THE ENEMIES OF BUTTERFLIES
The theory of mimicry demands that butterflies should have enemies, and
further that those enemies should exercise a certain discrimination in
their attacks. They must be sufficiently observant to notice the difference
between the mimetic and the non-mimetic form; they must be sufficiently
unobservant to confuse the mimetic form with the unpalatable model. And, of
course, they must have enough sense of taste to dislike the unpalatable and
to appreciate the palatable varieties. What these enemies are and whether
they can be supposed to play the part required of them we may now go on to
consider.
Butterflies are destroyed in the imago state principally by three groups of
enemies--predaceous insects, lizards, and birds. It is known that monkeys
also devour butterflies to some extent, but such damage as they inflict is
almost certainly small in comparison with that brought about by the three
groups already mentioned. In view of the very different nature of these
groups it will be convenient to consider them separately. {105}
I. _Predaceous Insects._ Butterflies are known to be preyed upon by other
insects of different orders, and a considerable number of observations have
recently been gathered together from various sources and put on record by
Professor Poulton[55]. These observations shew that butterflies may be
devoured by mantids, dragon-flies, and blood-sucking flies of the families
Empiidae and Asilidae. For mantids the records are scanty, but they have
been observed to kill presumably distasteful forms as often as those which
are considered palatable. An interesting set of experiments was made by G.
A. K. Marshall on captive mantids in Africa[56]. Of the eleven individuals
representing several species with which he experimented, some ate every
butterfly offered, including the distasteful Danaines and Acraeines.
Others, however, shewed some distaste of the Acraeines and would not devour
them so freely as butterflies of other species. There are no grounds,
however, for supposing that the mantids had any appreciation of the warning
coloration of the Acraeines. Whether completely eaten or not the Acraeines
were apparently sufficiently damaged to prevent their taking any further
part in the propagation of their species. Warning coloration is not of much
service to its possessor who has to be tasted and partially eaten before
being eventually rejected. Even if some mantids shew distaste of certain
unpalatable butterflies, that distaste is probably seldom {106} exercised
with a gentleness sufficient to ensure that the butterfly reaps the reward
of its disagreeable nature. And unless, of course, the butterfly is allowed
to do so the enemy can play no part in the production or maintenance of a
mimetic resemblance.
What is true for mantids is probably also true for the other groups of
predaceous insects. Dragon-flies and wasps have been recorded as attacking
the distasteful as well as butterflies of unprotected groups. Among the
most serious enemies of butterflies must probably be reckoned the
blood-sucking Asilids. These powerful and ferocious flies seize butterflies
on the wing with their strong claws and plunge their proboscis into the
thorax. Apparently they inject some swift poison, for the butterfly is
instantly paralysed, nor is there any sign of struggle. The Asilid flies
off with its victim, sucking the juices as it goes. There can be no doubt
in the mind of any one who has watched these creatures hawking butterflies
that their natural gifts are such as to enable them to exercise
discrimination in their food. Most insect life is at their mercy but they
appear to exercise no choice, seizing and devouring the first flying thing
that comes within easy reach. Certainly as regards butterflies palatability
or the reverse makes no difference, and they are known to feed
indiscriminately both upon the evil-flavoured and upon the good. Taking it
all together the evidence is such that we cannot suppose predaceous insects
to pay any attention to warning colours, and, therefore, we cannot regard
them as playing any part in connection with mimetic resemblance. {107}
II. _Lizards._ In those parts of the world where lizards of larger size are
abundant there is plenty of evidence that certain species are very
destructive to butterfly life. As might be expected this is especially true
of forms which are either arboreal or semi-arboreal in habit. Among the
reptiles of Ceylon, for example, are several species of the genus
_Calotes_, of which two, _C. ophiomachus_ and _C. versicolor_, are
particularly abundant. In appearance and habits they are not unlike
chameleons though far more active in their movements. Like chameleons, too,
they are able to change colour, and the fact that they can assume a
brilliant scarlet hue about the head and neck has probably led to their
popular name of "blood-suckers." It is not impossible that the assumption
of this scarlet coloration may serve as a lure to bring insects within
range. These lizards have often been observed to seize and devour
butterflies. Moreover, it is a common thing to find butterflies with a
large semi-circular patch bitten out of the hind wings, and there is little
doubt but that such injuries have been inflicted by lizards. There is,
however, no evidence to suggest that they exercise any discrimination in
their choice of the butterflies which they attack. This is borne out by
their behaviour towards various species offered to them, both when at
liberty and when caged. In an ingenious series of experiments Col. Manders
brought various butterflies within reach of a _Calotes_ by the help of a
fishing-rod and a long line of fine silk, by this means simulating natural
conditions as far as possible. {108} He found that the lizards ate the
so-called distasteful forms such as _Danais chrysippus_, _Euploea core_,
_Acraea violae_, and _Papilio hector_, as readily as the presumably more
palatable forms[57]. In captivity, too, they will take any butterfly as
readily as another. Experiments by Finn[58] and by the writer[59] proved
that they ate Danaids, Euploeas, and _Papilio aristolochiae_ without any
hesitation so long as the insects were alive and moving. When, too, a
mixture of different species, some with and some without warning
coloration, was given to them all were eaten, nor was there any
discrimination evidenced in the order in which they were taken. The lizard
simply took the first that came within reach and went on until the whole
lot was devoured, wings and all.
Some experiments by Miss Pritchett on the American lizard _Sceleporus
floridanus_ point to the same conclusion[60]. She found that it took
without hesitation any butterfly offered to it including the presumably
distasteful models _Danais archippus_ and _Papilio philenor_ (cf. pp. 45
and 49). On the other hand, another species of lizard with which Miss
Pritchett experimented, _Gerrhonotus infernalis_, refused all the
butterflies offered to it, though it fed freely on Orthopterous insects as
well as on spiders and scorpions.
It seems clear from these various observations and {109} experiments that
certain lizards devour butterflies freely, but that they do not exercise
any discrimination in the species which they attack. All are caught and
devoured indiscriminately, so that in spite of the fact that such lizards
are among the most serious enemies of butterflies we cannot suppose them to
play any part in establishing a mimetic resemblance.
III. _Birds._ The relations which exist between butterflies and their bird
enemies have for many years been the subject of keen discussion. It is
generally recognised that if mimetic resemblances become established
through the agency of discriminating enemies those enemies must be birds.
Hence those interested in the question of mimicry have for some years past
turned their attention to birds more than to the other enemies of
butterflies. That many birds systematically feed on butterflies is a fact
that does not admit of doubt. It is true that, as Mr Marshall points out in
the valuable paper in which he has summarised the evidence[61],
observations of birds eating butterflies are relatively scanty. Though, as
he points out, this is equally true for other groups of insects besides
butterflies, bird attacks on butterflies, owing to the conspicuous nature
of the victim, are much more likely to attract attention than attacks on
other groups. We are still without much information as to the extent to
which birds destroy butterflies and as to whether they shew any decided
preference for certain species over others. A careful examination of the
contents of the {110} stomachs of large numbers of insectivorous birds in a
tropical area would go some way towards deciding the matter, but at present
such information is lacking. We have to rely upon the existing observations
of birds attacking butterflies in the wild state, and upon certain feeding
experiments made with captive birds.
Observations on birds attacking butterflies where mimetic forms occur have
been made almost entirely in certain parts of Africa, in India, and in
Ceylon. For Africa, Marshall has collected some forty-six observations of
which almost half are concerned with Pierines. The remainder include four
instances of attacks on species of _Acraea_, a genus which on the mimicry
theory must be regarded as among the most unpalatable of butterflies.
The records from the Indo-Malayan region (principally India and Ceylon) are
somewhat more numerous and here again more than one-third of them refer to
Pierines. Among the others are records of the distasteful forms _Euploea
core_, _E. rafflesii_, _Acraea violae_, and _Papilio hector_ being taken
and devoured.
There is one interesting record which seems to suggest that Swinhoe's
Bee-Eater (_Melittophagus swinhoei_) may exercise that discrimination in
the butterflies it attacks which is demanded on the mimicry theory.
Lt.-Col. Bingham on one occasion in Burma noticed this species hawking
butterflies. He records that they took _Papilio erithonius_, _P. sarpedon_,
_Charaxes athamas_, _Cyrestis thyodamas_, and _Terias hecabe_, and probably
also species of the genera _Prioneris_, _Hebomoia_ (Pierines), {111}
_Junonia_ and _Precis_ (Vanessids). And he goes on to say: "I also
particularly noticed that the birds never went for a _Danais_ or _Euploea_,
or for _Papilio macareus_ and _P. xenocles_, which are mimics of Danais,
though two or three species of _Danais_, four or five of _Euploea_, and the
two above-mentioned mimicking _Papilios_ simply swarmed along the whole
road[62]."
Marshall also quotes a case of attack by a green bee-eater on a _Danais_ in
which the butterfly was caught and subsequently rejected, after which it
flew away. Little stress, however, can be laid upon this case in view of
the more recent data brought together by Col. Manders and Mr Fryer.
Discussing the attacks of birds on butterflies in Southern India and
Ceylon, Col. Manders gives the following quotation[63] from a letter of Mr
T. N. Hearsy, Indian Forest Service:
"Coimbatore, 6. 6. 10.... I have frequently seen the common green bee-eater
(_Merops viridis_) and the king-crow (_Buchanga atra_) take butterflies on
the wing, the butterflies being _Catopsilia pyranthe_, _C. florella_,
_Terias hecabe_ and _Papilio demoleus_. The bee-eater I have also seen
taking _Danais chrysippus_ and _Danais septentrionis_, and I remember to
have been struck with their taste for those latter...."
Col. Manders also brings forward evidence for these Danaids and Euploeas
being eaten by Drongos and by the paradise flycatcher. Still more recently
an interesting contribution to the matter has been made by {112} Mr J. C.
F. Fryer[64]. The Ashy Wood-swallow (_Artamus fuscus_) had been recorded on
two occasions as having attacked _Euploea core_. Mr Fryer was fortunate in
coming across this bird in the gardens at Peradeniya, near Kandy, at a time
when _Euploea core_ and _Danais septentrionis_ were particularly abundant,
and he watched a number of them systematically hawking these presumably
unpalatable species. As he observes, "in Ceylon a resemblance to the genera
_Danais_ and _Euploea_ is doubtfully of value; in fact in the neighbourhood
of Wood-swallows it is a distinct danger." Fryer also noted that the
mimetic forms of _P. polytes_ were taken as well as the non-mimetic.
For tropical Central and South America, that other great region where
mimetic forms are numerous, there are unfortunately hardly any records of
butterflies attacked by birds. Bates stated that the Pierines were much
persecuted by birds, and his statement is confirmed by Hahnel, but exact
observations for this region are remarkably scanty. Belt observed a pair of
birds bring butterflies and dragon-flies to their young, and noticed that
they brought no Heliconii to the nest although these swarmed in the
neighbourhood[65]. On the other hand, Mr W. Schaus[66], from an experience
of many years spent in the forests of Central America, considers that the
butterflies of this region are hardly, if ever, attacked by birds. {113}
For North America Marshall records over 80 cases of birds attacking
butterflies. Among them is an interesting record of a bird seizing and
rejecting a specimen of _Anosia plexippus_ (= _Danais archippus_), one of
the few Danaines found in this region.
It must be admitted that the data at present available with regard to the
attacks of birds upon butterflies under natural conditions are too meagre
to allow of our coming to definite conclusions on the points at issue. It
is safe to say that a number of species of birds have been known to attack
butterflies--that a few out of the number feed upon butterflies
systematically--that some of the most persistent bird enemies devour the
presumably protected forms as freely as the unprotected--but that in a few
instances there is some reason for supposing that the bird discriminates.
Beyond this it is unsafe to go at present.
In attempting to come to a decision as to the part played by birds in the
destruction of butterflies an evident desideratum is a knowledge of the
contents of the stomachs of freshly killed birds. Unfortunately few
systematic observations of this nature exist. G. L. Bates[67], when
collecting in the Southern Cameroons, noted the stomach contents of a
considerable number of birds. The remains of beetles were recognised in 213
cases: Orthoptera in 177: ants in 57 (mostly in stomachs of birds of the
genus _Dendromus_): other Hymenoptera in 8: coccids in 32: bugs in 19:
white ants in 31: slugs and snails in 24: spiders in 85 {114} (mostly in
Sunbirds): millipedes in 20; but in no single instance were the remains of
butterflies found. More recently Bates' account has been criticized by
Swynnerton[68] who comments on the difficulty of identifying butterfly
remains as compared with those of beetles and grasshoppers. He states that
the pellets ejected by captive birds after a meal of butterflies contain
only fine debris which is very difficult to identify. Further, he found
that of twenty small bird excreta collected in the forest no less than
eighteen contained scales and small wing fragments of Lepidoptera.
Some attention has been paid to the relation between birds and butterflies
in the United States, and under the auspices of the Department of
Agriculture a large number of birds' stomachs have been investigated.
Careful examination of some 40,000 stomachs of birds shot in their natural
habitats resulted in the discovery of butterfly remains in but four. It
cannot, therefore, be supposed that birds play much part in connection with
such mimetic resemblances as are found in North America (cf. pp. 45-49).
Nevertheless, it is known that on occasion large numbers of butterflies may
be destroyed by birds. An interesting case is described by Bryant[69] of an
outbreak in North California of _Eugonia californica_, a close relative of
the tortoiseshell. The butterfly was so abundant as to be a plague, and
five species of birds took advantage of its great abundance to prey largely
upon it. From {115} his examination of the stomachs Bryant came to the
conclusion that some 30% of the food of these five species was composed of
this butterfly. The stomachs of many other species were examined without
ever encountering butterfly remains. Nor did field observations support the
view that any species, other than the five specially noted, ever attacked
these butterflies. The case is of interest in the present discussion as
evidence that the identification of butterfly remains in the stomachs of
birds is by no means so difficult as some observers suggest.
Besides this evidence derived from observations upon birds in the wild
state some data have been accumulated from the experimental feeding of
birds in captivity. Of such experiments the most extensive are those of
Finn[70] in South India. He experimented with a number of species of
insectivorous birds belonging to different groups. Of these he found that
some, among which may be mentioned the King-crow, Starling, and
Liothrix[71], objected to Danaines, _Papilio aristolochiae_ and _Delias
eucharis_, a presumably distasteful Pierine with bright red markings on the
under surface of the hind wings (Pl. II, fig. 1). In some cases the bird
refused these forms altogether, while in others they were eaten in the
absence of more palatable forms. The different species of birds often
differed in {116} their behaviour towards these three "nauseous" forms. The
Hornbill, for example, refused the Danaines and _P. aristolochiae_
absolutely, but ate _Delias eucharis_. Some species again, notably the
Bulbuls (_Molpastes_) and Mynahs, shewed little or no discrimination, but
devoured the "protected" as readily as the "unprotected" forms. Finn also
states that "_Papilio polytes_ was not very generally popular with birds,
but much preferred to its model, _P. aristolochiae_."
In many of Finn's experiments both model and mimic were given to the birds
simultaneously so that they had a choice, and he says that "in several
cases I saw the birds apparently deceived by mimicking butterflies. The
Common Babbler was deceived by _Nepheronia hippia_[72] and Liothrix by
_Hypolimnas misippus_. The latter bird saw through the disguise of the
mimetic _Papilio polites_, which, however, was sufficient to deceive the
Bhimraj and King-crow. I doubt if any bird was impressed by the mimetic
appearance of the female _Elymnias undularis_" (cf. Pl. IV, fig. 5). Finn
concluded from his experiments that on the whole they tended to support the
theory of Bates and Wallace, though he admits that the unpalatable forms
were commonly taken without the stimulus of actual hunger and generally
without signs of dislike. Certainly it is as well to be cautious in drawing
conclusions from experiments with captive birds. The King-crow, for
instance, according to Finn shewed a marked dislike for Danaines in
captivity; yet Manders records this {117} species as feeding upon Danaines
under natural conditions (cf. p. 111).
A few further experiments with the birds of this region were carried out by
Manders[73] in Ceylon. The results are perhaps to be preferred to Finn's,
as the birds were at liberty. Manders found that the Brown Shrike (_Lanius
cristatus_) would take butterflies which were pinned to a paling. In this
way it made off with the mimetic females of _Hypolimnas bolina_ and _H.
misippus_, as well as with _Danais chrysippus_ and _Acraea violae_ which
were successively offered to it. Evidently this species had no repugnance
to unpalatable forms. Manders also found that a young Mynah allowed
complete liberty in a large garden would eat such forms as _Acraea violae_
and _Papilio hector_. As the result of his experience Manders considers
that the unpalatability of butterflies exhibiting warning coloration has
been assumed on insufficient data, and he is further inclined to doubt
whether future investigations will reveal any marked preference in those
birds which are mainly instrumental in the destruction of butterflies.
A few experiments on feeding birds with South African butterflies are
recorded by Marshall. A young Kestrel (_Cerchneis naumanni_) was fed from
time to time with various species of butterflies. In most cases the
butterflies offered were eaten even when they were species of _Acraea_. On
the other hand _Danais chrysippus_ was generally rejected after being
partly {118} devoured. When first offered this unpalatable species was
taken readily and it was only after it had been tasted that the bird
rejected it. When offered on several subsequent occasions it was partly
eaten each time, and the behaviour of the Kestrel did not suggest that it
associated a disagreeable flavour even with this conspicuous pattern.
Another young Kestrel (_Cerchneis rupicoloides_) was also used for
experiment. At first it would not take butterflies and at no time did it
shew any fondness for them. Indeed it is doubtful from the way in which
they seem to have shaped at the insects whether either of these Kestrels
had had any experience of butterflies before the experiments began.
A Ground Hornbill with which Marshall also experimented ate various
species, including _Acraea_, but, after crushing it, refused the only
_Danais chrysippus_ offered. It is hardly likely that this large omnivorous
bird operates as a selecting agent in cases of mimicry.
In an interesting paper published recently McAtee[74] discusses the value
of feeding experiments with animals in captivity as a means of indicating
their preference for different articles of diet. After reviewing the
various evidence brought forward he concludes that the food accepted or
rejected by captive animals is very little guide to its preferences under
natural conditions. He points out that a bird in captivity not infrequently
rejects what is known to form a main staple of its diet in nature, and that
conversely it may eagerly accept something which, in the wild state, it
{119} would have no opportunity of obtaining. Great caution must,
therefore, be exercised in the interpretation of feeding experiments made
with birds in captivity.
It appears to be generally assumed that colour perception in birds is
similar to what it is among human beings, but some experiments made by
Hess[75] render it very doubtful whether this is really the case. In one of
these experiments a row of cooked white grains of rice was illuminated by
the whole series of spectral colours from violet to deep red. Hens which
had been previously kept in the dark so that their eyes were adapted to
light of low intensity were then allowed to feed on the spectral rice. The
grains illuminated by green, yellow, and red were quickly taken, but the
very dark red, the violet, and the blue were left, presumably because the
birds were unable to perceive them. Again, when the birds were given a
patch of rice grains of which half was feebly illuminated by red light and
the other half more strongly by blue light, they took the red but left the
blue. Previous experiment had shewn that with ordinary white light the
birds always started on the best illuminated grains. It seems reasonable to
conclude, therefore, that in the red-blue experiment the feebly illuminated
red grains were more visible than the far more strongly lighted blue ones.
It might be objected that the birds had a prejudice against blue, but, as
Hess points out, this is almost certainly not the case because they took
grains {120} which were very strongly illuminated with blue. Results of a
similar nature were also obtained from pigeons, and from a kestrel which
was fed with pieces of meat lighted with different colours.
On the whole these experiments of Hess convey a strong suggestion that the
colour perceptions of birds may be quite different from our own, more
especially where blue is concerned. Great caution is needed in discussing
instances of mimicry in their relation to the bird, for we have no right to
assume that the bird sees things as we do. On the other hand, it is a
matter of much interest to find that in general blue plays relatively
little part in cases of mimetic resemblance among butterflies; some
combination of a dark tint with either red, white, brown, or yellow being
far more common.
It will probably be admitted by most people that the evidence, taken all
together, is hardly sufficient for ascribing to birds that part in the
establishing of a mimetic likeness which is required on the theory of
mimicry. That birds destroy butterflies in considerable numbers is
certainly true, but it is no less true that some of the most destructive
birds appear to exercise no choice in the species of butterfly attacked.
They simply take what comes first and is easiest to catch. It is probably
for this reason that the Wood-swallow feeds chiefly on Euploeines and
Danaines (cf. p. 112). It is probably for this reason also that such a
large proportion of the records of attacks on butterflies under natural
conditions refer to the Pierines; for owing to {121} their light colour it
is probable that the "Whites" are more conspicuous and offer a better mark
for a bird in pursuit than darker coloured species.
_Mammals._ Apart from man it is clear that only such mammals as are of
arboreal habits are likely to cause destruction among butterflies in the
imago state. Apparently there are no records of any arboreal mammal, except
monkeys, capturing butterflies in the wild state, nor is there much
evidence available from feeding experiments. But such evidence as exists is
of considerable interest. As the result of feeding butterflies of different
sorts to an Indian Tree-shrew (_Tupaia ferruginea_) Finn[76] found that it
shewed a strong dislike to Danaids and to _Papilio aristolochiae_ though it
took readily _Papilio demoleus_, _Neptis kamarupa_, and _Catopsilia_ (a
Pierine). It is fairly certain that if the Tree-shrew is an enemy of
butterflies in the wild state it is a discriminating one.
The other mammals with which experiments have been made are the common
baboon, a monkey (_Cercopithecus pygerythrus_), and a mongoose (_Herpestes
galera_)--all by Marshall[77] in South Africa. The mongoose experiments
were few and inconclusive, nor is this a matter of much moment as it is
unlikely that this mammal is a serious enemy of butterflies.
The monkey ate various forms of _Precis_ (a Vanessid), after which it was
given _Acraea halali_. This distasteful form was "accepted without
suspicion, but when {122} the monkey put it into his mouth, he at once took
it out again and looked at it with the utmost surprise for some seconds,
and then threw it away. He would have nothing to do with an _Acraea
caldarena_ which I then offered him[78]."
The experiments with the baboons were more extensive. Two species of
_Acraea_, _halali_ and _axina_, were recognised when first offered and
refused untasted. _Danais chrysippus_, on the other hand, was tasted on
being offered for the first time, and then rejected. This species was twice
offered subsequently and tasted each time before being rejected. When
offered the fourth time it was rejected at sight. The baboon evidently
learned to associate an unpleasant taste with the _chrysippus_ pattern. At
this stage it would have been interesting to have offered it some
well-known mimic of _chrysippus_, such as the female of _Hypolimnas
misippus_ or the _trophonius_ form of _Papilio dardanus_, but this
experiment was unfortunately not made. Marshall did, however, offer it at
the same time a specimen each of _Byblia ilithyia_ (a Vanessid) and of
_Acraea axina_ to which it bears a general resemblance. The baboon took the
former but neglected the latter altogether. The general resemblance between
the two species was not sufficiently close to deceive it.
These experiments with mammals, though few in number, are of unusual
interest. Should they be substantiated by further work it is not impossible
{123} that, as a factor in the establishing of a mimetic likeness, a
stronger case may be made out for the monkey than the bird. The monkey
apparently eats butterflies readily[79]: owing probably to a keener sense
of smell it shews far less hesitation as to its likes and dislikes: its
intelligence is such that one can easily imagine it exercising the
necessary powers of discrimination; in short it is the ideal enemy for
which advocates of the mimicry theory have been searching--if only it could
fly. As things are its butterfly captures must be made when the insect is
at rest, probably near sunrise and sunset, and this leads to a difficulty.
Most butterflies rest with their wings closed. In many of the well-known
cases of mimicry the pattern on the under surface of the mimic's wings
which would meet the monkey's eye is quite different from that of its
model. It is difficult in such cases to imagine the monkey operating as a
factor in establishing a resemblance between the upper surfaces of the
wings of the two unrelated species. On the other hand, some butterflies,
{124} _e.g._ _Papilio polytes_, rest with wings outspread, and there are
rare cases, such as that of _P. laglaizei_ (p. 27), where the most striking
point about the resemblance is only to be appreciated when the insects are
at rest with their wings closed. In such cases it is conceivable that the
monkey may play a part in the elimination of the non-mimetic elements of a
palatable species which at the same time possessed a mimetic form closely
resembling another species disagreeable to the monkey's taste. As has been
pointed out earlier (p. 96) even a slight persecution directed with
adequate discrimination will in time bring about a marked result where the
mimetic likeness is already in existence. It is not impossible therefore
that the establishing of such a likeness may often be due more to the
discrimination of the monkey than to the mobility of the bird.
* * * * *
{125}