Pigs, people and fish
When a boar is sexually aroused or displaying aggression, characteristic chomping jaw movements cause the secretion from the submaxillary gland of a viscous, frothy saliva with a repugnant odour 38. The boar snorts and blows the saliva close to the head of the sow. If she is receptive (because she has ovulated recently), she will adopt an immobile mating stance, which is known as "standing" and mating follows. In traditional farming practice, a "teaser boar" is used to detect "standing", in preparation for the expensive services of a stud boar. Saliva production is an important component of the mating ritual, although it is not essential because highly receptive sows will "stand" in response to the sound of the boars snort alone 39. Surgical removal of the submaxillary glands of the boar causes loss of libido and passive behaviour.
Photo courtesy of Five Tigers (Tiger food!)
The semiochemically active components of the saliva are androstenol 13 which has a musky odour and androstenone 14, which has a urinous odour and is present in smaller amounts 40 41. The proportions are age dependant and they are produced in the testes 42. Both are capable of eliciting the "standing" response and sow saliva contains only small amounts of these steroids. A mixture of androstenol (13) and androstenone (14) in an aerosol can (Boarmate ®) is used to detect ovulation as an alternative to "teaser boars". Androstenone (14) 43, skatole and to a lesser extent indole 44 45 are responsible for the unpleasant smell of cooked boar meat 46.
The remarkable aphrodisiac effect of these steroids on pigs led to a search for them in the vertical pig - man. The most likely site for pheromone production in man is the axillae (arm pit). This has a particularly high concentration of apocrine glands, which only become active with the approach of puberty. Androstenol (13) 47, and androstenone (14) 48 49 were detected in human axillae sweat, saliva, urine, semen and the blood stream 50, but only in trace amounts. The predominant steroid in axillae sweat is dehydroepiandrosterone sulfate 15 51. Many other steroids are secreted onto the skin as sulfates and glucuronides which are cleaved by bacteria to "free" steroids 52. The synergistic relationship between animals and bacteria is best exemplified by the observation that the human body contains more bacterial cells than human cells; albeit human cells are much bigger. The vast majority of these bacteria are located in the gut, in consequence up to 20% of the dry weight of human faeces consists of bacteria.
There have been many attempts to show that the pig pheromones affect human behaviour, but it is difficult to obtain convincing data and to interpret it. In one experiment; toilet cubicles in men's and women's toilets were sprayed with androstenol (13). Men avoided the treated cubicles, but women were unaffected 53. In another experiment female students exposed overnight to androstenol, participated in more social exchanges with men the next morning, whereas men treated similarly were unaffected 54. Although these results are interesting they do make a compelling case for a pheromone-like response to these steroids in man.
It is notoriously difficult to show that humans respond to pheromones at all. The much quoted McClintock study apparently showed that women in living together in dormitories synchronised the onset of their menstrual cycles and that women who had more contact with men tended to have shorter cycles 55. In the context of the behaviour of other primates, this is wholly reasonable, however although two studies confirmed these findings 56 57 a further two did not 58 59.
The putative steroid pheromones 13, 14 are also found in plants, but their roles in communication (if any) are unclear. Androstenol (13) is found in the ultimate delicacy, truffles, and this is why pigs are able to locate them, even when they grow up to half a metre below ground level 60. Caviar, celery and young parsnips also contain androstenone (14) 61, as do many of the exotic foods prized by epicureans 62. Even though excesses of these steroids smell unpleasant, humans respond favourably to them in small amounts. The African civet cat (Civettictis or Viverra civetta) has urogenital sacs which produce a marking secretion called civet. The secretion has a highly unpleasant faecal odour, but when diluted it is has a pleasant odour and is highly prized as a constituent of expensive perfumes.
In discussion of the presence of steroids in the axillae it is frequently assumed that these are responsible for the unpleasant (locker room) odour of the unwashed. In fact, the major malodorous component of armpit odour 63 is trans-3-methyl-2-hexenoic acid 16 64, which is found in the axillae of both males and females 65. At one time it was thought to be the characteristic smell of schizophrenics 66.
The detection of steroids which have pheromonal activity in pigs, in trace amounts in humans and vegetables might not occasion too much interest, but similar steroids are also major pheromones of fish 67. These are frequently released as glucuronides or sulfates in the urine and as free steroids from the gills 68.
The existence of chemical signals between fish was demonstrated as long ago as 1932, but it is only in the last ten years that the compounds responsible have been identified. The systems employed are best exemplified by the goldfish, which has been studied in the most detail. Goldfish do not have defined territories, are promiscuous and have no parental behaviour. By human standards they are paragons of political incorrectness! The females spawn amongst vegetation and are followed by a small shoal of suitors who fight to get close enough to fertilise the eggs. About 10 hours before spawning, female goldfish start to produce large quantities of a constellation of steroids 17abc, 18abc, 19ac, 20. These promote oocyte maturation and when released into the water, increase gonadotropin levels in males. This in turn promotes the formation of milt (seminal fluid and sperm) in males and increased intermale aggression during spawning 69. Oocycte final maturation is induced by the dihydroxypregnenone 17a, whereas the most important pheromonal components are the free and sulphated di- and trihydroxypregnenones 17ab, 18ab and androstendione 20 70, which are detected by the medial portion of the olfactory bulb 71. Androstendione (20) blocks the milt and gonadotropin promoting effects of the dihydroxypregnenone (17a), but the biological relevance of this is unknown at present.
Another intriguing fish pheromone is prostaglandin-F2a (PG-F2a 21a) which circulates in the blood stream of female goldfish and is associated with follicular rupture and ovulation. When it is released into the water together with a metabolite, 15-keto-PG-F2a 21b, it induces increased (but short lived) aggression amongst males and courtship behaviour 72. As prostaglandins are normally short range and short lived effectors, it is astonishing to find them being used in this way.