was attacked and swallowed after capture. The
handling behaviour of the birds and their reactions after a butterfly was eaten or
rejected (head shaking, vomiting) were noted. Butterflies rejected on taste were
observed further and assessed for ability to fly or not after being handled and released
by birds. In many cases butterflies escaped from bird attacks, and thus the categories
also include (4) the number of butterflies not captured (= NC) as well as (5) the
number of attacks (= NA) and unsuccessful attacks (= VA).
RESULTS
In all, 98 species and 668 individual butterflies were released to birds in the city
of Carajas. The pooled responses of the birds toward this set of butterflies are
summarized in the Appendix. Only 6.3% of the butterflies (42) were not attacked
(sight-rejected) by birds; 12.3% (82) were not captured (escaped), 8.7% (58) were
taste-rejected, and the remaining 72.7% (486) were eaten (but see footnote in the
Appendix). Time elapsed to detect butterflies varied between 4 and 10 sec after
butterflies were released to birds.
Unpalatability
Indication of unpalatability was found for several species taste-rejected by birds.
The highest proportion of taste-rejection (total taste-rejected/total captured) was
found for the three Parides species, with 70-80% of the butterflies being rejected by
birds. Tasting these butterflies also elicited aversive behaviours like head shaking
(Gillan, 1979), followed by beating the butterfly against the perch before deciding to
release it, as observed in two birds while handling a Parides lysander and a P. neophilus.
Most of the other aposematic and/or mimetic species (Mullerian mimics) were eaten
by birds, but some butterflies were occasionally taste-rejected. This group includes
Danaus eresimus, D. plexippus andLycorea cleobaea (Danainae), Dione juno, Eueides aliphera,
355
PALATABILITY AND ESCAPING IN BUTTERFLIES
100
Ithomiinae
Heliconlinae
Par/des
Limenitidinae
Danainae
80
60
%
40
20
Parldes
Dione
Eueldes
Hellconlus
Hypothyrls
"'echanltls
"'ellna..
Ca/llcore
Dlaethrla
Danaus
Lycorea
(3; 25)
(1; 10)
(5; 29)
(8; 58)
(4; 28)
(2; 20)
(2; 7)
(2; 8)
(1; 10)
(3; 24)
(1; 10)
Figure I. Probability of being released alive by wild kingbirds for butterflies in several aposematic genera.
The number of species and individuals tested (= captured by birds) is given in parenthesis.
E. tales, Heliconius erato, H. melpomene, H. numata, H. sara, H. wallacei and H. xanthocles
(Heliconiinae), Hypothyris daphnis, H. ninonia, Mechanitis mazaeus, M. polymnia and
Melinaea mneme (Ithomiinae), Biblis hyperia, Callicore astarte, C. maximilla and Diaethria
clymena (Limenitidinae), and Stalachtis phlegia (Riodinidae).
The probability of being released alive (see methods) after being captured and
handled by kingbirds for butterflies in several aposematic genera is shown in Figure
1. Except for the Parides, predominantly taste-rejected, the survivorship of butterflies
in most other genera was usually below 30%, with the lowest values being found for
the Heliconiinae (Heliconius, Eueides, Dione). Among the 58 individual butterflies
rejected on taste by birds, four (7%) were clearly damaged and were considered
"dead" for the purpose of the analysis. They include the single S. phlegia offered to
birds, one Diaethria clymena, and the two Parides knocked by birds against the
perch.
On the other hand, all Apaturinae, Charaxinae, Nymphalinae, Hesperidae, most
Limenitidinae and Papilionidae, and the presumably unpalatable and/or aposematic
species Actinote thalia, Danaus gilippus, Hypothyris euclea, Melinaea ludovica, Agraulis vanillae,
Dryadula phaetusa, Dryas iulia, Eueides lybia, E. vibilia, Heliconius burney, H. ethilla and
Philaethria spp were always eaten once they had been seized by birds. However,
several of these butterflies were insufficiently tested and their palatability assignment
here is, therefore, tentative (see also Discussion). Butterflies were always eaten
entirely, including the wings. Apart from those species not attacked by birds, it was
not possible to test the palatability of Morpho achilles and M. menelaus. The former was
never captured by birds and the single M. menelaus successfully captured by a kingbird
was taken away and neither handling nor consumption was observed.
Relationships between palatability, escaping abiliry and wing size
The correlation between unpalatability, measured by the proportion of butterflies
taste-rejected (= TR/N-SR-NC, see Methods), and escaping ability, measured by
the proportion of unsuccessful attacks (= UA/NA) is negative but weak (r = - 0.4).
C. E. G. PINHEIRO
356
However, a stronger correlation between unpalatability and escaping is found when
only members of the Nymphalidae (except the two Morpho) are considered
(r = -0.75) and a very similar result is found when escaping is measured by the
proportion of individuals not captured (= NC/N). Escaping correlates positively
with the wing size (wing length of males, in mm; r = 0.7), but is not correlated with
unpalatability (r = 0.1).
A species ordination obtained through a Principal Component Analysis (P.C.A.)
based on the correlation matrix between unpalatability, escaping and the size of the
butterflies is shown in Figure 2. As in the above correlations, only the 40 most
abundant species (with a minimum number of ten individuals tested for palatability)
and the two Morpho species were included in the analysis. Morpho species were
included as palatable (taste-rejections = 0; see also discussion). Details of the analysis
are given in Table 1. The first two Principal Components accounted for over 95%
of the total variation and produced the separation of species according to their
escaping ability and unpalatability.
The first axis accounted for over 60% of the total variation and is mainly
influenced by the proportion of unsuccessful attacks. There is a clear escaping
gradient along the axis with the two Morpho species more than two units of variance
•
•
Morphinae
3 -
2 -
I
0:
1-
Limenitidinae
I
0
Charaxinae
I
0-
II
I
I
I
:
I
I
I
•
D D
I
0
. " , iI""O',·
Apaturinae
-1
I
, . , tr .D' , , - , - - , , , , . , - - •- - , , , - - - - - , , , ,
Heli~oniinae
DO
•
Danainae
[]
0
D:
•D
Papilionidae
( Parides)
•
Ithomiinae
""
• •
Nymphalinae
(= E. eunice)
[[J
ill
-2
+
,....
..,...
-2
-1
o
Diaethria
...,...
-,
2
,...._....
3
P.C. II (UNPALATABILITY)
Figure 2. Principal component ordination of 42 butterfly species. Symbols indicate distinct taxa (see also
the text).
PALATABILITY AND ESCAPING IN BUTTERFLIES
357
1. Correlations of the three variables studied with Principal
Components (= eigenvectors) and the variance explained
TABLE
Unsuccessful attacks
Taste-rejections
Wing size
Variance explained (%)
Cumulative (%)
PC I
PC II
PC III
0.72
-0.33
0.61
59.52
59.52
-0.04
0.86
0.51
35.10
94.62
0.70
0.39
-0.61
5.38
100.00
beyond the most elusive Charaxinae (Prepona demophon) and Limentidinae iNapeocles
jucunda, Nessaea obrinus, Catonephele spp and Hamadryas spp). Nearly all relatively
unpalatable species correlate negatively with PC I and the lowest values were found
for Heliconius erato, Hypothyris spp, Parides lysander, and Diaethria clymena.
The second axis accounted for over 35% of the total variance and is mainly
influenced by the proportion of taste-rejections. This axis produced the separation of
the higher butterfly taxa with the Charaxinae, Limentidinae, Apaturinae, part of the
Heliconiinae (Dryas, Dryadula, Agraulis, Eueides, Dione) and Nymphalinae (Eresia) on one
side, and the remaining Heliconiinae (Heliconius spp), the Ithomiinae, Danainae,
Papilioninae, and Diaethria clymena on the other. An unpalatability gradient can be
observed from the highly unpalatable Parides, between 1 and 2 units of variance away
from the Ithomiinae and Danainae, to the other Nymphalidae, with the relatively
palatable Heliconiinae lying in an intermediate position. The positive correlation of
the Morphinae on this axis is due to the influence of the wing size, which correlates
positively with both axes (see eigenvectors in Table 1).
Other species relatively hard-to-catch not included in the analysis were Historis
odius, Protesilaus spp, Nessaea batesii, Prepona meander, and Siproeta stelenes. Two
swallowtails (one Heraclides torquatus and one Protesilaus sp) were observed to escape
from a bird's bill during handling, after birds had already returned to perch (these
cases differ from taste-rejection since the birds always tried to capture the butterflies
again). In both cases butterflies lost small parts of the wings.
DISCUSSION
Birds' reactions
The experiments performed in this study clearly demonstrated that kingbirds
attack butterflies in the field. Except for the two large, elusive Morpho species, they
were able to capture and handle all other butterflies tested, regardless of palatability
or SIze.
The high number of attacks, and the evident low frequency of sight-rejections
especially for the aposematic and mimetic species, suggest that birds in the city of
Carajas were rather naive regarding butterfly palatability - a group of three cliffflycatchers (Hirundinea ferruginea; Tyrannidae) foraging at another site with a rich
butterfly fauna, rejected on sight over 50% of the butterflies offered, especially the
aposematic and mimetic species (Pinheiro, in prep.). However, sight-rejection also
occurred occasionally (n = 42) which suggests that some birds had had a previous
experience with the butterflies (a list of butterflies observed in the city is given in the
358
c. E. G. PINHEIRO
Appendix), or learned to avoid them during the experiments, probably after tasting
one or more Mullerian mimics. Most mimetic species were sight-rejected later in a
group of birds' sequence of presentations.
The palatability tests suggest that kingbirds are more tolerant of chemical defences
of butterflies than jacamars (Chai, 1986) and other birds. Except for the highly
unpalatable Parides and Battus, all other aposematic and mimetic species were
generally eaten by birds. Furthermore, they ate the whole butterfly, whereas
jacamars and other more specialized birds (see Brown & Vasconcellos-Neto, 1976)
usually do not eat the wings that may contain a large amount of defensive chemicals
(Brower & Glazer, 1975). Collins & Watson (1983) also found that three other species
of tyrant-flycatchers were more tolerant of defensive chemicals of arctiid moths than
several other insectivores birds.
Chemical difences and Fisher's dilemma
In spite of being more tolerant of defensive chemicals of butterflies than other
birds, kingbirds also tended to reject on sight or taste several species also tested with
jacamars by Chai (1986; 1990) and many other predators used in palatability
experiments with the Danainae (Brower, 1958a, b; Ritland & Brower, 1991),
Heliconiinae (Brower, Brower & Collins, 1963; Boyden, 1976), Diaethria and Callicore
(Pinheiro & Martins, 1992). Results from these studies also tend to agree on the
general edibility of the Apaturinae, Charaxinae, Limenitidinae, Nymphalinae and
Hesperidae.
The strongly distasteful properties of Parides and Battus relative to the other species
suggest that chemical compounds such as aristolochic acids, alkaloids, terpenes and
phenolics commonly found in these butterflies (Rothschild et al., 1970; Urzua,
Rodriguez & Cassels, 1987; Brown et al., 1991) are more efficient in deterring
predation by birds than such compounds as cardiac glycosides (Cohen, 1985;
Malcolm, Cockrell & Brower, 1989) and pyrrolizidine alkaloids (Kelley et al., 1987)
found in the Danainae, dehydropyrrolizidine alkaloids in the Ithomiinae (Brown,
1987; Brown et al., 1991), and cyanogenic glycosides in the Heliconiinae (Davis &
Nahrstedt, 1985; Nahrstedt, 1985). Chemical defences in the two Callicore species,
Diaethria clymena, Biblis f!yperia and Stalachtis phlegia, on the other hand, remain largely
unexplored and should be investigated further in future studies.
Although most butterflies taste-rejected by birds were released alive and without
apparent injury, taste-rejections were rare and a large proportion of so called
unpalatable species were eaten when captured by birds. Thus, from the point of view
of individual survival, unpalatability as a defensive strategy seemed to be effective
only for Parides and Battus species, which were usually released by birds after pecking.
Most of the other species are at a high risk of predation when sampled by kingbirds,
and until birds learn to reject them on sight many other individuals may be killed.
This picture contrasts strongly with the results ofJarvi etal. (1981), Wicklund & Jarvi
(1981), and Engen, Jarvi & Wicklund (1986) who found or predicted a very low
probability of death for aposematic prey handled for the first time by predators. It
also indicates that kin selection could be required for the evolution of unpalatability
and/or aposematism in several butterfly taxa, as predicted by Fisher (1930). A high
mortality of aposematic butterflies attacked by birds in natural conditions has been
found also for several Ithomiinae species that form large aggregations during the dry
PALATABIUTY AND ESCAPING IN BUTTERFUES
359
season in South Brazil (Brown & Vasconcellos-Neto, 1976), and in the overwintering
colonies of Danaus plexippus in Mexico (reviewed by Brower & Calvert, 1985; and
Brower, 1988).
Mimicry
Data indicate that Batesian mimics (= mimics always eaten) tend to be rare in all
mimetic complexes. Only two species tested, Consulfabius and Eresia eunice, seemed to
be true Batesian mimics in the "Tiger" pattern, the largest mimetic complex in the
area (Appendix; see also Brown & Benson, 1974; Brown, 1988). The feeding
experiments with Heraclides Iryppason indicate that it is at least less unpalatable than
Parides though the number of insects tested was low. This is also the case for Agraulis
vanillae, Dryadula phaetusa, and Dryas iulia which seem to be Batesian mimics in the
"Orange" complex. Siderone martesia mimics Callicore and several other species.
However, mimicry in this complex is still poorly documented (but see also Descimon,
1988; Brown, 1988; Pinheiro & Martins, 1992). Other species always eaten by birds
in the "Red-ray", "Tiger", and "Monarch" pattern groups require further
investigation, since they were rare in the field. It is possible that they also store the
chemical compounds commonly found in closely related species (see Brown &
Francini, 1990 for chemical defences in Actinote) and should not be regarded as
Batesian mimics.
No evidence of unpalatability was found for species in the "Adelpha-Doxocopa" (see
also Aiello, 1984) and the "Green-and-Black" pattern groups. Therefore, the
similarities of colour pattern found among species in these groups (see Appendix)
cannot be interpreted in terms of classical mimicry. An alternative explanation
accepted by many authors (Van Someren &Jackson, 1959; Mallet & Singer, 1987;
Srygley, 1994) is that mimicry can also evolve in species with a good ability to escape.
Gibson (1974, 1980) showed that birds can be taught to avoid artificial prey that
suddenly disappears before it can be eaten. Several species in both complexes seemed
to exhibit a high ability to escape predators. However, they did not elicit sightrejection by birds, as observed in other mimetic butterflies. Thus, the hypothesis of
escape mimicry also requires further investigation.
In contrast, some results indicate that at least some palatable butterflies, such as
the two Morpho species (tested by Chai, 1986, 1990), advertise to predators that they
are not easily captured. These butterflies are easily detected in the field and exhibit
several attributes commonly found in aposematic species that could facilitate
learning by birds (see examples in Guilford & Dawkins, 1991). They are virtually
uncatchable by kingbirds and other tyrant-flycatchers (like H. ferruginea; Pinheiro,
unpub. data) and apart from the mimetic species only these butterflies were
occasionally rejected on sight by birds. To my knowledge, this is the best evidence in
prey insects for aposematism not related to palatability but to escaping ability (see
also Young, 1971).
Escaping
The negative correlation found between unpalatability and escaping ability
supports the assumption that these traits evolved in butterflies as alternative strategies
360
C. E. G. PINHEIRO
to avoid predation by birds, as predicted by many authors (Poulton, 1890; Fisher,
1930; Chai, 1990; Chai & Srygley, 1990; Endler, 1991; Malcolm, 1992; Srygley,
1994). However, exceptions did occur and seemed to be associated with other kinds
of defence. This is the case for some cryptic butterflies easily captured by birds, which
probably gain further protection by not being easily detected, as well as some
Batesian mimics (such as E. eunice) that probably rely on mimicry to avoid being
attacked by predators.
As a general rule larger butterflies tended to escape bird attacks more frequently
than small ones. Some of them are clearly powerful fliers which evade predators
through high speed and sometimes very unusual aerial manoeuvres. A positive
correlation between escaping and the wing size in butterflies has been also found by
Chai & Srygley (1990) and Srygley (1994). However, Srygley found that escaping in
some groups of butterflies correlates better with traits such as the position of the
centre of the body mass or wing mass, and sometimes with the wing shape.
Escaping can also occur by losing parts of the wings when pecked by birds. This
kind of defence provides the butterfly with a last chance to escape predators. It was
frequently observed in the two Morpho species, where in combination with a
characteristic "bobbing flight", it renders these butterflies virtually uncatchable by
kingbirds. It was also observed occasionally in several other species (such as Heraclides
torquatus and Protesilaus sp that escaped from birds during handling). However, it
seems to be restricted to palatable butterflies that, in contrast to chemically defended
species, have relatively soft wings and usually do not stop struggling when captured
by birds (Chai, 1990).
Most other aspects related to the escape tactics of butterflies remain uninvestigated. The earlier detection of predators by butterflies seems to be an important
factor in determining whether they could escape. Frontal attacks, especially, are
much more easily detected and unsuccessful than attacks on the hindwings.
ACKNOWLEDGEMENTS
I thank the Companhia Yale do Rio Doce for facilities in the Carajas region.
Rupeci, Edivaldo L.A. (CYRD) and Helio ]. Cunha (DnB) helped in the field. Prof.
D. Spencer Smith, Dr G. McGavin, Dr K.S. Brown Jr., and two anonymous
reviewers read drafts of the manuscript and furnished many helpful comments. Dr
K.S. Brown Jr. also identified several butterfly species. Financial support to the
author was provided by the Conselho Nacional de Desenvolvimento Cientifico e
Tecnologico-CNPq.
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Ithomiinae
Heliconiinae
Danainae
Charaxinae
NyrnphaIidae/
Acreinae
Apaturinae
Family/ subfam.
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
No.
Mimetic Complex
3
12
2
12
2
5
12
13
3
10
11
5
13
13
11
10
12
12
10
3
5
10
2
6
10
2
11
1
10
11
7
5
3
6
12
Number of
butterflies
1
0
0
0
0
0
0
0
0
0
I
1
2
2
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
3
2
2
SightRejected
0
0
0
0
0
0
0
0
0
0
2
0
3
2
0
I
0
0
1
0
0
I
0
0
2
0
I
0
2
I
1
0
0
0
3
TasteRejected
2
10
2
10
2
4
10
10
2
8
8
4
7
8
10
9
10
10
9
2
5
9
2
6
8
2
9
I
8
9
6
4
0
4
7
Eaten
Responses of wild Tyrannus melancholicus to butterflies
Actinote thalia
Tiger?
'Adelpha-Doxocopa'
Doxocopa Laure
Doxocopa linda ornata
Doxocopa selina
'Adelpha-Doxocopa'
Tiger-B.m.
Consulfabius
Memphis morous
Memphis ryphea
Preponademophon
Prepona laertes
Sideronemarthesia
'Callicore'- B.m.
Danaus eresimus plexaure
Monarch
Danaus gilippus
Monarch
Monarch
Danaus pkxippus erippus
Lycorea cleobaea
Tiger
Agraulis vanillae
Orange
Dionejuno
Orange
DryaduLa phaetusa
Orange
Dryas iulia
Orange
Eueides aliphera
Orange
Eueides isabella
Tiger
Eueides lybia
Orange
Eueides tales
Red-ray
Eueides vibilia
?
Heliconius burney
Red-ray
Heliconius erato
Red-ray
Heliconius ethilla
Tiger
Heliconius melpomene
Red-ray
Heliconius numata silvana
Tiger
'Sara'
Heliconius sara
'Sara'
Heliconius wallacei
Heliconius xanthocles
Red-ray
Philaethria spp**
Green-Black
Dircenna dero
Transparent
Hypothyris euclea
Tiger
Hypothyrisdaphnis daphnoides
Tiger
Butterfly
APPENDIX.
0
2
0
2
0
1
2
3
I
2
0
0
1
1
1
0
2
2
0
0
0
0
0
0
0
0
1
0
0
I
0
I
0
0
0
2
15
3
14
3
7
16
18
5
12
13
5
13
14
15
13
16
15
12
2
5
13
2
7
11
2
13
I
13
14
7
7
0
4
12
Number of
Not
Captured Attacks
0
5
1
4
1
3
6
8
3
4
3*
I
3*
4
5*
3
6
5*
2*
0
0
3
0
1
I
0
3
0
3
4
0
3
0*
0
2
Unsuccessful
Attacks
cc
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uo
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0
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S
>-
~
Limenitidinae
Family/subfam.
Butterfly
Hypothyris ninonia
Hypothyris vallonia
Mechanitis mazeus visenda
Mechanitis polymnia
Melinaea ludovica
Melinaea mneme
Methona themisto
Thyridia psidii
Adelpha cytherea
Adelpha mesentina
Adelpha phylaca
Adelpha iphiclus
Biblis hyperia
Callicore astarte
Callicore maximilla
Caumepheleaeontius (m)
Catonephele aeontius (f)
Catonephele numilia (m)
Catonephele numilia (f)
Coloburadirce
Diaethria clymena
Eunica concordia
Dynanime athemon
Hamadryas chloe
Hamadryas feronia
Hamadryas laodamia (m)
Hamadryas laodamia (f)
Hamadryas velutina (m)
Historis odius
Marpesia chiron
Marpesia norica
Marpesia orsilochus
Napeocles jucunda (m)
Napeocles jueunda (f)
Nessaea batesii (m)
Nessaeaobrinus (m)
No.
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51a
51b
52a
52b
53
54
55
56
57
58
59a
59b
60
61
62
63
64
65a
65b
66
67a
'Diaethria'
'Adelpha-Doxocopa'
'Adelpha-Doxocopa'
'Biblis'
'Callicore '
'Callicore '
Tiger
Tiger
Tiger
Tiger
Tiger
Tiger
Transparent
Transparent
'Adelpha-Doxocopa'
Mimetic Complex
13
2
13
12
3
6
2
1
11
5
6
12
2
5
6
6
8
7
6
4
13
3
2
11
12
5
8
3
3
12
12
11
8
6
4
8
TasteRejected
3
0
2
3
0
1
0
0
0
0
0
0
1
1
1
0
0
0
0
0
4
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
SightRejected
3
0
3
2
0
2
2
1
0
0
0
0
0
1
2
0
0
0
0
0
3
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Continued
Number of
butterflies
APPENDIX.
7
2
8
7
3
3
0
0
10
3
5
10
1
3
3
5
5
5
5
4
6
3
2
10
10
4
6
3
1
10
10
10
5
5
3
6
Eaten
0
0
0
0
0
0
0
0
1
2
1
2
0
0
0
1
3
2
1
0
0
0
0
1
2
1
2
0
2
2
2
1
3
1
1
2
11
9
5
11
2
13
12
4
4
0
0
15
6
7
15
2
4
5
9
10
11
8
5
11
4
2
16
15
7
10
4
4
17
15
16
11
Not
Number of
Captured Attacks
1
0
3
2*
1
0
0
0
5
3
2
5
0
0
1
4
5
6
3
1
1
1
0
6
5
3
4
1
3
7
5
6
6
4
2
5
Unsuccessful
Attacks
""
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0
~
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Butterfly
Nessaea obrinus (f)
Paulograma frYracmon
Pyrrhogyra crameri
Pyrrhogyra neaerea
Pyrrhogyra otolais
Temenis laothoe
Tigridia acesta
Anartia amathea
Anartia jatrophae
Eresiaclara
Eresiaeunice
Junonia evarete
Siproeta stelenes
Morpho achilles
Morpho menelaus (m)
Battus crassus
Battus polydamas
Eurytides dolicaon
Heraclides hyppason
Heraclides thoas
Heraclides torquatus
Parides lysander (m)
Parides lysander (f)
Parides neophilus (m)
Parides neophilus (f)
Parides panthonus (m)
Paridespanthonus (f)
Protesilausspp***
Stalachtis phlegia
Chioidescatillus
Urbanus procne
Urbanus teleus
Hesperidae sp 1
No.
67b
68
69
70
71
72
73
74
75
76
77
78
79
80
81
82
83
84
85
86
87
88a
88b
89a
89b
90a
90b
91
92
92
94
95
96
'Stalachtis'
'Parides'
'Parides'
'Parides'
'Parides'
'Parides'
'Parides'
'Parides '- B.m. (?)
'Polydamas'
'Crassus'
Green-Black
Tiger- B.m.
'Callicore'I
Mimetic Complex
5
1
2
12
1
10
4
2
6
3
10
4
5
9
10
1
2
2
6
1
2
8
2
6
5
3
2
5
1
2
4
1
5
668
Number of
butterflies
0
0
0
0
0
0
0
0
0
0
0
0
0
4
3
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
42
SightRejected
Continued
0
0
0
0
58
I
0
I
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
0
0
0
0
6
2
3
4
3
TasteRejected
4
1
2
10
1
10
4
2
6
3
10
3
4
0
I?
0
0
2
5
1
1
2
0
2
1
0
1
3
0
1
2
1
3
486
Eaten
0
0
2
0
0
0
0
0
0
0
1
1
5
6
0
0
0
1
0
1
0
0
1
0
0
0
2
0
1
2
0
2
82
I
7
1
3
16
1
13
4
2
9
3
12
6
7
18
32
0
3
3
8
2
3
10
2
8
7
4
2
7
1
2
4
1
5
830
Not
Number of
Captured Attacks
3
0
1
6
0
3
0
0
3
0
2
3
3
18*
31*
0
2
1
3
1
2
2
0
3
2
1
0
4
0*
1
2
0
2
287
Unsuccessful
Attacks
*Observed in the city. **Includes two species in the dido complex. ***lncludes P. protesilaus and P. glaucolaus. ?=not seen (bird flew away with the butterfly). m = male;
f = female; B.m. = Batesian mimic.
Total
Riodinidae
Hesperidae
Papilionidae
Morphinae
Nymphalinae
Family/subfam.
APPENDIX.
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