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Ethologic implications of the skin and its disturbances
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Ethologic Implications of the Skin and its Disturbances
Patrizia Messeri, Ph.D., and William Montagna, Ph.D.
From the Department of Zoology, University of Florence, Florence, Italy, and the Department of Dermatology, Oregon Health Sciences University, Portland, Oregon
From the beginning of its simplest forms, animal life appears to be organized according to specialization by inner functions and surface functions. The passage from prokaryotic to eukaryotic cells, from bacteria to unicellular organisms, consists essentially of a functional specialization of surfaces, accompanied by an extraordinary development of plasma membrane from which originate membranous surfaces that have become specialized into endoplasmic reticulum and nuclear envelope, transferred inside the cell. Whereas the inner functions of cells are prevalently synthetic or transformational, the surface functions are concerned with chemical, physical, or informational exchanges with the environment. With the progressive increase in complexity that accompanies the passage from unicellular to multicellular conditions and the formation of systems of organs, the functions of chemical exchange are performed by surface elements which progressively move inside the body and become specialized(lungs, intestines, kidneys), whereas the outer surface conserves the function of relations with both the physical and the living environment. The function of the outer surface is mainly a protective one. Among the functional protection from the physical environment are the control of osmotic equilibrium, protection from attrition, and the maintenance of body temperature. To perform these many functions in many different environments, the integumentary system presents a wide range of variations both in the skin and in its appendages (cuticles, scales, hair, feathers, beaks, nails and claws, and many others). Equally important functions of the integuments are those connected with relations between organisms and the living environment. The skin and its appendages are the principal signal transmitters for olfactory, visual, and tactile communications. Regarding tactile communication, moreover, the skin also functions as a receptor organ. Olfactory Communication Although it is the channel of communication most largely used in the animal world and the most primitive of all forms of animal communication, olfactory communication is the least known, largely 27
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because our own sense of smell is poorly developed. Animals live in a world full of sensory stimulations, and therefore, in order to be effective, a signal must be prominent by being endowed with peculiar characteristics. Visual and auditory signals usually achieve this aim by virtue of characteristic spatial or temporal patterns, but olfactory signals are particularly persistent and once emitted cannot be easily modified. Consequently, olfactory communication has limitations: first, it supplies a limited range of information (yes-no type); second, it is highly selective and, in some cases, a receptor appears to react only to one specific substance. The prolonged spatiotemporal persistenceof an odor also has advantages: chemical signals can act over a long distance and in many directions simultaneously and thus are the most important signals for specific recognition and for sexual encounters. Smell seems to be the best sense for long distance attraction; the males of certain species of moths can detect the presence of a female many kilometers away. Furthermore, these chemical signals are highly selective and elude individuals of other species and potential predators. Mammals were originally small, shy animals. It would be disadvantageous for them to emit signals that could make them easy prey to such predators as birds with excellent sight and limited, but highly discriminate hearing. This situation favored the development of an olfactory system useful for social encounters and for reproduction. Consequently, most of the 4,500-odd species of mammals have an acute sense of smell. Odors are used for territorial markings, group status and rank recognition, maternal behavior, and the detection of food and predators. Territorial behavior insures the animal of vital space and spatial distribution appropriate to environmental resources; a territory may be defended, marked, or both. Mammals delineate territory principally by scent marking: at special points in the territory, animals deposit gland secretions and/or
Clinics in Dermatology
urine or excrement. These scent marks are primary indicators for the owners, to help the animals orient themselves and feel “at home”; they probably also serve as repellents to outsiders. Marking methods vary from species to species: hamsters mark their den and salient surrounding objects by rubbing against them and depositing the secretion of their sebaceous flank glands; badgers use the secretion of their anal glands (in a sack at the base of the tail); and galagos urinate on their hands and rub the urine on their soles, to leave a scented trace when they climb trees. There are generally specific scent glands for marking, located in different parts of the body of different species. The development and use of these glandsdepend on the animal’s sex and rank; the largest and most active glands are found in high-ranking males, in which they are controlled by adrenal and gonadal hormones. In many species the scent marking is used for conspecific animals; for example, male rabbits “mark” their females by rubbing their submandibular gland secretions on them. Similarly, cats rub their cheeks against objects, humans, and other cats. The marking of conspecific individuals in social species, and in particular insects and mammals, establishes a group or family odor scent.’ Odor is particularly important at the time of birth. Mice made anosmic have no maternal behavior; and in sheep and goats, the mother-baby bond is influenced by the mother’s capacity to smell the odor of the baby during a brief critical period after the birth. These odors can also have lasting effects. Newborn mice kept in a nest artificially scented with a certain odor show a perference, when reaching sexual maturity, for partners scented with the same odor.2 Notwithstanding its many secondary functions in mammals, olfaction has a fundamental importance in species identification and sexual behavior. It is generally held that it is the males who perceive the odor of the females, particularly when the females are in estrus; these substances, called pheromones, are controlled by hormones. It has
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been shown that a male macaque can be trained to press a bar to gain access to a female in estrus, or to an ovariectomized female treated with estrogens. When the male was made anosmic, it ceased to press the bar. Female mammals also respond to the odor of males: cats and sows in estrus assume the coital position when exposed to the odors of a male cat or pig.3 It may seem strange that human beings agree that the sense they are least willing to do without is smell, while at the same time they expend so much effort in hiding their odor(s) with deodorants and perfumes. One possible explanation is that human beings are an exception among mammals; another is that our sensitivity to odors, because of its primitive character, is mostly unconscious.4 Young volunteers tested to see if they could recognize (by smell) clothing belonging to their sexual partners demonstrated that they could choose the correct article of clothing in a percentage of cases significantly higher than chance, although they were not able to explain why they chose as they did. Moreover, the perception and the production of odorous secretions elude conscious control, as is demonstrated by galvanic skin response (and as those affected with bromhidrosis know). Mammals use practically all their excretory organs to produce odors. One of the least specialized odors is that of urine. The sebaceous glands are, by far, the most active of all the cutaneous organs and the main source of odor, even in man. Apocrine glands in human beings are associated with body hairs, primarily in the armpits, sometimes the breasts, the genital and anal regions, the external auditory canal, the eyelids, and the lips. The surface of hairs increases the surface area for diffusion of secretions, and potentiate diffusion in the air. We do not perceive these secretions; the odors we perceive best, above all butyric acid, are caused by volatile substances produced by the action of bacteria on the secretions of sebaceous and apocrine glands. In any case, the activity of apocrine and sebaceous glands and the growth of body hair appear at puberty, which suggests a connec-
tion with sexual development, as is well known in nonhuman mammals.3 Moreover, the production and perception of these odors is in various ways connected with the phenomenon of reproduction. A large quantity of substances with a structure similar to that of testosterone, known as musk-like substances because they were first isolated from the preputial glands of the musk deer, are better perceived by women than by men. Ovariectomized women and women in menopause are much less sensitive to these odors; also, women are about ten times more sensitive to these odors at the time of ovulation than during their menstrual periods. Musk-like substances are widely used in perfumes, and it is curious that so much money is spent for them both by women who can appreciate them and by men who cannot, at least consciously. Other analogous facts in other mammals attest to the importance of odors that have sexual significance in our own species. Women who live in strictly female communities are said to achieve a synchronization of their menstrual cycles, accompanied by a prolongation of the cycle, similar to what has been observed in female mice. Nonsexual social contacts with men reduce the length of the cycle, again as happens in rodents. Moreover, in rodents, puberty occurs earlier in females brought up in a mixed environment. This factor and others could, hypothetically, explain the earlier age of menarche in the younger generation.5 Finally, the connection between olfactory communication and food deserves mention. The alimentary imprinting of rats through the milk, urine, or other substances produced by the mother is well known; young rats learn through their olfactory system the value or noxiousness of foods. Certain substances such as arsenic and diallyl sulphide (the active ingredient in garlic) are excreted by our merocrine sudoriparous glands and are easily recognized by us.3 Visual Communication It was not convenient
for the small
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zoic mammals, from which we evolved, to make themselves evident. Visual communication, because it is fleeting, directional, and can operate at a distance, is a more preferable sense than olfaction for sighting prey and predators than for encounters with conspecific animals. In brief, it is more profitable to receive visual signals than to emit them; in fact, while almost all animals possess photoreceptors, only very few of them have special organs that emit visual signals (a well-known example is the firefly). The body, however, is visible and visual communication occurs in at least three fundamental ways: active movements, gestures, as is the case of herring gulls that fly in a circle above the supply of food to indicate its presence to their companions; expressive movements, positions, postures, displays, or attitudes; and facial expressi0ns.l Since the cutaneous system is not responsible for the signals of movement, gestures, or mimicry, we will not deal with them here. Signals not dependent on body movement, but related to modifications of the skin and/or its appendages, such as the colorful plumage of certain birds or the brilliant coloring of tropical fish, are fairly rare in mammals. This does not mean that visual communication between conspecific animals is poorly developed, but rather that it involves very subtle signals, appreciable only at short distances. The same can be said for auditory communication, particularly in our species where the very refined communication of language makes use of stimuli of rather low intensity and frequencies with respect to the powers of emission. To be conspicuous is an ecologic disadvantage for escaping predators, and this disad-
vantage must in some way be compensated. This compensation is found in the reproductive context: conspicuous coloring or structures are usually present only in males and play a significant role in courtship (eg, the peacock’s tail) or in the competition between males for access to the female (the elk’s horns). Secondary sexual characteristics can be a handicap for the bearer, but it is possible that it is precisely this that signals to the
Clinics in Dermatology
female the greater vitality in the individual who has managed to survive in spite of his handicap and that makes females prefer males with a handicap as the fathers of their offspring.6 Clearly, old age could also be a correlate of vitality and be indicated by such special signs as uhiteningfur in gorillas and baldness in chimpanzees, both connected with testosterone production. In fact, in chimpanzees and gorillas, the older males are the most successful in mating. Even predators may exercise selective pressure on the appearance of a species. To avoid being caught by predators, it is useful for animals to be inconspicuous. Another method is to warn the predator either by signaling one’s own “weapons,” real or false, or by threatening movements. The conspicuousness of such highly colored animals as wasps or the poisonous coral snakes is aimed at discouraging potential predators. Perfectly appetizing and harmless animals may imitate these by assuming the same colorations, and thus attain the same protection. The apparent increase in body size during piloerection in mammals can be considered a threatening gesture; although it is induced by fear, its effect is to provoke fear in the beholder. Sometimes characteristic movements are accentuated by the manifestation of hidden markings when alarmed, Thompson’s gazelles, like most ungulates, switch their tails while assuming a special alert position and exhibit the normally hidden, distinctive black and white markings under the tail.’ Although the selective pressures exercised by predators balance out those related to the necessity of finding a partner, the best strategy is compromise; for example, the presence of signals in parts of the body which are easily hidden: the blue scrotum of vervets, light colored eyelids of mangabeys, and the red, glabrous areas on the chest of gelada baboons. An example of extensive modification of the fur is the coloring in many immature mammals. A baby schema results also from a different body form caused by allometry during growth and is fundamental to gua-
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rantee parental care and the tolerance of other adult animals; it helps recognition at a distance, even when size could be deceptive. In our species, which has lost its “coat” of hair, it is thickness of the subcutaneous fat, the “chubby” look, which, together with the large head and short limbs, makes babies seem cute and triggers reactions of affection.7 Evident skin modifications in monkeys are the periodic reddening and swelling around the perineum (sex skin) in adult females, which appears after the menstrual period and subsides after ovulation. The presence of sex skin, particularly conspicuous in baboons, macaques, talopoins, and chimpanzees, apparently makes the females more attractive to the males. This conspicuousness is almost an exception. However disadvantageous it may be, it is limited to particular periods of time, and it offers advantages to reproduction in that for females, too, although they do not compete for partners, it is important to mate and especially to mate at the right time. Passing from visual communication with each other to gaining visual information about self, it must be observed that an animal can smell itself, touch itself, and also listen to itself (some birds exercise self-control of their singing), but it appears to gain very little information about itself through sight. In the animal world, only the anthropomorphic apes act in front of a mirror in a way that suggests possession of a visual image of self A dog or a cat, for example, rapidly loses interest in its own image reflected in a mirror once it has ascertained that no odors are emitted; whereas, some monkeys and apes explore the image at length, and the anthropomorphic apes seem to realize that it is an image of individual self. Chimpanzees are said to be able to make use of their reflection in a mirror to clean their fur.8 Tactile Communication We are sometimes led to think that tactile communication is limited, even though, to the contrary, tactile signals can be very rapidly initiated, interrupted, and varied in
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intensity and duration. We probably cannot acknowledge the richness of information in the tactile language of love, but we observe that bees can transmit information regarding direction, distance, and quality of a food supply to their companions inside the hive by codified tactile signals in a language comparable in complexity to that of man. Though not limited in codes, tactile communication is much more limited in use than the means of communication mentioned above because the individual can perceive only those objects with which it is in physical contact. One particular type of cutaneous communication is thermal stimulation; because of its nonspecificity, the signal acquires meaning only in conjunction with other information systems. Thermal stimulation has a primary role in the rearing of offspring in birds and mammals, including human beings, both in mother-child and in sibling relationships. Since by “signaling” we normally mean sending information at a distance, and tactile communication occurs through contact, signaling is easily confused with a way of being rather than with a way of communicating. In fact, tactile communication is realized through formalized types of touching; but an individual can obtain information about conspecific animals or even itself through various categories of phenomena connected with touch which we will treat separately: making contact, contact, heterotouching, and self-touching. Making
Contact
Both solitary and social animals maintain precise distances from others and become aggressive as soon as a certain interindividual distance is violated. This type of aggressiveness is released by the sight of a conspecific animal and is inhibited by specific types of ceremonies, including the offering of gifts, which consist principally of expressive movements derived from the behavior of caring for offspring. Such stylized gestures serve to reduce aggressiveness also in other contexts, for example, gestures of submission and appeasement after combat (greeting type gestures). Jackals greet each other
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with a push on the side of the mouth, the same gesture used by the young when requesting parental regurgitation of food. Food passing among insects has the value of social peace: originally used for the nutrition of the larvae, it is important to group cohesion in bee. ant, and termite colonies. Mouth-to-mouth feeding is frequent in maternal care among chimpanzees and in man; kissing is held to have originated from the ritualization of this behavior. Another type of kiss is that of smacking the lips in greeting baboons: these kisses are released by the sight of the pink parts of the body of a conspecific animal, the nipples, penis, perineum, or even the muzzle of a young animal. Consequently, exhibition of one of these areas has the result of an appeasement or greeting gesture, as in the case of the presenting behavior of the female by exhibiting her genital area, or the male by showing his pink, highly vaseularized perineum. Free-rangingchimpanzeesgreet each other with presenting behavior, kisses, and embracing, which may derive from the behavior of the young grasping onto the mother’s fur. Moreover, chimpanzees grasp or “shake” hands; a submissive animal extends his hand palm up begging for a greeting, and higher ranking animals extend their own hands to reassure a companion. These are cases of contact facilitated by ritual touching. Such behavior is fairly frequent in animals used to living close to each other: for example, cats greet with a reciprocal tactile stimulation consisting in light knocks with the head. In the same way, cleansing behaviors express availability for contact and have become ritualized touching for greeting ceremonies.1 Man usually smiles in greeting, thus tranquilizing and dominating possible anger: an equivalent expression is the open-mouthed grin which indicates submission among monkeys. Our laughter seems to be the equivalent of a monkey’s ritualized biting, and ambivalent aggression/submission drive representing both approach and withdrawal. Different degrees of intensity probably characterize theseextremes, represented, respectively, by a scornful laugh and a timid smile.
Dermatology
Contact
Whereas one can speak of visual, olfactory, or auditory contact, we refer here only to bodily or tactile contact, which, as we have seen, requires specific ceremonials in both solitary and social animals. Among solitary animals contact is sought during sexual relations and sometimes during the care of offspring: among social animals, contact seems also to be self-remunerative. All gregarious animals display an evident need for closeness and bodily contact which they seek with obvious appetitive behavior. The importance of such contact becomes evident in animals which, when separated from their group and kept in isolation, show signs of unease. Many anthropoid apes in zoos need a custodian to play with, to scratch them, caress them, and otherwise keep them company. Otherwise, they become ill. Free-ranging animals have particular positions of contact: for example, titi monkeys entwine their tails when resting. Contact is also observed in such social animals as prairie dogs when sunbathing. Chimpanzees have been observed to hold an arm on the shoulder of another, usually lower ranking, subject. Human beings too, with some cultural variations, walk hand in hand. Our caresses, hand-holding, and kisses are behavioral patterns which derive from the mother-child repertoire. The most important type of contact for proper development of a social animal is the mother-child contact. This is also at the root of the search for contact among adults; contact behavior, in fact, is mainly adapted from infantile behavior and behavior connected with care of offspring. The importance of this contact in apes and monkeys has been shown by the dramatic consequences of maternal deprivation on subsequent behavior. Rhesus monkeys deprived of their mothers sit passively in their cages, gazing into space and present stereotype behavior such as hugging their own body or head, rocking back and forth for long periods, suckingvarious parts of their body, and, in some cases, they even traumatize themselves with bites and scratches.9 Their entire sociosexual
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behavior is disturbed: they are often attacked by their male companions because of their abnormal behavior in staring at them without averting their eyes; they do not participate in play or socialized group grooming. As adults, they are incapable of reproduction: the males tend to be rejected by females and are, in any case, incapable of assuming the correct position for copulation.The females, when they bear offspring, never manifest normal maternal behavior.10 How does isolation achieve this effect? The question is what inflicts the most damage, the lack of the mother or the lack of peers? Also, which aspects of maternal behavior are the most important? Individual analysis of these factors, modified one at a time, shows that the absence of peers is mainly responsible for deficiencies in play and sexual behavior, and that the absence of the mother produces similar effects; young animals reared without the mother interact little with their companions, spending most of their time hugging each other or their surrogate mothers. This is probably due to the fact that the young without a mother have not experienced her rejection. In normal motheroffspring situations the initiative for making contact is taken by both the young and the mother; the mother may accept or reject the contact. During the baby’s first weeks the mother initiates and accepts contact; this period is followed by an ambivalent stage, and finally the mother rejects contact more and more often while the offspring seek it less and less. The behaviors leading to interruption of contact are analogous. Young animals with surrogate mothers do not experience this kind of “weaning” and their social initiative and development remain blocked. Use of surrogate mothers has permitted an evaluation and analysis of the individual stimuli offered by true mothers in the development of the attachment of their young to them. Using models that supplied one stimulus or more at a time (ie, nutrition, warmth, a surface to cling to, rocking, and/or slight inclination), it was observed that the crucial factor in the development of love for the mother and the baby’s seeking her out was
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the comfort of contact produced by a soft, furry (better if warm, rocking, and slightly inclined) surface. A model of this type is clearly preferred to a wire model even if it is equipped with a milk distributor.” Heterotouching We have already discussed the ritual touching that helps many animals overcome their initial aversion to and their fear of contact. Specific behavioral patterns, such as sexual behavior or care for the young or, in animals open to contact, simple contact follow. Particular touchings, also serve to maintain a form of physical contact, that can be autoremunerative. These kinds of touching in animals inclined to contact consist mainly of grooming and are much more frequent than the cleaning needs of the body would require. Birds preen and many social species of mammals groom the fur with the teeth or more often with both hands (or front paws) to pick, scratch, or otherwise explore the hair. This behavior has been observed in almost all of the primate species studied. One of the functions of this behavior is hygienic, as is demonstrated by the fact that the parts of the body most commonly picked by another animal are those that the individual himself cannot reach in self-grooming; most of the attention is given to removing dirt, scales of dry skin, or parasites and to attending to wounds. A second immediate function of grooming is to reduce aggressiveness; in fact, this reciprocal touchinggrooming often follows an approachment sequence in many mammal species and occurs most frequently in cases of forced closeness. It is probable that its appeasement effect is produced by keeping the animals still; dogs and cats, for example, remain still while being petted. The long-term effects of grooming are much more important for stable relationships between individuals. The distribution frequency with which this behavior is executed among individuals in a group faithfully reflects the group’s social structure and is sensitive to all the structural factors of a primate society, ie, sex, age, hierarchy, and kinship. Grooming is done more by females
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than males, and more by adults than by the young, and the latter are the main object of grooming. High ranking individuals groom others less and are themselves groomed more: grooming occurs most frequently among kin I:! The human equivalents of grooming are quite obvious. Skin care, picking at pimples, or doing the hair, as well as removing dry or peeling skin are, like caresses, appeasing behavior which consolidates bonds of intimacy and confidence. Curiously, having one’s hair groomed induces a certain degree of relaxation (perhaps because it requires immobility). Evidently, the structural factors of human society are much more complex than those of a group of monkeys: but, at least at first sight, sex, age, and kinship act in a not completely contrasting way in human groups, too.
When animals face a conflicting situation they often react with movements that cannot be attributed to either of the two contrasting solutions. These movements are called substitute activities and derive mainly from the spheres of eating, sleeping, and, most often. body care: cleaning the beak, scratching, shaking, washing, and many other types of behavior connected to body hygiene can become substitute activities. Conflict often arises from a drive contrasted by a threat and threatening contexts usually provoke the ruffling of feathers or raising of hairs, or, in the case of humans, sweating, reactions that all offer appropriate stimuli for body care and cleansing. It may be for this reason that the most substitute activities derive from the repertoire of body care. Although the primary function of self-grooming is to rid the hair of parasites and dirt, grooming could be partially interpreted as a substitute activity since it is most frequent in contexts where one could hypothesize states of anxiety, frustration, or conflict. Groomingactivities are quite different from scratching, and nothing can be said about itching. The human equivalents of self-grooming have been examined in detail by observing
Clirucs in Dermatology
the behavior of speakers who are presumably torn between the desire to escape and the impossibility of doing so, if not the desire to attack the audience. The most serious cases exhibit sweating, trembling, or restlessness; speakers usually control these reactions, limiting them to substitute activities such as biting a pen or smoking-taken from the eating context-yawningor stretching-taken from sleeping context-or, most often, scratching the head, smoothing the beard, adjusting the tie, touching the chin, or passing the hand(s) over the body as if to dry sweat-all taken from the grooming contexti One particular type of self-touching, selfinjury, which we mentioned above, is common in rhesus monkeys brought up in social isolation. This behavior becomes conspicuous after the animals have reached the ageof three, ie, puberty, and is most often manifested in the presence of strangers. These facts, along with the self-aggressive aspects, reminds us of the behavior of autistic children.” The Unique Characteristic of Human Skin If a nonhuman zoologist had to place in an exhibit with other animals, a human specimen preserved in alcohol, he would most probably put it next to the anthropoid apes. If he had to specify the human specimen’s peculiar characteristics, he would say that it is almost hairless. Although humans have more hair on their skins than apes, from a functional point of view man is naked and this is the most evident of his distinctive characteristics. Moreover, many other typically human characteristics are related to the skin. Compared with that of apes, human skin is thicker and more elastic, tougher and more sensitive. The dermis of human skin is richer in elastic fibers and is better vascularized; it has many nervous terminations and is rich in sudoriparous glands.14 No other primate is naked, and of the more than 4,500 species of mammals only very few have relinquished the adaptive advantage of a thick fur. These few species have one char-
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acteristic in common: they all live in an unusual environment. Bats have denuded wings to enable them to fly better: some mammals that live underground do not need fur; seals and dolphins achieve better thermoregulation with a thick subcutaneous fatty layer than they would if they had fur. Aside from these examples there are very few relatively naked land mammals, and those that exist are all of large dimensions and to some degree bound to an aquatic environment, eg, elephant, hippopotamus, and rhinoceros. These large animals also have specific problems of thermoregulation linked with their very low surface area/volume ratio.lj In our present condition as human beings, however, we have nothing in common with animals that fly or live in water or underground or are gigantic, and little can be said of our past styles of life. In any case, the factors which must have greatly influenced our peculiar transformation into naked creatures were probably connected with problems of locomotion and thermoregulation. In agreement with this, it has been claimed that in some period of our history we must have lived an aquatic phase in response to the need to escape from the large carnivores.16 More realistically the loss of fur cover could depend on the different thermoregulatory requirements of the continuous muscular tension involved in standing and moving in an erect position. I7 When our ancestors abandoned the forest and adapted to live in the Savannah, they adopted a less furtive way of life, but a life in which it was important to run on open ground, both to flee from predators and to procure food. Since chimpanzees easily assume an erect stance and a bipedal locomotion when they run on open ground, it can be hypothesized that the creatures from which we derive could do the same before undergoing a complete evolutionary adaptation. This implies extra muscular labor. Our erect stance itself is not completely functional; sometimes we need to sit or to lie down in order to rest. In any case, man today finds himself equipped with a thermoregulatory system, with sudoriparous glands that ensure cooling by evaporation of the liquid they
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secrete, and with a thick subcutaneous layer of fat that protects from cold, which allows great and long-lasting physical efforts. The time of human evolution has been a very long one for behavioral transformations, but a short one for basic biologic evolution and a new function could often come about by behavioral change rather than through organ evolution. This is especially true for signaling functions. In fact, we have seen how behaviors evolved for the care of the young can be utilized in a different sociosexual context and a communicative pattern can be transferred from one context to another. On the contrary innate releasing mechanisms, which make animals and man respond automatically to the signal independently from the context, remain relatively fixed. In this way transformations in our external aspect, and particularly our unique features connected with the skin, however produced, can assume new communicative functions, that can tentatively be interpreted in the light of old releasing mechanisms. Although it is not possible to establish the physiologic need that stimulated the evolution of swollen breasts in women, the deposits of adipose and connective tissue in the female breast and in the puffy cheeks of infants form signaling structures that impart appeasing effects. Still less can be said about the evolution of prominent red lips or eyebrows, but they do emphasize expressive movements such as offering food or threateningly widening the eyes. Somealterations in the skin give information only about the fact itself, like wrinkles due to age; others give us information about things of which we are unaware, as for example, the small waist and consequently protruding bottom of a woman inform one of her good reproductive ability and hormonal function, and it is not necessary for a man to know physiology to appreciate this evidence. It is the same with flushing: not knowing what color skin our far-away ancestors had, we cannot risk any hypothesis on its evolution, but currently it informs us, even without any physiologic knowledge, of a state of excitement causing peripheral vasodilata-
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tion which in turn provokes excitement. analogous to that induced by the sight of sexual skin among monkeys and apes.lk This is not deception, just as it is not deception when an advertisement uses a young girl with a lovely smile to present a product. No one expects to receive the girl or the smile when he/she buys the product and noone believes that the product is really better than another, but the presence of that releasing signal automatically induces us to be well disposed to whatever follows. It has been suggested that our automatic responses to innate releasing mechanisms are so strong that they can remain at work even in the absence of the signaling structure, as for example, the idea of courage evoked by broad shoulders in man. even now that with the reduction of hairs the frightening aspect caused by piloerection is no longer produced. The ethologic implications of the skin considered above are prevalently communicative ones. Although there is no evidence of specific behavior connected with skin affections in animals, as permanent or cyclic transformations in external aspect became new signals independently of the causative context and physiologic mechanisms, analogous communicative value of reactions induced by pathologic transformations cannot be excluded. Furthermore, the symptom, whatever its physiologic origins, is a sign of the communicative repertory involving the suffering person and his social environment within which medical semiotics of any type are only a particular communicative code peculiar to the doctor-patient pair. References 1. Eibl-Eibesfeldt
I. Ethology: the biology of behavior. New York: Halt. Rinehart and Winston, 1970.
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\lainardi I). Marson M. Pasquali A. Causationofsexual preferences in the house mice. The behaviour of
mice reared by parents whose odor was artificially altered. Atti Sor Ital Sci Nat Mus Civ Star Nat Milano. 19ti6:104:325-338. Stoddart DM. Mammalian odors and pheromones. I,ondon: Edward Arnold. 1976. Mykytowyck
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%ahavi A. Mateselection:aselection Theor Rio]. 1975:5X205-214.
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fora handicap..J
Marler I’. Visual systems. In: Sebeok TA, ed. Animal communication. Bloomington: Indiana Universit! f’ress. 1968:10%126.
Mitchell (;. Abnormal behavior in primates. In: Rosenblum 1,A. ed. Primate behavior: developments in field and laboratory research. Vol. 1. New York: Academic Press. 1970:195-249. Sackett
in rhesus monkeys folIn: Friedman RC. Richert RM. Vande Wiele RL, eds. Sex differences in behavior. New York: John Wiley & Sons. 1974:99-122. lowing
GP. Sex differences
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Harlow HF. Zimmerman RR. Affectional responses In the infant monkey. Science. 1959;130:421-432, Mitchell G. Tokunaga DH. Sex differences in nonhw man primate grooming. Behav Proc. 1976:1:335-347. z+lss R. Beobachtungen zur frage der ubersprungbeweyungen im menschlichen verhalten. Psycho1 Bcitr. 1965:Y:l-97. Montagna W. Parakkal PF. The structure and function of skin. New York: Academic Press. 1974. Morris 1). The naked ape. New York: Dell Publishing (‘0. 1967. Hardy A. Was man more aquatic Scient. 1960:7:642-645.
in the past? New
Montagna W. The skin of primates and origin human skin. Anthrop Cont. 1980:3:242-24X Morris 1977.
D. Manwatching.
for correspondence: Patrizia Messeri, Ph.D., Istitutodi Via Romana, 17, 50125 Florence, Italy.
London:
Zoologiadella
Jonathan
of
Cape.
Universitadi
Ethologic Implications of the Skin and its Disturbances
Patrizia Messeri, Ph.D., and William Montagna, Ph.D.
From the Department of Zoology, University of Florence, Florence, Italy, and the Department of Dermatology, Oregon Health Sciences University, Portland, Oregon
From the beginning of its simplest forms, animal life appears to be organized according to specialization by inner functions and surface functions. The passage from prokaryotic to eukaryotic cells, from bacteria to unicellular organisms, consists essentially of a functional specialization of surfaces, accompanied by an extraordinary development of plasma membrane from which originate membranous surfaces that have become specialized into endoplasmic reticulum and nuclear envelope, transferred inside the cell. Whereas the inner functions of cells are prevalently synthetic or transformational, the surface functions are concerned with chemical, physical, or informational exchanges with the environment. With the progressive increase in complexity that accompanies the passage from unicellular to multicellular conditions and the formation of systems of organs, the functions of chemical exchange are performed by surface elements which progressively move inside the body and become specialized(lungs, intestines, kidneys), whereas the outer surface conserves the function of relations with both the physical and the living environment. The function of the outer surface is mainly a protective one. Among the functional protection from the physical environment are the control of osmotic equilibrium, protection from attrition, and the maintenance of body temperature. To perform these many functions in many different environments, the integumentary system presents a wide range of variations both in the skin and in its appendages (cuticles, scales, hair, feathers, beaks, nails and claws, and many others). Equally important functions of the integuments are those connected with relations between organisms and the living environment. The skin and its appendages are the principal signal transmitters for olfactory, visual, and tactile communications. Regarding tactile communication, moreover, the skin also functions as a receptor organ. Olfactory Communication Although it is the channel of communication most largely used in the animal world and the most primitive of all forms of animal communication, olfactory communication is the least known, largely 27
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because our own sense of smell is poorly developed. Animals live in a world full of sensory stimulations, and therefore, in order to be effective, a signal must be prominent by being endowed with peculiar characteristics. Visual and auditory signals usually achieve this aim by virtue of characteristic spatial or temporal patterns, but olfactory signals are particularly persistent and once emitted cannot be easily modified. Consequently, olfactory communication has limitations: first, it supplies a limited range of information (yes-no type); second, it is highly selective and, in some cases, a receptor appears to react only to one specific substance. The prolonged spatiotemporal persistenceof an odor also has advantages: chemical signals can act over a long distance and in many directions simultaneously and thus are the most important signals for specific recognition and for sexual encounters. Smell seems to be the best sense for long distance attraction; the males of certain species of moths can detect the presence of a female many kilometers away. Furthermore, these chemical signals are highly selective and elude individuals of other species and potential predators. Mammals were originally small, shy animals. It would be disadvantageous for them to emit signals that could make them easy prey to such predators as birds with excellent sight and limited, but highly discriminate hearing. This situation favored the development of an olfactory system useful for social encounters and for reproduction. Consequently, most of the 4,500-odd species of mammals have an acute sense of smell. Odors are used for territorial markings, group status and rank recognition, maternal behavior, and the detection of food and predators. Territorial behavior insures the animal of vital space and spatial distribution appropriate to environmental resources; a territory may be defended, marked, or both. Mammals delineate territory principally by scent marking: at special points in the territory, animals deposit gland secretions and/or
Clinics in Dermatology
urine or excrement. These scent marks are primary indicators for the owners, to help the animals orient themselves and feel “at home”; they probably also serve as repellents to outsiders. Marking methods vary from species to species: hamsters mark their den and salient surrounding objects by rubbing against them and depositing the secretion of their sebaceous flank glands; badgers use the secretion of their anal glands (in a sack at the base of the tail); and galagos urinate on their hands and rub the urine on their soles, to leave a scented trace when they climb trees. There are generally specific scent glands for marking, located in different parts of the body of different species. The development and use of these glandsdepend on the animal’s sex and rank; the largest and most active glands are found in high-ranking males, in which they are controlled by adrenal and gonadal hormones. In many species the scent marking is used for conspecific animals; for example, male rabbits “mark” their females by rubbing their submandibular gland secretions on them. Similarly, cats rub their cheeks against objects, humans, and other cats. The marking of conspecific individuals in social species, and in particular insects and mammals, establishes a group or family odor scent.’ Odor is particularly important at the time of birth. Mice made anosmic have no maternal behavior; and in sheep and goats, the mother-baby bond is influenced by the mother’s capacity to smell the odor of the baby during a brief critical period after the birth. These odors can also have lasting effects. Newborn mice kept in a nest artificially scented with a certain odor show a perference, when reaching sexual maturity, for partners scented with the same odor.2 Notwithstanding its many secondary functions in mammals, olfaction has a fundamental importance in species identification and sexual behavior. It is generally held that it is the males who perceive the odor of the females, particularly when the females are in estrus; these substances, called pheromones, are controlled by hormones. It has
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Ethology of the Skin
been shown that a male macaque can be trained to press a bar to gain access to a female in estrus, or to an ovariectomized female treated with estrogens. When the male was made anosmic, it ceased to press the bar. Female mammals also respond to the odor of males: cats and sows in estrus assume the coital position when exposed to the odors of a male cat or pig.3 It may seem strange that human beings agree that the sense they are least willing to do without is smell, while at the same time they expend so much effort in hiding their odor(s) with deodorants and perfumes. One possible explanation is that human beings are an exception among mammals; another is that our sensitivity to odors, because of its primitive character, is mostly unconscious.4 Young volunteers tested to see if they could recognize (by smell) clothing belonging to their sexual partners demonstrated that they could choose the correct article of clothing in a percentage of cases significantly higher than chance, although they were not able to explain why they chose as they did. Moreover, the perception and the production of odorous secretions elude conscious control, as is demonstrated by galvanic skin response (and as those affected with bromhidrosis know). Mammals use practically all their excretory organs to produce odors. One of the least specialized odors is that of urine. The sebaceous glands are, by far, the most active of all the cutaneous organs and the main source of odor, even in man. Apocrine glands in human beings are associated with body hairs, primarily in the armpits, sometimes the breasts, the genital and anal regions, the external auditory canal, the eyelids, and the lips. The surface of hairs increases the surface area for diffusion of secretions, and potentiate diffusion in the air. We do not perceive these secretions; the odors we perceive best, above all butyric acid, are caused by volatile substances produced by the action of bacteria on the secretions of sebaceous and apocrine glands. In any case, the activity of apocrine and sebaceous glands and the growth of body hair appear at puberty, which suggests a connec-
tion with sexual development, as is well known in nonhuman mammals.3 Moreover, the production and perception of these odors is in various ways connected with the phenomenon of reproduction. A large quantity of substances with a structure similar to that of testosterone, known as musk-like substances because they were first isolated from the preputial glands of the musk deer, are better perceived by women than by men. Ovariectomized women and women in menopause are much less sensitive to these odors; also, women are about ten times more sensitive to these odors at the time of ovulation than during their menstrual periods. Musk-like substances are widely used in perfumes, and it is curious that so much money is spent for them both by women who can appreciate them and by men who cannot, at least consciously. Other analogous facts in other mammals attest to the importance of odors that have sexual significance in our own species. Women who live in strictly female communities are said to achieve a synchronization of their menstrual cycles, accompanied by a prolongation of the cycle, similar to what has been observed in female mice. Nonsexual social contacts with men reduce the length of the cycle, again as happens in rodents. Moreover, in rodents, puberty occurs earlier in females brought up in a mixed environment. This factor and others could, hypothetically, explain the earlier age of menarche in the younger generation.5 Finally, the connection between olfactory communication and food deserves mention. The alimentary imprinting of rats through the milk, urine, or other substances produced by the mother is well known; young rats learn through their olfactory system the value or noxiousness of foods. Certain substances such as arsenic and diallyl sulphide (the active ingredient in garlic) are excreted by our merocrine sudoriparous glands and are easily recognized by us.3 Visual Communication It was not convenient
for the small
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zoic mammals, from which we evolved, to make themselves evident. Visual communication, because it is fleeting, directional, and can operate at a distance, is a more preferable sense than olfaction for sighting prey and predators than for encounters with conspecific animals. In brief, it is more profitable to receive visual signals than to emit them; in fact, while almost all animals possess photoreceptors, only very few of them have special organs that emit visual signals (a well-known example is the firefly). The body, however, is visible and visual communication occurs in at least three fundamental ways: active movements, gestures, as is the case of herring gulls that fly in a circle above the supply of food to indicate its presence to their companions; expressive movements, positions, postures, displays, or attitudes; and facial expressi0ns.l Since the cutaneous system is not responsible for the signals of movement, gestures, or mimicry, we will not deal with them here. Signals not dependent on body movement, but related to modifications of the skin and/or its appendages, such as the colorful plumage of certain birds or the brilliant coloring of tropical fish, are fairly rare in mammals. This does not mean that visual communication between conspecific animals is poorly developed, but rather that it involves very subtle signals, appreciable only at short distances. The same can be said for auditory communication, particularly in our species where the very refined communication of language makes use of stimuli of rather low intensity and frequencies with respect to the powers of emission. To be conspicuous is an ecologic disadvantage for escaping predators, and this disad-
vantage must in some way be compensated. This compensation is found in the reproductive context: conspicuous coloring or structures are usually present only in males and play a significant role in courtship (eg, the peacock’s tail) or in the competition between males for access to the female (the elk’s horns). Secondary sexual characteristics can be a handicap for the bearer, but it is possible that it is precisely this that signals to the
Clinics in Dermatology
female the greater vitality in the individual who has managed to survive in spite of his handicap and that makes females prefer males with a handicap as the fathers of their offspring.6 Clearly, old age could also be a correlate of vitality and be indicated by such special signs as uhiteningfur in gorillas and baldness in chimpanzees, both connected with testosterone production. In fact, in chimpanzees and gorillas, the older males are the most successful in mating. Even predators may exercise selective pressure on the appearance of a species. To avoid being caught by predators, it is useful for animals to be inconspicuous. Another method is to warn the predator either by signaling one’s own “weapons,” real or false, or by threatening movements. The conspicuousness of such highly colored animals as wasps or the poisonous coral snakes is aimed at discouraging potential predators. Perfectly appetizing and harmless animals may imitate these by assuming the same colorations, and thus attain the same protection. The apparent increase in body size during piloerection in mammals can be considered a threatening gesture; although it is induced by fear, its effect is to provoke fear in the beholder. Sometimes characteristic movements are accentuated by the manifestation of hidden markings when alarmed, Thompson’s gazelles, like most ungulates, switch their tails while assuming a special alert position and exhibit the normally hidden, distinctive black and white markings under the tail.’ Although the selective pressures exercised by predators balance out those related to the necessity of finding a partner, the best strategy is compromise; for example, the presence of signals in parts of the body which are easily hidden: the blue scrotum of vervets, light colored eyelids of mangabeys, and the red, glabrous areas on the chest of gelada baboons. An example of extensive modification of the fur is the coloring in many immature mammals. A baby schema results also from a different body form caused by allometry during growth and is fundamental to gua-
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rantee parental care and the tolerance of other adult animals; it helps recognition at a distance, even when size could be deceptive. In our species, which has lost its “coat” of hair, it is thickness of the subcutaneous fat, the “chubby” look, which, together with the large head and short limbs, makes babies seem cute and triggers reactions of affection.7 Evident skin modifications in monkeys are the periodic reddening and swelling around the perineum (sex skin) in adult females, which appears after the menstrual period and subsides after ovulation. The presence of sex skin, particularly conspicuous in baboons, macaques, talopoins, and chimpanzees, apparently makes the females more attractive to the males. This conspicuousness is almost an exception. However disadvantageous it may be, it is limited to particular periods of time, and it offers advantages to reproduction in that for females, too, although they do not compete for partners, it is important to mate and especially to mate at the right time. Passing from visual communication with each other to gaining visual information about self, it must be observed that an animal can smell itself, touch itself, and also listen to itself (some birds exercise self-control of their singing), but it appears to gain very little information about itself through sight. In the animal world, only the anthropomorphic apes act in front of a mirror in a way that suggests possession of a visual image of self A dog or a cat, for example, rapidly loses interest in its own image reflected in a mirror once it has ascertained that no odors are emitted; whereas, some monkeys and apes explore the image at length, and the anthropomorphic apes seem to realize that it is an image of individual self. Chimpanzees are said to be able to make use of their reflection in a mirror to clean their fur.8 Tactile Communication We are sometimes led to think that tactile communication is limited, even though, to the contrary, tactile signals can be very rapidly initiated, interrupted, and varied in
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intensity and duration. We probably cannot acknowledge the richness of information in the tactile language of love, but we observe that bees can transmit information regarding direction, distance, and quality of a food supply to their companions inside the hive by codified tactile signals in a language comparable in complexity to that of man. Though not limited in codes, tactile communication is much more limited in use than the means of communication mentioned above because the individual can perceive only those objects with which it is in physical contact. One particular type of cutaneous communication is thermal stimulation; because of its nonspecificity, the signal acquires meaning only in conjunction with other information systems. Thermal stimulation has a primary role in the rearing of offspring in birds and mammals, including human beings, both in mother-child and in sibling relationships. Since by “signaling” we normally mean sending information at a distance, and tactile communication occurs through contact, signaling is easily confused with a way of being rather than with a way of communicating. In fact, tactile communication is realized through formalized types of touching; but an individual can obtain information about conspecific animals or even itself through various categories of phenomena connected with touch which we will treat separately: making contact, contact, heterotouching, and self-touching. Making
Contact
Both solitary and social animals maintain precise distances from others and become aggressive as soon as a certain interindividual distance is violated. This type of aggressiveness is released by the sight of a conspecific animal and is inhibited by specific types of ceremonies, including the offering of gifts, which consist principally of expressive movements derived from the behavior of caring for offspring. Such stylized gestures serve to reduce aggressiveness also in other contexts, for example, gestures of submission and appeasement after combat (greeting type gestures). Jackals greet each other
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with a push on the side of the mouth, the same gesture used by the young when requesting parental regurgitation of food. Food passing among insects has the value of social peace: originally used for the nutrition of the larvae, it is important to group cohesion in bee. ant, and termite colonies. Mouth-to-mouth feeding is frequent in maternal care among chimpanzees and in man; kissing is held to have originated from the ritualization of this behavior. Another type of kiss is that of smacking the lips in greeting baboons: these kisses are released by the sight of the pink parts of the body of a conspecific animal, the nipples, penis, perineum, or even the muzzle of a young animal. Consequently, exhibition of one of these areas has the result of an appeasement or greeting gesture, as in the case of the presenting behavior of the female by exhibiting her genital area, or the male by showing his pink, highly vaseularized perineum. Free-rangingchimpanzeesgreet each other with presenting behavior, kisses, and embracing, which may derive from the behavior of the young grasping onto the mother’s fur. Moreover, chimpanzees grasp or “shake” hands; a submissive animal extends his hand palm up begging for a greeting, and higher ranking animals extend their own hands to reassure a companion. These are cases of contact facilitated by ritual touching. Such behavior is fairly frequent in animals used to living close to each other: for example, cats greet with a reciprocal tactile stimulation consisting in light knocks with the head. In the same way, cleansing behaviors express availability for contact and have become ritualized touching for greeting ceremonies.1 Man usually smiles in greeting, thus tranquilizing and dominating possible anger: an equivalent expression is the open-mouthed grin which indicates submission among monkeys. Our laughter seems to be the equivalent of a monkey’s ritualized biting, and ambivalent aggression/submission drive representing both approach and withdrawal. Different degrees of intensity probably characterize theseextremes, represented, respectively, by a scornful laugh and a timid smile.
Dermatology
Contact
Whereas one can speak of visual, olfactory, or auditory contact, we refer here only to bodily or tactile contact, which, as we have seen, requires specific ceremonials in both solitary and social animals. Among solitary animals contact is sought during sexual relations and sometimes during the care of offspring: among social animals, contact seems also to be self-remunerative. All gregarious animals display an evident need for closeness and bodily contact which they seek with obvious appetitive behavior. The importance of such contact becomes evident in animals which, when separated from their group and kept in isolation, show signs of unease. Many anthropoid apes in zoos need a custodian to play with, to scratch them, caress them, and otherwise keep them company. Otherwise, they become ill. Free-ranging animals have particular positions of contact: for example, titi monkeys entwine their tails when resting. Contact is also observed in such social animals as prairie dogs when sunbathing. Chimpanzees have been observed to hold an arm on the shoulder of another, usually lower ranking, subject. Human beings too, with some cultural variations, walk hand in hand. Our caresses, hand-holding, and kisses are behavioral patterns which derive from the mother-child repertoire. The most important type of contact for proper development of a social animal is the mother-child contact. This is also at the root of the search for contact among adults; contact behavior, in fact, is mainly adapted from infantile behavior and behavior connected with care of offspring. The importance of this contact in apes and monkeys has been shown by the dramatic consequences of maternal deprivation on subsequent behavior. Rhesus monkeys deprived of their mothers sit passively in their cages, gazing into space and present stereotype behavior such as hugging their own body or head, rocking back and forth for long periods, suckingvarious parts of their body, and, in some cases, they even traumatize themselves with bites and scratches.9 Their entire sociosexual
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behavior is disturbed: they are often attacked by their male companions because of their abnormal behavior in staring at them without averting their eyes; they do not participate in play or socialized group grooming. As adults, they are incapable of reproduction: the males tend to be rejected by females and are, in any case, incapable of assuming the correct position for copulation.The females, when they bear offspring, never manifest normal maternal behavior.10 How does isolation achieve this effect? The question is what inflicts the most damage, the lack of the mother or the lack of peers? Also, which aspects of maternal behavior are the most important? Individual analysis of these factors, modified one at a time, shows that the absence of peers is mainly responsible for deficiencies in play and sexual behavior, and that the absence of the mother produces similar effects; young animals reared without the mother interact little with their companions, spending most of their time hugging each other or their surrogate mothers. This is probably due to the fact that the young without a mother have not experienced her rejection. In normal motheroffspring situations the initiative for making contact is taken by both the young and the mother; the mother may accept or reject the contact. During the baby’s first weeks the mother initiates and accepts contact; this period is followed by an ambivalent stage, and finally the mother rejects contact more and more often while the offspring seek it less and less. The behaviors leading to interruption of contact are analogous. Young animals with surrogate mothers do not experience this kind of “weaning” and their social initiative and development remain blocked. Use of surrogate mothers has permitted an evaluation and analysis of the individual stimuli offered by true mothers in the development of the attachment of their young to them. Using models that supplied one stimulus or more at a time (ie, nutrition, warmth, a surface to cling to, rocking, and/or slight inclination), it was observed that the crucial factor in the development of love for the mother and the baby’s seeking her out was
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the comfort of contact produced by a soft, furry (better if warm, rocking, and slightly inclined) surface. A model of this type is clearly preferred to a wire model even if it is equipped with a milk distributor.” Heterotouching We have already discussed the ritual touching that helps many animals overcome their initial aversion to and their fear of contact. Specific behavioral patterns, such as sexual behavior or care for the young or, in animals open to contact, simple contact follow. Particular touchings, also serve to maintain a form of physical contact, that can be autoremunerative. These kinds of touching in animals inclined to contact consist mainly of grooming and are much more frequent than the cleaning needs of the body would require. Birds preen and many social species of mammals groom the fur with the teeth or more often with both hands (or front paws) to pick, scratch, or otherwise explore the hair. This behavior has been observed in almost all of the primate species studied. One of the functions of this behavior is hygienic, as is demonstrated by the fact that the parts of the body most commonly picked by another animal are those that the individual himself cannot reach in self-grooming; most of the attention is given to removing dirt, scales of dry skin, or parasites and to attending to wounds. A second immediate function of grooming is to reduce aggressiveness; in fact, this reciprocal touchinggrooming often follows an approachment sequence in many mammal species and occurs most frequently in cases of forced closeness. It is probable that its appeasement effect is produced by keeping the animals still; dogs and cats, for example, remain still while being petted. The long-term effects of grooming are much more important for stable relationships between individuals. The distribution frequency with which this behavior is executed among individuals in a group faithfully reflects the group’s social structure and is sensitive to all the structural factors of a primate society, ie, sex, age, hierarchy, and kinship. Grooming is done more by females
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Messed and Montagno
than males, and more by adults than by the young, and the latter are the main object of grooming. High ranking individuals groom others less and are themselves groomed more: grooming occurs most frequently among kin I:! The human equivalents of grooming are quite obvious. Skin care, picking at pimples, or doing the hair, as well as removing dry or peeling skin are, like caresses, appeasing behavior which consolidates bonds of intimacy and confidence. Curiously, having one’s hair groomed induces a certain degree of relaxation (perhaps because it requires immobility). Evidently, the structural factors of human society are much more complex than those of a group of monkeys: but, at least at first sight, sex, age, and kinship act in a not completely contrasting way in human groups, too.
When animals face a conflicting situation they often react with movements that cannot be attributed to either of the two contrasting solutions. These movements are called substitute activities and derive mainly from the spheres of eating, sleeping, and, most often. body care: cleaning the beak, scratching, shaking, washing, and many other types of behavior connected to body hygiene can become substitute activities. Conflict often arises from a drive contrasted by a threat and threatening contexts usually provoke the ruffling of feathers or raising of hairs, or, in the case of humans, sweating, reactions that all offer appropriate stimuli for body care and cleansing. It may be for this reason that the most substitute activities derive from the repertoire of body care. Although the primary function of self-grooming is to rid the hair of parasites and dirt, grooming could be partially interpreted as a substitute activity since it is most frequent in contexts where one could hypothesize states of anxiety, frustration, or conflict. Groomingactivities are quite different from scratching, and nothing can be said about itching. The human equivalents of self-grooming have been examined in detail by observing
Clirucs in Dermatology
the behavior of speakers who are presumably torn between the desire to escape and the impossibility of doing so, if not the desire to attack the audience. The most serious cases exhibit sweating, trembling, or restlessness; speakers usually control these reactions, limiting them to substitute activities such as biting a pen or smoking-taken from the eating context-yawningor stretching-taken from sleeping context-or, most often, scratching the head, smoothing the beard, adjusting the tie, touching the chin, or passing the hand(s) over the body as if to dry sweat-all taken from the grooming contexti One particular type of self-touching, selfinjury, which we mentioned above, is common in rhesus monkeys brought up in social isolation. This behavior becomes conspicuous after the animals have reached the ageof three, ie, puberty, and is most often manifested in the presence of strangers. These facts, along with the self-aggressive aspects, reminds us of the behavior of autistic children.” The Unique Characteristic of Human Skin If a nonhuman zoologist had to place in an exhibit with other animals, a human specimen preserved in alcohol, he would most probably put it next to the anthropoid apes. If he had to specify the human specimen’s peculiar characteristics, he would say that it is almost hairless. Although humans have more hair on their skins than apes, from a functional point of view man is naked and this is the most evident of his distinctive characteristics. Moreover, many other typically human characteristics are related to the skin. Compared with that of apes, human skin is thicker and more elastic, tougher and more sensitive. The dermis of human skin is richer in elastic fibers and is better vascularized; it has many nervous terminations and is rich in sudoriparous glands.14 No other primate is naked, and of the more than 4,500 species of mammals only very few have relinquished the adaptive advantage of a thick fur. These few species have one char-
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acteristic in common: they all live in an unusual environment. Bats have denuded wings to enable them to fly better: some mammals that live underground do not need fur; seals and dolphins achieve better thermoregulation with a thick subcutaneous fatty layer than they would if they had fur. Aside from these examples there are very few relatively naked land mammals, and those that exist are all of large dimensions and to some degree bound to an aquatic environment, eg, elephant, hippopotamus, and rhinoceros. These large animals also have specific problems of thermoregulation linked with their very low surface area/volume ratio.lj In our present condition as human beings, however, we have nothing in common with animals that fly or live in water or underground or are gigantic, and little can be said of our past styles of life. In any case, the factors which must have greatly influenced our peculiar transformation into naked creatures were probably connected with problems of locomotion and thermoregulation. In agreement with this, it has been claimed that in some period of our history we must have lived an aquatic phase in response to the need to escape from the large carnivores.16 More realistically the loss of fur cover could depend on the different thermoregulatory requirements of the continuous muscular tension involved in standing and moving in an erect position. I7 When our ancestors abandoned the forest and adapted to live in the Savannah, they adopted a less furtive way of life, but a life in which it was important to run on open ground, both to flee from predators and to procure food. Since chimpanzees easily assume an erect stance and a bipedal locomotion when they run on open ground, it can be hypothesized that the creatures from which we derive could do the same before undergoing a complete evolutionary adaptation. This implies extra muscular labor. Our erect stance itself is not completely functional; sometimes we need to sit or to lie down in order to rest. In any case, man today finds himself equipped with a thermoregulatory system, with sudoriparous glands that ensure cooling by evaporation of the liquid they
35
secrete, and with a thick subcutaneous layer of fat that protects from cold, which allows great and long-lasting physical efforts. The time of human evolution has been a very long one for behavioral transformations, but a short one for basic biologic evolution and a new function could often come about by behavioral change rather than through organ evolution. This is especially true for signaling functions. In fact, we have seen how behaviors evolved for the care of the young can be utilized in a different sociosexual context and a communicative pattern can be transferred from one context to another. On the contrary innate releasing mechanisms, which make animals and man respond automatically to the signal independently from the context, remain relatively fixed. In this way transformations in our external aspect, and particularly our unique features connected with the skin, however produced, can assume new communicative functions, that can tentatively be interpreted in the light of old releasing mechanisms. Although it is not possible to establish the physiologic need that stimulated the evolution of swollen breasts in women, the deposits of adipose and connective tissue in the female breast and in the puffy cheeks of infants form signaling structures that impart appeasing effects. Still less can be said about the evolution of prominent red lips or eyebrows, but they do emphasize expressive movements such as offering food or threateningly widening the eyes. Somealterations in the skin give information only about the fact itself, like wrinkles due to age; others give us information about things of which we are unaware, as for example, the small waist and consequently protruding bottom of a woman inform one of her good reproductive ability and hormonal function, and it is not necessary for a man to know physiology to appreciate this evidence. It is the same with flushing: not knowing what color skin our far-away ancestors had, we cannot risk any hypothesis on its evolution, but currently it informs us, even without any physiologic knowledge, of a state of excitement causing peripheral vasodilata-
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and Montaana
tion which in turn provokes excitement. analogous to that induced by the sight of sexual skin among monkeys and apes.lk This is not deception, just as it is not deception when an advertisement uses a young girl with a lovely smile to present a product. No one expects to receive the girl or the smile when he/she buys the product and noone believes that the product is really better than another, but the presence of that releasing signal automatically induces us to be well disposed to whatever follows. It has been suggested that our automatic responses to innate releasing mechanisms are so strong that they can remain at work even in the absence of the signaling structure, as for example, the idea of courage evoked by broad shoulders in man. even now that with the reduction of hairs the frightening aspect caused by piloerection is no longer produced. The ethologic implications of the skin considered above are prevalently communicative ones. Although there is no evidence of specific behavior connected with skin affections in animals, as permanent or cyclic transformations in external aspect became new signals independently of the causative context and physiologic mechanisms, analogous communicative value of reactions induced by pathologic transformations cannot be excluded. Furthermore, the symptom, whatever its physiologic origins, is a sign of the communicative repertory involving the suffering person and his social environment within which medical semiotics of any type are only a particular communicative code peculiar to the doctor-patient pair. References 1. Eibl-Eibesfeldt
I. Ethology: the biology of behavior. New York: Halt. Rinehart and Winston, 1970.
Address Firenze,
Clinics In Dermatology
\lainardi I). Marson M. Pasquali A. Causationofsexual preferences in the house mice. The behaviour of
mice reared by parents whose odor was artificially altered. Atti Sor Ital Sci Nat Mus Civ Star Nat Milano. 19ti6:104:325-338. Stoddart DM. Mammalian odors and pheromones. I,ondon: Edward Arnold. 1976. Mykytowyck
\kin glands.
R. The behavioural Naturwissenschaften.
Mai 1,. Chemical rommunication pology, ITCLA. 1972:4:57-83.
role of mammalian 1972:59:133-139. in primates.
%ahavi A. Mateselection:aselection Theor Rio]. 1975:5X205-214.
Anthro-
fora handicap..J
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for correspondence: Patrizia Messeri, Ph.D., Istitutodi Via Romana, 17, 50125 Florence, Italy.
London:
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