By Matt Walker
Editor, Earth News
Bees carefully select mates
In the fading light, a male moves past a female and catches the whiff of her fragrance.
The scent catches his attention. He turns, sensing she may be the one he has spent his life searching for.
He follows her trail, eager to impress.
What he has detected in these few moments - from this haze of pheromones - is not that the female is his soul mate, a potential life partner, or someone to captivate his mind. But that she is a virgin.
The amorous male meadow vole is not the only creature to use this technique; brown lemmings do it, lizards do it, even beetles, spiders and bees do it.
Scientists are just now discovering how important smell may be to courting animals.
Many males are able to "smell" whether a potential female partner is a virgin, and if not, how many times she has mated.
This is according to a paper published this month in the journal Biological Reviews.
Male meadow voles judge the opposite sex
Male brown lemmings (Lemmus sibiricus) much prefer the odour of virgin females to that of females that have just copulated.
It seems that the males use scent as an indicator, and that virgin females smell very different from those that have had multiple partners because they produce very different chemicals.
Even the insect world is heady with the aromas of sex. Mated female leaf miner flies (Agromyza frontella), for example, express their status by producing lower levels of an aromatic chemical called 3,7-dimethylnonadecane than unmated females.
And across bee species, mated females appear to express a chemical that virgin females do not.
There have been few direct studies of the strange effects of odour of sexual behaviour. Most have been based on insects, according to evolutionary biologist Dr Melissa Thomas of the University of Western Australia, Crawley, who has published the latest review.
But those studies that have been done suggest that smell may be crucial for the successful reproduction of many species.
Animals, it seems, secretly waft the scent of their sexual status in three ways.
First, after meeting, female animals may produce a scent that repels other males.
Second, females may actually stop emitting male-enticing pheromones after they have mated.
This occurs in the gypsy moth, so the pregnant female can flutter away without being pestered by other amorous males (Lymantria dispar).
Lastly, males can actually apply chemicals to females while mating with them - sneakily rubbing on perfumes that deter rivals from later mating with "their" female.
When fruit flies (Drosophila melanogaster) mate, the male transfers a chemical called 7-tricosene to the females. This is the only known example of pheromones being passed between the sexes by simple bodily contact.
In other species, the transfer can be much more intimate.
In some moths and butterflies, for example, pheromones in the male's ejaculate "switch off" the calling behaviour of receptive females. While a chemical in the male fruitfly ejaculate renders the females less attractive to new suitors.
And one insect, the bee Osmia rufa, actively attempts to influence the mating game after copulation. After mating, the male bees appear to rub the female's wings, coating them in a substance that marks the females out as virgins no more.
Benefits for all?
Why males go to such lengths to determine which females are virgin, and then mark those that have been mated, depends on the mating system of each animal.
In monogamous animals, which only have one mate at a time, using pheromones to signal a female's status is good for both sexes.
It means males do not have to waste time searching for females who may turn out to be unreceptive, while females do not get harassed by many males at once.
In animals where multiple males may copulate with a female, finding a virgin has obvious benefits, including that his sperm will not have to compete with that of his rivals.
For the females the benefits are less clear. Being marked out as an unacceptable partner could prevent her finding the best mate, or even receiving nuptial gifts from courting males.
And often the changes are permanent.
After mating, female corn mealworms suffer a significant drop in the emission of pheromones they emit to attract males.
The levels rise again during each day that passes, but they never again reach the levels expressed by virgin mealworms.
Some animals can go even further than smelling whether a female is a virgin or not.
Amorous male meadow voles can tell how many partners his potential fragrant partner has copulated with, all by her smell and that of rival males nearby.
That may be an extreme example of an animal "judging" another's sexual history.
But when it comes to romance, among animals, the mating game has a whiff of the weird about it.