Communication is fundamental for the survival of all living beings. The exchange of information occurs through the transmission of mechanical or chemical signals or by emanations that stimulate one or more sensory channels of the recipient individual. Chemical signals are the oldest and most widespread method of communication in the plant and animal kingdoms. The first research on this subject was carried out in insects and demonstrated the presence of some chemical signals that differed from those involved in chemotaxis and the perception of smell and taste.
Studies carried out at the beginning of the 1960s identified and classified a large number of substances excreted into the external environment which were able to modify the physiology and/or behaviour of the recipient subject. These substances, perceived by the main and accessory olfactory systems, can convey messages directed at individuals of the same species or of different species: those with an interspecies action are defined allomones when they give an advantage to the individual that emits them (for example, defensive secretions) and kairomones when the benefits are destined for those receiving the substances (for example, the emission of terpenes by diseased conifers that signal to some insects the presence of a vulnerable tree). Substances with an intraspecific action, which involve the same species, include the pheromones (from the Greek φερέιν = to bear and ωρμάο = to stimulate, excite). Communication through pheromones is not only a feature of insects, but is also widely used by fish, reptiles and mammals. Among the mammals, carnivores are the animals endowed with the greater number of pheromone-producing structures.
The set of neurophysiological mechanisms involved in the secretion of pheromones is still poorly understood. According to P. Pageat the pheromones intervene, thanks to the involvement of the hypothalamus, in hormonal secretions, influencing in particular the production of sex hormones. Furthermore, they seem able to provoke emotional changes which underlie different behavioural responses (for example, avoidance, flight or aggression) depending on changes in the reaction status of the individual.
SECRETORY STRUCTURES
The production and secretion of pheromones are involuntary. In mammals they are excreted from various glandular structures distributed in the epidermis and mucous membranes around the natural body orifices. The main secretory structures in the dog are the sebaceous glands in the intermammary sulcus, the perioral glands (spread across the chin, lips, skin of the muzzle near the vibrissae and the cheeks), the ceruminous glands in the auricle, the anal glands (which include the circumanal hepatoid glands, the sebaceous glands in the cutaneous part of the anus, rectal mucosa and para-anal sinuses), the subcaudal glands (on the ventral surface of the base of the tail) and the footpad glands (spread in the plantar footpads and in the skin of the interdigital region). Furthermore, there are pheromones, called pheromones of adoption, which appear to be present in solution in the amniotic fluid, in the saliva, in the urine (social micturition) and in the faeces (social defecation).
CHEMICAL COMPOSITION
The chemical composition of pheromones has not yet been determined. Most of the components that have been identified so far are simple organic compounds such as carboxylic acids, alcohols, aldehydes, ketones, amines, steroids and terpenes. The central message is given by three components: oleic acid, palmitic acid and linoleic acid. These are associated with other elements that differ from one species to another and which are indispensable for the action of the pheromone. It has proven very difficult to reproduce the effects of the complete secretion in the laboratory by using some of the active components because the composition of pheromones depends on the species, the individual, its physiological state and the situation. Pheromones are secreted in the form of precursors (pro-pheromones) which are often inactive. As a result of chemical reactions (for example, esterification or hydrolysis) brought about by saprophytic bacterial flora on the skin, the pro-pheromones are activated by their transformation into pheromones. The pheromones can be emitted together with proteins or in a free form.
A protein carrier has been demonstrated in rodents and the rabbit. The existence of binding proteins in carnivores has not been unequivocally confirmed even though the binding proteins in rodents and the rabbit show numerous structural analogies with the protein called Feld 1 in the cat and with the homologous Canf 1 in the dog, both proteins produced by the sebaceous glands of the skin. The production of Feld 1 and Canf 1 is greatly increased in seborrhoeic skin disorders of the dog and cat. Feld 1 is not only the major allergen produced by the cat, but is also responsible for 85% of the allergic reactions in humans and animals. The biological function of this protein is controversial. It is possible that it binds some steroids (as occurs for other proteins) or that it is involved in the synthesis or transport of the steroids themselves. Feld 1 is produced by the sebaceous glands in the area of the cheeks, in the anal sacs and in the interdigital region of the cat (sites in which the pheromones involved in marking behaviour are produced. Spectrofluorimetry has demonstrated that Feld 1 is capable of binding to the fatty acids that make up the pheromones of the cat (above all to the fatty acid most present in F4) and to the steroids responsible for sexual communication. This protein could, therefore, play an important role in the chemical communication of the cat.
PERCEPTION
Pheromonal secretions can be transmitted through air or water or deposited on the ground or solid supports. Although they have particular olfactory characteristics, they do not act only as olfactory stimuli and cannot, therefore, be considered simple scents. Formed of volatile substances, like the true odorous molecules, they reach the olfactory organ in currents of air. In terrestrial animals they are perceived above all through the olfactory channel and, to a lesser degree, through taste. In mammals there are two pathways enabling access of the molecules to the olfactory organ: the nasal pathway and the retro-nasal pathway. The nasal pathway is involved during inspiration, whereas when the retro-nasal route is involved, the air reaches the olfactory organ during expiration and, when there is food in the oral cavity, contributes to the perception of taste. The real odorous molecules, transported by the cilia immersed in mucus, bind to receptors in the olfactory mucosa which transmit information to the olfactory bulb and to the dorsomedial and ventroposteromedial nuclei of the thalamus from which the impulses to the prefrontal cortex and the somaesthetic area depart. The integration and interpretation of the olfactory profile occurs in these latter structures. The pheromones follow a different pathway, involving the accessory olfactory system.
The vomeronasal organ or Jacobson’s organ seems to be the structure most involved in the perception and recognition of pheromones. The vomeronasal organ is formed of paired ducts on the floor of the nasal cavity that open into the incisor canal. The organ is poorly developed in humans at birth and seems to atrophy subsequently. The perception of pheromones in Artiodactyla (Ovidae, Bovidae, Cervidae), in Perissodactyla (Equidae) and in carnivores occurs through the Flehman or lip-curl response which consists of raising the upper lip with the mouth half open in inspiration, completed by licking and wrinkling the truffle in the dog and by tongue movements in the cat. These facial movements cause upward traction of the upper lip which is followed by the opening of a cartilaginous operculum that partially covers the incisor meatus.
Pheromones, which are not soluble in water, bind to proteins (pheromone-binding proteins) dissolved in the mucus produced by the glands adjoining the vomeronasal organ (there are specific proteins for most of the known pheromones). By binding to these proteins the pheromones can reach the olfactory receptors which are immersed in a hydrophilic environment. The electrical impulses generated by the receptors travel along the vomeronasal nerve, reaching the accessory olfactory bulb and from here pass to the limbic system. Some pheromones do not, however, trigger the Flehmen response, while others are perceived contemporaneously by both lip-curling and the nasal pathway. Many authors believe that some pheromonal molecules, particularly those present in anal and vaginal secretions, are perceived through the involvement of gustatory cells.
CONCLUSIONS
In the coming years, progress in scientific research will enable the identification and functional analysis of an ever greater number of pheromones. Some of these could be used in the auxiliary treatment of behavioural disorders. Pheromone therapy is, therefore, destined to play a role of considerable importance in behavioural medicine.
Suggested readings
- Borsa F. «Lezioni di fisica e biofisica medica », 3° edizione, La Goliardica Pavese, 1980;
- Clement M. G, Chiara O. «Compendio di fisiologia 2 », Società editrice Esculapio, 1983;
- Coupry V. «L’attaccamento primario è indispensabile per la sopravvivenza », La Settimana Veterinaria, n° 361, 23 ottobre 2002;
- D’ancona U. «Zoologia », Unione Tipografico – Editrice Torinese, ristampa della terza edizione, 1981;
- Gaultier E. « La communication canine», 3° cycle professionnel des Ecoles Nationales Vétérinaires, Ecole de Toulouse mai 2000;
- Michel G. «Embriologia degli animali domestici », Edi. Ermes, 1980;
- Nickel R, Schummer A, Seiferle E. « Trattato di anatomia degli animali domestici II», Casa editrice ambrosiana Milano, 1979;
- Pageat P. « La communication chimique dans l’univers des carnivores domestiques », Le Point Vétérinaire, vol. 28, n° 181, février 1997;
- Pageat P. « Patologia comportamentale del cane », Edition du Point Vétérinaire, 1° edizione, 1999;
- Pageat P. « Les phéromones d’attachement », Pre – congrès Mondialvet, Lyon 1999;
- Pageat P. « Bases biologiques de la psychodermatologie: exemple du chien », Veto – Alp 2002, Chamonix;
- Stayer L. «Biochimica », Zanichelli, seconda edizione, 1989;
- Vadurel A, Gogny M. « L’odorat du chien: aspects physiologiques et facteurs de variation», Le point Vétérinaire, vol. 28. n° 181, février 1997;
- « Cours de Base du GECAF », Strasbourg 2001.