Mimicry in Butterflies/Chapter 9

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.

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. 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. 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 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.

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. 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. In captivity, too, they will take any butterfly as readily as another. Experiments by Finn and by the writer 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. 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 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, 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 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), 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 ."

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 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 Mr J. C. F. Fryer. 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. On the other hand, Mr W. Schaus, 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.

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, 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 (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 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 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 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 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, 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 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 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 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 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 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 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 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 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 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 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 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 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 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 ."

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 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 : 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, 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.