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-. 136 Zoologica: New York Zoological Society (42: 12 Crane: lmaginal Behavior in Butterflies of the Family Heliconiidae 137 1957] 1, I Enough corroborative observations have now I sequence of changes in colony functions have known, but they have reached their highest de by flowering weeds and by the pond. Branches been made in the field, however, to show that been studied in worker honeybees (Rosch, velopment in birds . . . So far as is at present with bromeliads attached stand upright at inter the apparent eccentricities are equally charac 1925), Polistes (Steiner, 1932) and in various known they have a comparatively insignificant vals against the netting, as a further aid in main teristic of free-flying butterflies. Further cor ants (e.g. Buckingham, 1910). Verlaine (1932) taining humidity and natural conditions. The roboration of the natural prevalence of the types reported differences between young and old role among insects. A thwarted solitary wasp, Bembex rostrata, when forced to remove pebbles wild banana group (Heliconia) beside the bog of behavior under consideration comes from the mason wasps in nest-repairing and provision be forms the coolest, most shady corner of the cage. fact that, now that the causes are better under havior, that of old bees late in the season being repeatedly from the mouth of its burrow merely buzzed loudly and ran around in a wide arc H. erato, melpomene and other shade-lovers in stood, the patterns shown in the insectaries are incomplete; this observation invalidated a con variably seek it out during the heat of the day. highly predictable. clusion drawn by Fabre (1879; ed. 1920) from (Nielsen, 1945). When experimenting with but terflies attracted to pieces of coloured paper In contrast, other species, such as H. isabella, Some of the behavioral discrepancies have experiments which he performed, using aged which is most active around noon, frequent the individuals. Pardi (1947) found that age was Dr. D. Ilse noticed movements which might proved to be due simply to age differences in the open center of the cage around a group of Lan one of the factors determining the status of in have been displacement activities (personal individuals observed. The full courtship pattern tana, B.idens and Asclepias. In this cage all of dividual Polistes females in a dominance hier communication) . Possibly one of the factors re characteristic of the species, for example, is the latter, favorite food blossoms of the heli elicited only in and by individuals between cer archy. Nielsen & Nielsen (1952) reported that sponsible for the apparently slower speciation of the migratory period of a pierid butterfly insects than birds (Mayr, 1942) is the greater coniids, thrive and are allowed to grow freely tain ages, although successful reproduction can over most of the cage. This scattering of a take place throughout a much longer portion of (Astia) was confined to a single day of the five displacement-proneness of the latter." day life-span. As an example of intrageneric A few recent observations and comments, natural food supply encourages a normal amount imaginal life. of flight by the butterflies. Other irregularities appear when, as Tin variation, the parasitic wasp genus (Opius) may however, suggest that displacement activities The success of the new design is attested by bergen (1952, p. 26) defines the conditions for be cited: males of certain species cannot mate may prove, after all, to be widespread among the fact that all of the six species (p. 135) of displacement activities, "a strongly activated for five days or more after emergence, although · higher arthropods. References to date appear heliconiids discussed in the present paper feed, drive is denied discharge through its own con in other species they do so early in the, imaginal to be confined to the following: salticid spiders court, mate and lay eggs. Many individuals re summatory act(s)." However, in the present period (Hagen, 1953). Finally, entomologists (Crane, 1949), mantids (idem, 1952), the but paper the term "irrelevant behavior" (suggested would probably agree that female insects that terfly Heliconius erato (idem, 1955), Drosophila main alive, barring accidents, for one to three and one-half months, although differences in by Rand, 1943) will be employed as a more have recently molted into the final instar are in (Bastock & Manning, 1955) and fiddler crabs, general term than "displacement behavior." The general more attractive to males than are older genus Vea (Gordon, 1955, and Crane, 1957). viability are shown. H. isabella is the most dif latter, it seems, may be usefully restricted to the individuals. It will be noted, however, that use ficult to maintain, and observations on this III. MATERIAL AND METHODS definition given by Bastock, Morris & Moynihan of the inexact term "recently" is necessary. species are still somewhat deficient. Two locally rare heliconiids, Philaetraea dido (Linnaeus) (1~5~, p. 25) :. "A displacement activity is an Rockstein (1956) discussed the unreality of The studies were all conducted in out-of-door activity belongmg to the executive motor pat a sharp boundary between the pupal and imag wire mesh insectaries in Trinidad (Crane & Flem and Heliconius wallacei Reakirt, have not been tern of an instinct other than the instincts inal stages in insects, citing recent reasearcb on ing, 1953; Crane, 1955) between 1954 and successfully maintained. They live a few days activated." biochemical changes occurring after emergence 1957. During the past two seasons a new in and feed, but do not "settle in" and spend most This distinction between terms seems desir in the .worker honeybee, house fly, Drosophila, sectary, designed as were the earlier ones by of their active periods batting against the roof. able since some of the butterfly actions under moths and the Japanese beetle. In Drosophila Henry Fleming, bas been in operation. Con Presumably a higher cage is needed. consideration do not at all appear to belong to there are concomitant increases in glycogen con structed entirely of aluminum, it measures 24 X Broods from all the species of heliconiids in the motor pattern of another instinct and hence tent and wing-beat frequency during the first 36 feet, the dimensions of the larger of the two cluded in this study were raised in the labora will be simply referred to as "irreleva~t actions." week of imaginal life. Although this frequency earlier structures, but it is higher than its prede tory. The young imagoes were kept in small Others, which fulfil the conditions of the more change is not directly related to social behavior, cessor, measuring 12 feet at the ridgepole. It cages out-of-doors until needed for observation restricted definition of displacement activities the phenomenon illustrates the kind of corre also has two doors with a small vestibule be or testing in the large insectary. General meth will be so designated here and treated as a sub: lation which may be brought to light in investi tween, forming a baffle which has proved very ods are given in an earlier paper (Crane, 1955). division of irrelevant actions. gations linking invertebrate physiology and be useful in preventing the escape of butterflies. A Table 1 gives an idea of the number of healthy 1:fY thanks go to the National Geographic havior. small pond and bog have been added near one imagoes that were used in the preparation of Society for a grant-in-aid, to Dr. William Beebe, Studies of irrelevant actions, including dis end; they form an efficient aid in maintaining this study. Substandard specimens, as well as Mr. Henry Fleming and Dr. D. W. Snow for placement behavior, in vertebrates are increas the necessary high humidity. those obesrved in the early seasons before tech helpful suggestions, and to Miss Barbara P. ing in number, following the pioneer work of The aluminum netting reflects far more heat niques were perfected and the present problems Young for rearing numerous larvae. Lorenz, Tinbergen, Makkink, Koorlandt and than does bronze mesh; it also diffuses the light formulated, are not included. Armstrong. General accounts and references are better, making it excellent for photography. II. HISTORICAL REVIEW given by Armstrong (1950), Lorenz (1950), Finally, species suitable for keeping in a cage IV. SURVEY OF SOCIAL BEHAVIOR IN SIX SPECIES The special aspects of social behavior under Tinbergen (1951, 1952), and Bastock, Morris of this size tend to bat against the netting less, OF TRINIDAD HELICONIIDAE consideration are little-known fields in the study & Moynihan ( 1953). Recent studies on particu even when they have just been released into it, The social behavior of all six of the Trinidad of invertebrates. lar species of birds and fish include those of than they did against the bronze netting of the species discussed below consists of three general The gradual development of behavior pat Hinde (1953), van Iersel (1953), Moynihan previous insectary. types-courtship, "social chasing" and roosting. terns in physiologically adult vertebrates has (1953) and Morris (1954)~ For this reason, as well as because of the in These have already been described in some de been extensively studied, and it is well known The probable occurrence of equivalent be sectary's relative coolness, heavy vines giving tail for H. erato (Crane, 1955). Except for minor that c~anges occur in response to physiological havior in invertebrates has apparently not been large areas of dense shade have been found to differences they are characteristics of the other alterations due both to increasing age and to suggested until recently. Armstrong (1950, pp. be not only unnecessary but undesirable. Instead, five species as well. Although these slight specific seasonal causes. 379 ff.) summarized the situation as it appeared the planting is kept to several well-separated differences are of great potential interest from a Corresponding information has been gath at the time of his writing as follows: "Probably major groups of shrubs, saplings and wild phylogenetic point of view, their detailed dis ered on ~ew invertebrates,. although the Hymen displacement activities are commoner in some bananas of varying degrees of height, density cussion belongs in subsequent papers on the optera mclude outstandmg exceptions. The other groups besides birds than is at present and leaf size. The rest of the space is occupied ethology of the genus. ? .~ .(/v.J11J!r-<:~· .U~~_,, •.I ?~ ,/.'·" 138 Zoo/ogica: New York Zoo/ gica/ Society [42: 12 1957] Crane: Imaginal Behavior in Butterflies of the Family Heliconiidae 139
TABLE l. NUMBERS 'op INDIVIDUALS UPON WHICH pe ding on the species, facing in the same TABLE III. APPROXIMATE AGES AFTER EMERGENCE In both sexes and all species, roosting accord PRESENT DATA ARB BASED · ection as the female. The latter, meanwhile, AT WHICH VARIOUS TYPES OF ACTIVITY OCCUR IN ing to the species habit begins on th~ second .or (From broods reared during the seasons of :fl tters her wings, also characteristically, elevates SIX SPECIES OF HELICONIIDS third night. Even in the most gregarious species 1954-1957, incl.). e abdomen and, in this stage or the next, ex l (erato, melpomene and sara), however, young t udes the subterminal scent glands. Activity Age females often hang up for the night alone, unless Species courting or mating has proceeded during the late Males Females Stage II. Secondary Fanning. The male fans afternoon. At such times the female, too, often he female from a different position from that in Flutters to ground when disturbed 1 hr. Dryas ju/ia 49 46 roosts with the group. Stage I, but still facing in the same direction as First flight when undisturbed 2 hrs. Heliconius melpomene 27 28 she. The female meanwhile extrudes the sub First feeding, rarely 6hrs. VI. IRRELEVANT ACTIONS Heliconius erato 71 terminal scent glands if she has not already done so. First feeding, usually 2nd day A. Males. Under certain conditions the court H eliconius ricini 38 Stage III. Alighting and Engaging. The male Earliest copulation, female 10-30 minutes ship pattern characteristic of the various species Heliconius isabel/a 21 alights beside the female, either just in front of Earliest copulation, male 3rd day of heliconiids becomes atypical. Instead of court Heliconius sara (1957 only) 16 or just behind her, moves back or forward ap Complete courtship pattern ship proceeding in the usual fashion to copula propriately and, as she closes her wings, curves elicited, female 2nd & 3rd days tion or, alternatively, to the point whe~e one partner stops responding and both go their sep his abdomen up between her posterior wings, en Complete courtship pattern 3rd day- A. COURTSHIP. Since the sim~'la· i . the gages her genitalia with his harpes, and swings elicited, male 2% months arate ways, t~alfL~~:m_!!~~:~- sl'.:ci~l-~~~pr behavior within the genus are far ater tna he around so that the two insects now face in op- that nevei: ends in.. copulat1on. On the very rare differences, a comparative chart (Table 2) f Latest copulation, unmated females 6th-8th day ~ occasions when mating soon ensues between the the patterns of fully developed co tshil'~W - Latest copulation, males (2 species) 2% months same partners following the first stages of this Discussed first in 1955, by{{ dicate'the trends to the extent needed for esent po:~~:~:ici::sING. First eggs laid 4th-12th day irregular behavior, the male has returned to an \ purposes. Crane, in erato, "soda! chasing" was the term early stage of courtship, and then followed the ' given to social flights that are not apparently di It typical sequence. will be seen from the table-that courtship rectly of a sexual nature. It was found to take Maximum ages reached, males and females (2 species) 31h months \ usually begins and always ends similarly in all similar form in the other five species. In all, Irrelevant actions never begin before the male \ species, while differentiation is shown principal it consists of the pursuit of males and old females has reached Stage II of the Sedentary Ph~se. ly in the first and second stages of the second, by males of any age, and of either sex by old In other words, he is in the final phase of fanmng sedentary phase. females. It will be discussed on pp. 141 and 142. emergence. In isabella, it is not even possible to above, in front of, or behind the alighted female, In brief summary, the sequence in its most see all the specific characteristics at one time. his position depe~ding on the pattern c1;1aracter complete form is as follows: C. RoosTING. Four of the six species roost During the female's first day, the wing :flutters istic of his species (Table 2). Sometimes the gregariously, namely H. erato, melpomene, ricini of the sedentary phase are very similar to those male has reached Stage III, having alighted be 1. Aerial Phase. and sara. All return to the same bush or vine, of erato and the aerial phase is, as usual, normal- side the female and tried unsuccessfully to attach Stage I. Nudging. A flying male approaches and often to the same twigs or tendrils, night . Iy non-existent; yet by the second day the special his harpes. a resting female from the rear. She then takes after night. Usually .the perch selected is dry. ized flutter is already disintegrating into the more One of two major types of irrelevant behav~or wing, usually without his actually touching her Although the four species tend to maintain sep generalized Dryas-type :flutter (see Table 2). In in any way. arate roosts, erato, melpomene and ricini often follows, depending on whether the female flies all the species after their third day the wing away and evades the male or whether she stays Stage II. Flight. The male chases and over roost together, as do ricini and sara. :flutterings of the females are diminished pro in place. takes the female, rises above and in front of her A trace of gregariousness is found in Dryas, gressively in intensity and characteristic form. In the first type, having lost track of the fe and fans her with the rapid vibration of his wings, which sometimes hangs up for the night near In males, copulation does not occur until the ·so spreading the products of his scent scales. She one or two others of its kind. H. isabella, how male the male flies about at unusual speed for third day ( 48 hours after emergence) and may up t~ five minutes at a time, without pausing, then descends or is forced down to a perch. ever, always roosts alone. The two latter species not take place until the fourth or fifth; these Chases sometimes include mutual circling and always hang from beneath green leaves. Roost feeding or making any apparent "searc~ing" later dates are apparently always characteristic motions (as he may do, on other occasions, spiralling in all the species. At these times the ing will be further considered on p. 139. of H. sara. No social activity by the males what circling by the female is apparently always among the vegetation). This type of behavi~r has ever is shown until the second day, 24 hours been artificially induced by the observer's simply merely the result of her temporarily successful V. CHANGES IN SOCIAL PATTERNS WITH AGE after emergence, when males sometimes nudge effort to duck out from under and behind the picking up the female and keeping her tem None of the social behavior patterns sum young females from the rear. After noon of the porarily out of sight. flying male and rise above and in front of him; second day slight chasing may occur, but this marized in the foregoing section is fully ex The second type of irrelevant behavior follows he in turn repeats the manoeuvre and the result behavior does not usually take place until the pressed when the insect emerges from the chrys when the female stays alighted and often appears ing vertical circling may continue for several third day. minutes. Horizontal spiralling is less frequent alid, and it now appears that the maturation to the observer to be making full courting re but seems to have a similar basis. In the pre time for the various responses is similar in all Unlike females, males court and can mate sponses. The first manifestation is always poor viously published account of erato (Crane, 1955) six species. Table 3 shows these periods. "Age" practically throughout life. In older males, al orientation in the fanning (Pl. I, Figs. 7-8). this flight stage, which is little developed in that indicates time after emergence from chrysalid. though complete and successful courtship is Normally in all the species the male faces in species and often omitted, was not separated It will be seen from the table that the full swiftly elicited by second-day females, relatively exactly the same direction as the female, al from Stage I of the Sedentary Phase below. pattern of courtship-including Stage II of the little attention is paid to older unmated or egg though the longitudinal axes of the two insects Aerial Phase and the specifically characteristic laying individuals. are usually more or less oblique to each other 2. Sedentary Phase. wing :flutters of the Sedentary Phase-is evinced Males chase each other freely throughout life, since the male fans characteristically from down Stage I. Primary Fanning. The male fans by females only on their second and third days, especially in the absence of young females, ex in-front to up-in-back. In disoriented fanning the the alighted female from the front or rear, de- that is, between 24 and about 56 hours after '• cept during their first two days. male may face in any direction, even backward 140 Zoologica: New York Zoological Society [42: 12 1957] Crane: lmaginal Behavior in Butterflies of the Family Heliconiidae 141 with respect to the female, and frequently close wave of the observer's hand. Under ordi she grows older her flight above him more and omitted, seem to depend predominantly on fe changes the direction without any regular se nary conditions such a gesture sends into the quence. 2 more resembles the swift, vigorous flight of the male scent, as do courtships in moths. All spe air even butterflies that are fully accustomed to fanning male, in which the fore- and hindwings cific differentiation shows in courting females After disoriented fanning has continued for moving human beings and insectary conditions. are well separated (whether or not the friction later in the first afternoon and, particularly, any period up to five minutes in length, there are Nine situations regularly elicit irrelevant be surfaces in the species concerned hold the scent a number of alternate sequels. on the second or third days. Beyond that age, havior in courting males. As previously stated, scales) . The male usually soon gives up and flies unmated females are receptive for at least three Most frequently the partners separate, either an advanced stage of courtship must have been away, without irrelevant behavior (seep. 139). to six days, although their characteristic actions the male or the female flying off, and neither one reached before irrelevant behavior begins. As the female grows older she chases passing decline in both intensity and specialization. thereafter evinces either excitement or special 1. Courting of an unmated female, four to behavior. butterflies with increasing frequency, regardless Courting of very young males by other males, eight hours after her emergence; that is, on the of their age or sex. Some chasing of other spe or of young individuals of other species, is un Ocaasionally the female takes wing and eludes afternoon of her first day. cies, either related or of similar size and color, doubtedly due to the strong family odor of re the male, whereupon the male flies about rapidly 2. Coillting of a young mated female. It is also occurs. This behavior continues even after cently emerged insects. It is interesting that this as described under the first type of irrelevant behavior. now certain that second matings in females are egg-laying has ceased and, at least in H. erato, odor apparently does not develop until the insect very rare, and are practically confined to indi is strongest in those females that have completely is at least ten minutes out of the chrysalid. Once 2ln the study of H. erato already published (Crane, viduals that have already reached egg-laying age finished egg-laying; in that species no eggs are a male H. sara actually copulated with a female 1955), Plate I, Figs. 5 and 6, are excellent examples of and are being persistently courted by young laid after the age of about six weeks, while the H. melpomene when the latter, aged about one disoriented fanning. A third example from the same ·I series is published as Plate I, Fig. 8, of the present con males in the absence of young unmated females. female's imaginal life often extends to more than hour, was still unable to fly. Usually these two tribution. At the time these photographs were made, 3. Courting of a mated female about to lay l three months. Only in the last two weeks of life species, which are strikingly different both .in '\ the existence of this type of irrelevant behavior had not eggs. does this energetic chasing decrease. color and, even to the human sense, in odor, been recognized. It is now clear that the sequence of have very little attraction for each other. still photographs in the earlier plate could not be taken, 4. Courting of a male on his first or second The following special behavior has been ob \ with present-day still camera apparatus, to illustrate a day. served only in females of H. sara. It occurs only It is unlikely that females, which spend the complete, normal consumated courtship between the on the two days preceding their first egg-laying first day practically inactive, are often found by same two individuals, photograp)ledJn sequence. This is 5. Courting of a very young imago of either because these courtships always proceed too swiftly to sex, belonging to another species. or, alternatively, when another female has al males during these early hours. Odor alone is permitlrecharging of the speedlamp between flash shots. 6. Loss of an unmated female,· during court ready laid on the only available space. (This not an adequate releaser. A male, after losing Only during the prolonged repetitions of irrelevant be ship, through her flying out of sight. species in Trinidad lays eggs in a cluster on the sight of a newly alightecl, young female that has havior can still photographs be made of a single pair terminal leaflets of Passifiora auriculata). On slipped underneath a leaf, sometimes searches during a consecutive period of courting behavior. A mo 7. Courting of females, unmated or mated, tion picture camera, operated at high speed, is of course these occasions sara uncoils the proboscis and around with every appearance of vagueness and suitable for the work. more than three days old by males more than with it touches either the spot on which she inefficiency, and only rarely locates her once about one month old. would normally lay, or the eggs already laid by again. Jn a common sequel to disoriented fanning, 8. Overcrowding of the insectary. This results another female. This procedure never occurs the male settles near the female. He may be in somewhat indiscriminate courting activity, B. SOCIAL CHASING AND RELATED TOPICS. It when she is actually ready to lay her own eggs, now seems clear that all the activities referred beside her, back of her or, most frequently, apparently clearly attributable to the operation or when no other eggs are already in place. facing her. He then extends the proboscis, some of the principle of heterogeneous summation to in the paper on H. erato (Crane, 1955) as times uncoiling and coiling it repeatedly and and resulting in the courting of unsuitable in "social chasing" are appetitive fragments of the VII. DISCUSSION with speed and force; when uncoiled it often dividuals. courtship pattern. They correspond to instances in numerous other animals where, as in frogs, a, touches or even palpates the female's head, 9. Unresponsiveness of unmated young fe A number of points which have emerged from male in response to an incomplete stimulus situa thorax, legs or, rarely, abdomen (Crane, 1955, males, or other failure in the final stages of the observations described in the preceding pages Pl. III, Figs. 13-14) .. tion embraces another male and, in the absence courtship, due to unknown causes. now require comment. ·. Sometimes the male palpates similarly with of appropriate response, releases his grip. B. Females. Equivalent irrelevant behavior of It is clear that, in this group of butterflies, his antennae. In these cases the proboscis is not It is possible that in the wild some species of females following broken-off courtships has not there can be no accurate description of court uncoiled. heliconiids maintain territories. All that can be been detected. However, later in life a female's ship or other social behavior that is based on a said now is that in this family no trace of terri Once only a male Dryas, after prolonged dis resistance to courtship appears to change in char few observations and individuals, any more than torial behavior, or of a dominance hierarchy, oriented fanning, settled obliquely to the side of acter to such an extent that it may be termed this is possible in the case of a higher vertebrate. has been observed either in the insectaries or the female, facing her,· and alternately brushed irrelevant behavior. The ages and past experience of each butterfly during field observations. There is no patrolling each of his own eyes with the palp of the cor observed, particularly females, must be known responding side. The motion was repeated sev A recrudescence of courtship of egg-laying of definite routes, no special display that lends females is usual in all species. Very rarely these in order properly to describe and evaluate their eral times and the performance was repeated an activities. itself to an interpretation of threat behavior, hour later. attempts end in copulation. The usual procedure no overt fighting, no individual that usually is is for the male to chase the female when she is Occasionally a period of proboscis extension A. AGE. As in many birds, the patterns of the pursuer in the frequent inter-male chases. beginning to hover around the foodplant, and to reproductive behavior are not closely linked with On the other hand all of the chases of one male or antenna! palpation will be followed by re try to force her to alight for tfie Sedentary Phase sumed disoriented fanning, and then a second successful reproduction. In the first place, the by another can be explained satisfactorily as in the usual fashion. At these times the female, full specific courtship pattern is unnecessary for merely the chasing phase of normal courtship period of the more extreme form of irrelevant flying with increasing strength as she is freed behavior. Sometimes the male persists in alter copulation. Before pairing with first-day females, which, because of the inadequacy of the sexual of the weight of eggs, usually manages to duck males omit all except Stage III of the Second situation, breaks down. The break usually occurs nate disoriented fanning and its sequels until he out from under the flying male and fly well above appears altogether exhausted and remains (Sedentary) Phase of courtship, and the young after more or less mutual circling, which exactly him. Then, instead of flying away as unrespon est females gives no overt responses at all. These resembles the circling resulting from the evasion perched motionless nearby. At these times he sive younger females do, she hovers, mounting cannot even be urged into flight by a sudden exceedingly simple courtships, in which prac attempts of unresponsive females (p. 138). higher as he in turn tries to come on top. As '· tically all appetitive behavior is almost always When two males are courting the same female,
'-•- .. BEEBE & KENEDY PLATE I 142 Zoologica: New York Zoological Society [42: 12
the latter often escapes in the general excitement observer witnesses irrelevant behavior of some and the two males 'continue for a short time kind than a specifically characteristic courtship. chasing and fanning each other. Even when, The various phases of irrelevant behavior and through the breakdown of the releaser sequence, the situations which produce it have proved to they "discover" the mistake there is no evidence be similar in all six species. In males, it is known of agonistic behavior; the two simply separate certainly to take place only following .an ad FIG.2 and go 1heir ways. Rarely one or both of the vanced stage of an incomplete courtship that males may continue rapid flight, apparently of is directed toward an unsuitable individual. It an irrelevant character (p. 139). occurs in females after their most receptive It seems likely that the phylogenetic origin of period (see preceding section). Experiments to f gregarious roosting was the continuation of determine whether irrelevant behavior takes .I social chasing until time to hang up for the place in hungry individuals that are prevented night. This could have become fixed, through from reaching visible and olfactorily detectable :j the action of natural selection, into the stereo food have so far been inconclusive. typed patterns of the species, as it came to have The instances of irrelevant behavior described protective value. Presumably the strong species are in completely different categories from "so odors, which laboratory tests show to be un cial chasing" since. they are in no sense merely I pleasant to predators, become intensified through unfinished portions of the regular reproductive crowding and could be a strong deterrent to or roosting patterns. Like "social chasing," how FIG, 4 nocturnal enemies that depend largely on the ever, they never end in copulation. I sense of smell. These enemies are probably Two of them, irrelevant proboscis-uncoiling chiefly reptiles and small mammals. and excessive, rapid, undirected flight, c~~ ~p The increase of chasing by older females is propriately be termed displace?1ent actlVIt~es. I of particular interest. This masculine type of Occurring when the strongly activated sex dnve activity would, in a vertebrate, be subject to a 1 is denied expression through its own consum I hormonal interpretation, in which the decline matory act, the motions are clearly associated 'i of female reproductive hormones leads to visible with other patterns of behavior, namely feeding effects of male hormone activity. However, in and flight. insects, morphological sexual characters, at least, The once-observed eye-rubbing with the palps I are not glandularly controlled; rather " ... the may be equivalent to the apparently displaced sex of every part is controlled directly by the cleaning motions described in mantids (Crane, FIG.5 FIG.6 chromosome constitution of the cells composing 1952), Drosophila (Bastock & Manning, 1955) FJG;7 it. Hence the sexual characters are unaffected by and ocypodid crabs (Crane, 1957). the removal of the ovary or the testes or even by their transplantation" (Ford, 1945, p. 192). The two remaining types of irrelevant be Schneirla (1953, pp. 677-678), after citing refer havior in courting male heliconiids cannot be ences concerning mating behavior in insects that further classified at present. They should not, it were castrated or otherwise sexually abnormal, seems, be termed displacement activities in the commented, "Such results suggest that factors restricted sense (p. 136) since they do not occur governing susceptibility ill male and female in in other behavior patterns found within the spe ! sects are not directly dependent upon testes or cies. These motions are disoriented fanning and ovaries, but may concern hormones already in palpation of the female with the antennae. It I the blood . . . the activity of some cephalic may be, of course, that this palpation with the endocrine secretion, or other physiological antennae, as well as with the proboscis, produces FIG.9 agencies such as neural processes." The present chemotactic sensations in a situation where the instance, therefore, of pseudo-masculine be usual olfactory stimuli from the female are likely havior in aged female butterflies, is one more to be weak or incomplete. In the European instance of the desirability of cooperative studies satyrid, Eumenis semele, movements of the an between physiologists and students of behavior. tennae form an integral part of courtship (Tin bergen et al., 1943). c. IRRELEVANT BEHAVIOR. Irrelevant behavior Disoriented fanning, in which the male may proves to play a large part in the apparently face in any direction with respect to the female, normal social life of all butterflies under obser appears to be a disintegration of the normal pat FIG. II FIG. 12 vation. It is not confined to species in captivity, tern, resulting from a breakdown in the usual since it has also been frequently observed in the sequence of male-female responses. Subsequent FIG. 13 wild. In fact, if only a few pairs of butterflies of ly the pattern often collapses altogether, the a given species are observed in the Sedentary remaining energy being channelled into displace HABITS, PALATABILITY AND MIMICRY IN THIRTEEN Phase in the field, it is far more likely that the ment-feeding or displacement-flight. CTENUCH!D MOTH SPECIES FROM TRINIDAD, B.W.I, ' -1 i t 1957] Crane: lmaginal Behavior in Butterflies of the Family Heliconiidae 143
. 1 In all irrelevant behavior appearing during mon form of activity. It apparently represents courtship, the non-responsiveness of the female, simply a fragment of the appetitive portion of for whatever reason, appears to be the major the courtship pattern. Neither territorial defense .\;. factor. Males that are not in a physiological con nor inter-male threat behavior seems to be in I dition to complete courtship simply break it off volved. at an early stage. Irrelevant actions of a number of kinds are As stated in earlier pages, it is now certain frequent. Most occur in males that are thwarted, that females normally mate only once. Each usually by the unresponsiveness of the female, develops a specifically characteristic odor, given after an advanced stage of courtship has been off by the abdominal glands, which becomes ap reached. Two kinds of irrelevant actions, a dis parent to the human observer about an hour or oriented type of wing-fanning and palpation more after the butterflies have separated. It is with the antennae, are not known in any normal the same odor given off by mated females when behavior pattern of the species. Other types of seized. It seems likely that it is one of the de irrelevant behavior appear to be true displace terrents leading to irrelevant behavior when ment activities, since they occur as appropriate males court mated females and do not follow actions in other fields of the insects' behavior, through to copulation even. though the females such as in feeding and flight. are making, to the human eye, all the visible responses characteristic of the species. Another deterrent in such cases seems to be the failure IX. REFERENCES of the female to fold the wings, which have been ARMSTRONG, E. A. more or less flattened during the _courtship flut 1950. The nature and function of displacement \ tering, above her back when the male alights activities. Symposia of the Society for Ex beside her in Stage III. It is impossible for him perimental Biology, No. 4. Physiological to reach her abdomen with his harpes so Jong mechanisms in animal behavior. Academic as her wings are flattened. Press, N. Y., 361-384. Use of the proboscis. by H. sara, when egg- BASTOCK, M., & A. MANNING · laying is apparently thwarted, is no part of the 1955. The courtship of Drosophila melanogaster. normal egg-laying procedure of any of the mem Behaviour, 8: 85-111. bers of the family that have been studied, and BAsTocK, M., D. MORRIS & M. MoYNlliAN perhaps should be termed displacement be 1953. Some comments on conflict and thwarting havior. Unlike members of some other families in animals. Behaviour, 6: 66-184. (Ilse, 1955 and refs.), none of the heliconiids drum the foodplant with their feet before laying. BEEBE, W. Finally, it may be re-emphasized that almost 1952. Introduction to the ecology of the Arima all these types of irrelevant behavior occur in the Valley, Trinidad, B.W.I., Zoologica, 37: lives of all individuals of the appropriate sexes 158-184. and ages that have been studied. No reliable BUCKINGHAM, E. interspecific differences have yet been observed. 1910. Division oflabor among ants. Proc. Amer. Acad. Arts & Sci., 46: 425-507. VIII. SUMMARY CRANE, J. Six species of heliconiid butterflies from Trini 1949. Comparative biology of salticid spiders dad, B.W.I., were reared in the laboratory and at Rancho Grande, Venezuela. Part IV. An their post-emergence behavior studied in insec analysis of display. Zoologica, 34: 159-214. taries. Their social behavior patterns are briefly 1952. A comparative study of innate defensive compared. behavior in Trinidad mantids (Orthoptera, Mantoidea). Zoologica, 37: 259-293. Social responses, including courtship, vary 1955. Imaginal behavior of a Trinida? butter~y, with age. In females the full courtship pattern Heliconius erato hydara Hew1tson, with is elicited only on the second and third days, special reference to the social use of color. although they can mate successfully when both Zoologica, 40: 167-196. younger and older. Younger females not only 1957. Basic patterns of display in fiddler crabs give little or no overt response but draw scarcely (Ocypodidae, Genus Uca). Zoologica, 42: any pre-copulatory behavior from males. Older 69-82. females show progressively fewer specifically CRANE, J., & H. FLEMING characteristic responses. ' Ji 1953. Construction and operation of butterfly Brief chasing of males or unreceptive females insectaries in the tropics. Zoologica, 38: by males of any age and by old females is a com- 161-172 .
. ·-) - - 1
144 Zoologica: New York Zoological Society [42: 12 1957) Crane: Imaginal Behavior in Butterflies of the Family Heliconiidae 145 FABRE, J, H. NIELSEN, E.T. 1879. Souvenirs· Entomologiques. Paris, Dela 1945. Moeurs des Bembex. Spolia Zoo!. Mus. grave. (Ed. def, illustree, 1914-1924. Vol.. Haun. Copenhagen 7: 1-174. 2). NIELSEN, A., & E.T. NIELSEN FORD, E. B. 1952. Migrations of the Pieride butterfly Ascia 1945. The New Naturalist: Butterflies. Collins, monuste L. in Florida. Ent. Meddel., London. xiv+ 368 pp. 26(5): 386-391. EXPLANATION OF THE PLATE GORDON, H. R. s. PARDI, I. 1947. Beobachtungen Uber das interindividuelle 1955. Displacement activities in fiddler crabs. Verhalten bei Polistes gallic11s (Unter PLATE I Nature, 176 (4447): 356-357. FIG. 6. Heliconius sara rhea. General color: suchungen Uber die Polistini no. 10). Be Black; forewing bands pale yellow; basal HAGEN, K. S, , haviour, 1(2): 138-172. Figs. 1-6, incl. Species and subspecies of butterflies half of hindwing with dark blue irides discussed in this contribution. Photograph by Sam cence. 1953. A premating period in certain ipecies of RAND, A. L. the genus Opius (Hymenoptera: Eurytom Dunton, New York Zoological Society. FIG. 7. Irrelevant courtship behavior in Dryas 1943. Some irrelevant behavior in birds. Auk, 1ulia: Sedentary phase, Stage II, showing idae). Proc. Hawaiian Ent. Soc., 15 ( 1): 60: 168-171. FIG. 1. Dryas julia julia. General color: Orange. 115-116. poor orientation in fanning. In normal RocKSTEIN, M. FIG. 2. Heliconius melpomene euryades. General fanning the flying male faces in exactly HINDE, R. A. 1956, Metamorphosis: a physiological interpre color: Black; forewing band scarlet. the same direction as the sedentary female 1953. The conflict between drives in the court tation. Science, 123: 534-536. (Table II and p. 138). Note that female FIG. 3. Heliconius erato hydara. Color as in H. has forewings almost closed as required in ship and copulation of the chaffinch. Be melpomene. haviour, 5: 1-31. RoscH, G. A. Stage III. However, the hindwings are still 1925. Untersuchungen Uber die arbeitsteilung FIG. 4. Heliconius ricini insulana. General color: fluttering, as is characteristic of earlier \ lERSEL, J. J. A. VAN im bienenstaat. I. Teil: Die Tatigkeiten Black; forewing bands pale yellow; central courtship stages, but atypical here. Photo 1953. An analysis of the parental behaviour of im normalen bienenstaate und ihre bezie \portion of hindwing scarlet. graph by M. Woodbridge Williams,® Na the male three-spined stickleback (Gas hungen zum alter der arbeitsbienen. tional Geographic Society. terosteus aculeatus L.). E. J. Brill, Leiden. Zeitschr. Vergleich. Physiol., 2: 571-631. FIG. 5. Heliconius isabella isabella. General color: FIG. 8. Irrelevant courting behavior in Heliconius 159 pp. Reddish • brown to yellowish - brown; erato, corresponding to stage shown in SCHNEIRLA, T. C. marked with black. Fig. 7. Photograph by Rosemary Kenedy. ILSE, D. 1953. Basic problems in the na~ure of in~ect be 1955. Behaviour of butterflies before oviposition. havior. (In: Insect Phys10logy, edited by Jour. Bombay Natural Hist. Soc., 53: K. D. Roeder; John Wiley & Sons, Inc., 486-488. New York, xiv+ 1100 pp.). pp. 656-684. STEINER, A. LORENZ, K. z. 1932. Die arbeitsteilung der feldwespe Polistes 1950. The comparative method in studying in dubia K. Zeitschr. Vergleich. Physiol., 17: nate behaviour patterns. Symposia of the 101-152. Society for Experimental Biology, No. 4. Physiological mechanisms in animal be TINBERGEN, N. haviour. Academic Press, N. Y., 221-268, 1951. The study of instinct. Oxford, Clarendon Press, 228 .PP· MAYR, E. 1952. "Derived" activities; their causation, bio 1942. Systematics and the origin of species, logical significance, origin, and emancipa Columbia University Press, N. Y., viii+ tion during evolution. Quart. Rev. Biol., 334 pp. 27: 1-32. MORRIS, D. TINBERGEN, N., B. J. D. MEEUSE, K. K. BoEREME 1954. The reproductive behaviour of the zebra & W.W. VARIOSSEAU finch (Peophila g11ttata), with special ref 1943. Die balz des sampfalters, E11me11ia erence to pseudofemale behaviour and (Satyrus) semele (L.). Zeitschr. Tierpsy displacement activities. Behaviour, 6: chol., 5: 182-226. 271-322. VERLAINE, L. MoYNIBAN, M. 1932. L'instinct et !'intelligence chez les Hy 1953. Some displacement activities of the black menopteres. Bull. Soc. Roy. Sci. Liege, 2: headed gull. Behaviour, 5: 58-80. 248-253.
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I
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