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6 THE WILSON BULLETIN (^) Vol. 60, No. 1March 1948
SOCIAL RELEASERS AND THE EXPERIMENTAL
METHOD REQUIRED FOR THEIR STUDY’
BY N. TINBERGEN
PART 1: REVIEW
S
OME years ago, Dr. Rand ( 1941, 1942) published two short papers in which he criticized some of the hypotheses and conclusions of Lorenz (1935 and 1937)) especially the releaser concept. Discussing my paper (1939b) on vertebrate social organization, Dr. Rand (1942:404) goes as far as to argue that “the data available hardly justify” me in assuming even as a lerorking hypothesis a social, communicative function for conspicuous and highly specialized structures whose participation in non-social processescannot be found. Though I am in complete agree- ment with Dr. Rand when he stressesthe need for further experimental research on the function of conspicuous structures and movements, I cannot agree with his statement that “the probable existence of releasers has not been clearly demonstrated in any cases” (Rand, 1941: 289). This astonishing statement can be explained only by assuming that a number of experimental facts published in American and European journals have escaped Dr. Rand’s attention. In order to make these facts better known, it seemsworth while to give, as the first part of this paper, a short review of the experimental and other evidence on releasers. In addition, the experiments reported by Rand in his 1942 paper, which tend to show that the anal feather circlet in nestling passerine birds does not function as a releaser, are not, in my opinion, conclusive (though I admit that they are useful as a warning against over-simplistic views). Therefore, in the second part of this paper, I shall discusssome general problems connected with the kind of experiments required in work of this type. The releaser concept has sometimes been misunderstood even though Lorenz has given a clear definition of it. Rand (1941: 289) is confusing matters considerably when he assumes that a releaser in Lorenz’s sense is “that portion of the object which sends out the stimuli to which the bird responds.” The^ cause of this misunderstanding lies in^ the para- doxical fact that not everything that releases a response is a “releaser” in Lorenz’s sense. A number of experimental studies on the nature of the external sensory stimuli necessary to release innate responses have shown that innate behavior is never a reaction to the environmental situation as a whole, but only to a few parts of it. Other parts-although they may be received by the animal’s sense organs-are entirely ignored. This is not
‘Extension of an address delivered at the Annual Meeting of the Wilson Omitholog- ical Club, Omaha, Nebraska, November 29, 1946.
SOCIAL RELEASERS 7
the place to give a complete review of the pertinent facts, and I must refer the reader to the literature, especially to Lorenz ( 1940), to Russell’s compilation (1943)) and to my own paper (1942). To cite a few examples: The escape reactions of many birds from passing birds of prey are a response to a type of movement and to a special characteristic of shape, namely, “short neck” (Figure 1) ; any
Figure 1. Cardboard models used by Lorenz and Tinbergen to test the reactionsof birds to birds of prey. Only the models with a short neck (marked +) released escapereactions.
bird, or even a cardboard dummy, that has a short neck releases an escape response independently of the shape of wings, tail, etc., and of the color (Goethe, 1937b; Krtitzig, 1940; Lorenz, 1940). The hunting response of a pike can be released by a shining silvery object pulled through the water. Gulls and many other ground-breeding birds will show incubation responses to many objects other than eggs, provided they have rounded shapes (Kirkman, 193 7; Lorenz and Tinbergen, 1938 ; N. Tinbergen and Booy, 193 7) ; size or color can be varied within very wide limits. Russell (1943) called these influential stimuli (the parts of the environmental situation to which innate behavior patterns respond) “perceptual signs” or “perceptual clues,” but for various rea- sons I prefer the term “sign stimuli.” It should be emphasized that it is only innate behavior that is de- pendent on sign stimuli; as I will show below, many if not all con- ditioned reactions are dependent on quite another type of stimulus situa- tion. So far as we know at present, every unconditioned reaction of an animal is dependent on its own special sign stimuli, and different re- actions respond to different sign stimuli. This shows that the release of every unconditioned reaction is dependent on a special central nervous mechanism, which is called the “innate releasing mechanism.” Lorenz (1935) put forward the theory, based on an unrivaled amount of observational facts, that in animals intraspecific social rela- tions are dependent to a large extent on stimuli sent out by one indi- vidual (the ‘Lactor”) releasing responses in another individual (the “reactor”). As a result of evolutionary adaptation, many species have developed special structures or movements that serve to send out stimuli especially adapted to act on innate releasing mechanisms of
N. Tinbergen SOCIAL^ RELEASERS^9
The three-spined stickleback. This stickleback (Gasterosteus acu- leatus) displays visual releasers of movement, form, and color. Ex- periments on the function of these releasers have been published by Ter Pelkwijk and Tinbergen (1937) and by N. Tinbergen (1939b, 1940, 1942). The male stickleback isolates himself in spring, develops a nup- tial dress of whitish-blue on the back and brilliant red on throat and belly, selects a territory which it defends against other males, builds a kind of nest, and entices a female to enter the nest and spawn. The red belly acts as a releaser both to other males and to fe- males. To a male any fish with a red belly is a rival, that is to say, it elicits flight in a male that is outside its own territory and evokes attack in any male that is on its own territory. This is demon- strated by a series of experiments of which the crucial ones may be summarized here. Two series of models of sticklebacks were prepared, each con- taining dead sticklebacks and more or less schematic models. The models of series ‘<R” were red on the ventral side; those of series “N” were the neutral color of a male in the non-breeding season and of females throughout the year (silver, with a dark greenish-black dorsal shading).
Figure 2. Two modelsof the R series(left) and a model of the N series(right) for testing the releasingpower of the stickleback’sred belly. After N. Tinbergen, 1947.
Experiment 1 consisted of bringing a model into an occupied terri- tory for a fixed period. This was done in over 20 territories, and the models were presented in irregular order with due intervals be- tween. Models with a red belly were attacked much more intensely than neutral models. In Experiment 2 a model was placed in a territory from which the owner had been removed, and the behavior of the neighboring male stickleback in the same tank was watched. A neighbor-male always tries to intrude in a territory as soon as the owner is removed. All R models could appreciably retard the intrusion whereas N models had scarcely any influence.
10 THE WILSON BULLETIN Vol.March 60,^ No.^1948
The females’ reactionswere tested by trying to induce them to
follow a model. In this we succeededonly when playing the models
of Series R; no reaction, except occasionalavoidance,was obtained
with SeriesN.
A glanceat the R and h models (Figure 2) sufficesto showthat
the exact form has little influence,if any at all; modelsof most real-
istic form but devoid of red (Series N) had little or no releasive
value.
In boundary disputes,a male stickleback often showsa special
threateningmovement: standingnearly vertically with his head point-
ing downward,his broad side turned to the rival and (often) the ven-
tral spine on that side erected, he thrusts his snout into the bottom
with abrupt jerks (Figure 3)) a movementthat can easily be imitated
Figure 3. Male stickleback threatening reflection in mirror. Note the unilateral display of the ventral spine. Photo by N. Tinbergen.
with a model. In a group of tests with modelsfrom both the R and
the N series, each model was presentedalternately in threatening
posture and in normal swimmingposition, both in the situation of
Experiment 1 and in that of Experiment 2 describedabove. A “threat-
ening” model, whether from the N or from the R series,had more
influence than a model in horizontal position. Also, a male taken
from his territory was returned as a captive in a glasstube before the
neighborhad trespassed.The neighborwas much more intimidated
when the owner was presentedin a wide tube that allowed him to
perform the threat motion than when he was confinedin a narrow
tube that forcedhim to stay in the neutral, horizontalposition (Figure
4 A).
12 THE WILSON BULLETIN (^) Vol.March 60.^ No.^1948
in releasing the male’s fighting behavior, but for courting or leading, the swollen abdomen of the pregnant female has a strong releasing power-as demonstrated by comparing the influence of neutral models with that of “pregnant” models. It has even been possible to change live males into ‘Lpregnant” animals by excessive feeding, which caused the abdomen to swell to such an extent that not only the human observer but also the courting male sticklebacks mistook them for females. The relative unimportance of other particulars of form was also shown by comparing the influence of a dead stickleback (Figure 5 B) having a neutral abdomen with a highly simplified model having a swollen abdomen (Figure 5 C). Males invariably courted the ‘(pregnant” dummy, while the dead stickleback affected them little. The releasing mechanisms of these reactions are all innate. A male that was reared in isolation and built a nest was tested with models before it had ever seen another stickleback. The red belly, the threatening posture of a “male,” the upright posture of a “female,” and a “female’s” swollen abdomen had the same releaser functions as in the experiments with normal males. All these results exactly fit the original releaser theory as out- lined by Lorenz.
The English Robin. Lack’s results (1943) with the English Robin (E&hams rubecula) show surprising parallels with our stickleback work. The red breast evokes furious attacks in any robin holding territory. It is by far the most effective of all the morphological characteristics of the bird. A mere bundle of red breast feathers is
Figure 6. Tuft of red feathers (left) and complete mounted young robin (right). After Lack, 1943.
attacked, whereas a complete mounted young robin, having a spotted brown breast instead of a red one, is ignored (Figure 6). The red breast is a releaser just as the stickleback’s red belly is, although the function of the releaser is not the same in the two cases, since, in the robin, both male and female have a red breast.
N. Tinbergen SOCIAL^ RELEASERS
The Flicker. Noble (1936) studied the releasing value of the “moustache” of the male Flicker (Colaptes auratus). Male and female of a pair in his garden readily distinguished between a mounted male and a mounted female, which shows that morphological characters, though perhaps not necessarily the only means of recognition, were sufficient. When the female of the pair was given an artificial “moust- ache” by gluing black feathers on the area which the moustache oc- cupies in the male, the female was vigorously attacked by her own mate. After removal of the moustache she was accepted again. It would be worth while to repeat and extend this experiment, but from Noble’s descriptions of the male’s behavior it seems certain that the moustache has an enormous influence on the male. It is not certain whether the male’s response to the moustache is innate or learned. Noble thinks it is learned, but it is not clear on what evidence he bases this opinion.
The Shell Parakeet. The experiments of Cinat-Tomson (1926) with Shell Parakeets (Melopsittacus undulatus) are especially con- vincing. The color of the cere (Figure 7), brown in females and blue
Figure 7. Shell Parakeet. Arrow indicates cue, which is blue in males, brown in females. After N. Tinbergen, 1947.
in males, acts as a releaser. Females with cere painted blue are attacked by the males, males with cere painted brown are courted. It is not known whether these reactions are innate. The color of the cere is used as a recognition mark only in judging strangers- a bird recognizes its own mate, in spite of an artificial color change, as soon as it hears the mate’s voice.
The Iierring Gull. The red patch on the lower mandible of the Herring Gull (Layus argentatus) seems to be a releaser during feeding. Goethe (1937a) presented two stuffed Herring Gull heads to new- born chicks, two of which had been taken from the nest shortly after hatching, while two others were incubator-hatched. One of the gull heads had a bill in natural colors; in the other the red patch was painted yellow of the same shade as the rest of the bill.
SOCIAL RELEASERS
stimulus situation is very simple, for the male fights against rather crude dummies provided that they are (1) laterally compressed, offer- ing a large surface to the male, (2) glossy silver or blue, and (3) spotted with “jewels.” (^) Seitz also tested a male reared in isolation; its fighting response was evoked by exactly the same external situa- tion as that of normal males, showing that the releasing mechanism of the fighting response is innate. On the other hand, the isolated male’s courting response could also be evoked by very simple models, such as a silvery ball, whereas the normal males never courted any model at all, however accurate an imitation of the living female it might be. This proves that the releasing mechanism of the courting behavior is changed by conditioning. The female has no structures or movements that could be classified a priori as releasers. The splen- did nuptial dress of the male, however, appeaks to be adapted to an innate releasing mechanism and acts as a releaser, a fact which could be predicted from the releaser theory. In Hemichromus bimaculatus, the African jewel fish, male and female are not very different; both have a red nuptial dress and are spotted with “jewels.” Seitz (1942) and Noble and Curtis (1939) showed that the red color is an important recognition mark to which both males and females respond, when in mating condition, by fighting and courting. Seitz tested the male’s releasing mechanisms of fighting and courting; in both, special movements make sex-discrimination possible; a male will erect and display its fins, a female, after an initial display, has to “break down” and show a submissive attitude in order to be accepted as a female. The^ releasers on which sex-dis- crimination is founded, therefore, are not special morphological structures, but rather specialized movements, as could be expected in view of the similar (though not absolutely identical) coloration of the sexes. A further development of this sex-discrimination mecha- nism occurs during individual life: the fish learn to know their own mates individually; in other words, the releasing mechanism is made more specific by conditioning (Noble and Curtis, 1939).
The cuttlefish. The most striking demonstration of how far con- vergencies can go in these phenomena, is given by L. Tinbergen (1939) in his study of the mating behavior of the cuttlefish Sepia oficinalis. Parallel with the development of eyes in cephalopods (con- vergent to those of fish) the courtship of the cuttlefish has evolved into a typically visual one closely resembling the courtship of certain sexually dimorphic fish, lizards, and birds. A male Sepia in mating condition assumes a strongly variegated pattern of alternating white and dark purple bars, and displays the most conspicuous part, the broad, flattened lateral surface of the fourth arm, toward other individuals (Figure 8). Reactions of males
16 THE WILSON BULLETIN (^) Vol.March 60.^ No.^1948
and females to this display differ essentially: a male returns the dis- play, a female in mating condition keeps quiet and allows the male to copulate. A series of varied experiments with models showed that the male’s nuptial colors, and especially the color and display
Figure 8. Male cuttlefish in neutral dress (upper) and in display (lower). After L. Tinbergen, 1939.
of the arm, released fighting in other males. The experiments did not determine whether the male’s display acted on the female as a releaser. The males treated all models colored and “behaving” like females as if they were females. This state of affairs closely resembles that found by Noble and Bradley (1933) in Sceluporus. In both species the male’s display is primarily a means of threatening other males; in both species the stimulating influence on the female is apparently small. The male’s nuptial dress is primarily a “gladiator’s vestment” (Noble, 1934). This review of experimental work, short as it is, shows that the releaser theory is not an “ideology” that has to be “accepted blindly” as Dr. Rand thinks. It is true that more experimental work is needed (though not to prove that releasers do occur, since that is clear). A further study of releasers will almost certainly give us an under- standing of such diverse problems as the sociological structure of ani- mal communities, the innate releasing mechanism, and last, thougb not least, the evolution of behavioral elements.
NON-VISUAL RELEASERS
Auditory releasers. There is good experimental proof of the re- leasing function of the chirping of crickets and grasshoppers. The
18 THE^ WILSON^ BULLETIN^ Vol.60,No.lMarch^19181
special releasers may be found whose exclusive function is to act on the chemo-receptors of congeners. Several of these cases have been studied. Von Frisch’s classic work on the L’language” of hive bees has shown that pioneer workers after discovering a new source of nectar perform a “dance” in the hive which stimulates a number of other bees. These react by leaving the hive and extensively searching the vicinity, eventually gathering on the species of plant that had been discovered by the pioneer. Experiments prove that the bees are at- tracted to the flower by its odor which was carried in the “fur” of the pioneer that had visited the flower before “dancing” in the hive. When flowers without a distinct odor are concerned, the bees that have been “given the cue” by the pioneer do not alight at once on the flowers when they find them but first perform a long ceremonial flight amongst the flowers while protruding their scent organs, which are located in the abdomen. This ceremony marks the exact spot with a typical scent which attracts other bees. (von Frisch, 1923; see also 1946.) The male of the grayling butterfly (Eumenis semele) has a scent organ on the dorsal surface of the forewing (Figure 9). This is used during an elaborate courtship display, which reaches its climax in the male’s characteristic bowing performance in front of the female, when her antennae, which bear chemo-receptors, are caught between the male’s wings and are thus brought into contact with the scent organs (Figure 10). These act as the releaser necessary to secure the female’s cooperation in coition. Males in which the scent organs have been removed have great difficulty in acquiring a mate in spite of intensive courting (Tinbergen, Meeuse, Boerema, and Varossieau, 1942). In other animals, scent may be used, in much the same way as song and visual releasers are, as a means to advertise occupation of a territory. This was first discovered in the domestic dog, which erects “scent flags” on prominent places in its territory (von Uexkiill and Sarris, 193 1). Holzapfel (1939) discovered that the hyena (Hyaena) had a comparable habit, and recently Hediger (1944) listed a whole series of similar phenomena in a number of mammals.
Tactile releasers. Even tactile stimuli may serve as specialized re- leasers-for example, human courtship and human mother-infant rela- tions are partly based on them. The mating of the snail H&x pomatia offers another example. As Szymanski (1913) showed, the characteristic movements and postures of each of the partners are reactions to tactile stimulation by the other. The “courtship” GUI- minates in the thrusting out of the “dart” (Figure 11)) the only func- tion of which is the delivery of a powerful stimulus; the dart is a true releaser.
N. Tinbergen SOCIAL^ RELEASERS^19
Figure 9. The grayling butterfly. Upper: dorsal side; lower: ventral side. Black line in upper left figure indicates position of scent organ on left wing. After N. Tinbergen, Meeuse, Boerema,and Varossieau,1942.
Figure 10. Grayling butterfly male (right) bowing before female, so that the female’s antennae come in contact with the scent organ of the male. After N. Tin- bergen, Meeuse, Boerema, and Varossieau, 1942.
N. Tinbergen SOCIAL^ RELEASERS
innate releasing mechanisms are fitted together; they act as a won- derful, complicated system the only function of which is the con- struction of a means of social communication. In fact, such compli- cated structures are understandable-they “make sense”-only in con- nection with their function; the coincident presence in the same species of stridulation organs, the stridulating drive, and an innate tendency to react in certain “purposive” ways can be recognized as an adaptive feature only when the releaser function is recognized. Hence, it is quite justifiable to conduct experimental work on the basis of the releaser hypothesis even when only parts of the whole mechanism are known, that is, for example, when only the effector organ (e.g., a conspicuous structure) is found, with a movement dis- playing this effector. It is true, as Dr. Rand remarks, that one has to reckon with the possibility of “maladaptation.” However (apart from the question whether it is satisfactory to consider without proof a highly specialized structure such as the syrinx of song birds or the wing of an Argus Pheasant as a functionless error of evolution), there is a difference between a critical attitude and a defeatist attitude. Any hypothesis aiming at “finding the use” has to be seriously tested before it is abandoned in favor of a purely negative hypothesis. These considera- tions justify the following enumeration of cases in which only part of the mechanism has been investigated and the releaser function of the whole has not yet been experimentally tested. Since it is especially the existence of visual releasers that is doubted, I will confine myself to supposed visual releasers. The argument applied is: when we again and again observe that a conspicuous, highly “improbable” structure is used as an instrument by an equally conspicuous and “improbable” movement resulting in a display of this structure, we suppose that both structure and movement form part of an adaptive mechanism that has the function of display. I will take the risk of being accused of “following ideologies blindly” and cite as significant the conclusion reached by Hkinroth, who worked along these general lines and must in fact be considered one of the founders of modern ethology. This great observer, whose disinclination to formulate general conclusions is well known,3 said, as early as 1900, that conspicuous structures in birds are always used in display. Huxley (1914:523) wrote: “The same instinctively dis- played parts-wings and tail, throat and crown-are the parts which are especially singled out for the development, first of special colours,
‘Typical of Heinroth’s attitude is the following anecdote, related to me by o~ne of his intimate friends. Heinroth once delivered an address full of interesting facts ar- ranged in such a way as to suggest a special and important conclusion. He did not, however, formulate this conclusion himself, but concluded his speech with: “Na, meine Herren, den Reim dazu kiinnen Sie Sich selbst machen.”
22 THE WILSON BULLETIN (^) Vol.March 60,^ No.^1948
... then of special colours and structures combined.” This sentence, while evolutionary in sense, is based upon descriptive evidence re- vealing the same general rule as that pointed out by Heinroth. The following facts serve to substantiate this general rule. Of widespread occurrence is the type of display in which the body as a whole is laterally flattened and enlarged and made as high as possible, often with the help of erectile structures such as fins and feather fans. Correlated with this lateral flattening is an orientation toward the reactor which offers the most imposing view of the body as a whole. Further, the coloration of the body is localized in such a way as to be most conspicuous during the lateral display. Often the color pattern covers both body and extensions, such as fins. This is especially obvious in many fish, where, for instance, black bars or fields of ‘Ljewels” extend over the dorsal and anal fins. I often won- dered in such cases which part of the coloration would be the re-
Figure 12. TiZa$Cunatalensis male. In asexual (left) and sexual (right) coloration. After N. Tinbergen, 1947.
leaser until I realized that such a fish must be considered as one huge releaser. One could say: such fish “have” no releasers; they ‘lare” releasers (Figure 12). In fish, the stickleback is only one of the less prominent performers of lateral display. Bet& (fighting fish), sunfish (Centrarchidae), cich- lids, and many others offer extreme examples (Figures 13 and 14). In Aequidens latifrons, for instance, the dorsal, caudal, and anal fins, when erected, nearly double the visible surface. The caudal, anal, and hind part of the dorsal fins are also locomotory organs, but the forepart of the dorsal fin has no locomotor function and seems to have been adapted entirely to display purposes.
Figure 13. Aequidens Zatifrons male. In posture of inferiority (left) and in threat posture (right).
24 THE WILSON BULLETIN (^) Vol. 60, No. 1March 1948
Figure 16. Anolis carolinememale. Dewlap display. After Evans, 1938.
Among birds, the lateral display is very common. Numerous in- stances are found in the Phasianidae, e.g., in the Golden Pheasant, Chrysotophus p&us (Figure 17), Amherst’s Pheasant, C. amherstiae, Bulwer’s Pheasant, Lobiophasis bulweri, the domestic fowl, and the turkey. But it is also observed, to a lesser degree, in other birds.
Figure 17. Golden Pheasant. Lateral display of male (left) before female. After Hagenbeckin Heilborn, 1930.
N. Tinbergen SOCIAL^ RELEASERS^25
I have seen it in the European Jay, Garra&s glandarius, though this species has no feather fans especially developed for the purpose, and it is quite astonishing to see it render itself as flat as a knife. Apart from the general pattern of lateral display, there are numer- ous instances of directed display of special parts of the body, some of which show a remarkable and grotesque correlation of movement with structure. Both the African jewel fish (Hemichromis bimacula- tus) and the South American Cichlasoma meeki have a morpholog- ical releaser on the gill-cover, consisting of a black patch bordered by a yellowish or greenish golden ring. This structure is used during a frontal threat display which consists, as in so many fish, of erecting the gill-covers. Now in meeki the black patch is situated at the ven- trocaudal edge of the gill-cover, in bimaculatus at the dorsocaudal edge. In conformity with this, meeki spreads especially the ventral part of the gill-cover (Figure 18, right), while bimaculatus displays its releaser by spreading especially the dorsal part of the gill-cover (Figure 18, left). Both movements are rather specialized forms of gill-cover display.
Figure 18. Henzichromus bimacdatus (left) and Cichlasoma meeki (right). Frontal display. After N. Tinbergen, 1947.
In birds, so many instances of visual reIeasers are known (see 0. and M. Heinroth, 1928; Stresemann, 1927-34; Armstrong, 1942) that I will confine myself to a few rather unconventional types. The male Snow Bunting, Plectrophenan: nivalis, displays the variegated black and white pattern of the dorsal surface (Figure 19A) and in doing so walks slowly away from the female (N. Tinbergen, 1939a). The threat movement of the Common Crane, Grus gyus, consists of dis- playing the occiput, where a red wattle appears (Heinroth, 1928). A male Lapwing, Vanellus vanellus, when trying to attract a female to one of his scrapes, displays his under tail coverts, which are a warm chestnut-brown (Figure 19B). When the female moves, the male promptly turns his tail, presenting a full view (Rinkel, 1940). A Flicker, Colaptes auratus, also displays its under tail coverts in threat but uses quite a different method: it tilts the tail sideways and for-
