If the idea of a cold, motionless sexual partner isn't one of your turn-ons, then you're clearly not an echidna. The males of these spiny Australian animals will happily mate with females even if they're hibernating.
Gemma Morrow and Stewart Nicol from the University of Tasmania have spent the last decade studying the short-beaked echidnas of Tasmania. Over that time, they discovered many instances of males mating with torpid females in deep hibernation, or with females who roused themselves briefly only to re-enter their deep slumber. Over the last two years, the voyeuristic duo use a combination of cameras, radio-trackers and infrared motion detectors to get a more intimate glimpse at the bizarre sex life of these animals.
They found echidnas having sex on 26 occasions over the last two years. In 11 of these sessions, the female was accompanied by more than one male and one three occasions, she was with no less than four! Over a third of the females were torpid - slow to react to things going on around them, and with body temperatures of 10 to 29 degrees Celsius. The males, on the other hand, were always active and had the normal echidna body temperature of 32C. When the duo swabbed the genitals of some of the hibernating females, they found that the majority were full of sperm, some of it fresh and often from the same male
Morrow and Nicol think that these sexual habits are the result of extreme competition among males, who have large ranges in a relatively small island. This competition is apparent elsewhere in Australia. On Kangaroo Island, echidnas often form "mating trains", where up to 11 males and females gather together and follow each other around for 2-6 weeks in intense bouts of courtship and sex. On Tasmania, when a male finds a female, he'll mate with her - hibernating or not - and guard her from rivals for some time.
Timing is also an issue. Males and females hibernate with slightly offset schedules so that males rouse from their wintery slumbers about a month before females do. This means that there's a chunk of time every year, round about July and August, where the Tasmanian countryside is rife with randy males and sleepy females.
Bumbling echidna, filmed by me at Tower Hill Game Reserve
As always, it's not all about the males. Morrow and Nicol tracked four of the females who were actively taking part in mating groups, and found that all of them re-entered hibernation soon after. They suggest that this is a ploy on the part of the females, to improve their odds of trading up for a superior mate. Over the winter of 2008, the duo found evidence for this idea by carefully tracking one specific female, surrounding her burrow with cameras and surgically fitting her with an internal thermometer.
She started hibernating in March and during July, she mated at least five times, repeatedly re-entering a state of torpor between her liaisons. On July 15, an ultrasound scan revealed some good news - she was pregnant, with an egg in her womb (the echidna, along with the platypus, are the only two living examples of egg-laying mammals). Echidnas only raise one youngster at a time, but despite already having an egg, the female still mated with new suitors, for Morrow and Nicol kept on finding fresh sperm in her genitals.
It's difficult to explain why a pregnant female would want to slip back into torpor, which would prolong her gestation and slow the development of her foetus. Only one other animals does this - the hoary bat - and in its case, hibernation is used to delay birth so that the new mother doesn't have to suffer the cost of producing milk for its large litter amid the harsh winter. The same argument couldn't apply to the echidna, which only produces one young at a time, raises it in a sheltered nursery burrow, and doesn't spend much energy on milk production.
Instead, Morrow and Nicol suggest that since a female can't do anything about males who try their luck while she is hibernating, she exerts her choice after the fact. By re-entering hibernation, she gives herself time to be found by another male and allows herself the option of abandoning the first pregnancy.
This surreptitious choice on the part of females creates extra competition for the males, at the level of sperm. Successful males aren't necessarily those who manage to mate, but those who ensure that their sperm fertilises the female's eggs - this could be one reason why they seem keen to stick around and guard her for some time after mating.
Intense sperm competition could also explain the male echidna's elaborate genitals. Not only does it have large testicles for its size, but it also brandishes a bendy, four-headed phallus that only uses two heads at a time and ejaculates large bundles of sperm.
Reference: Morrow, G., & Nicol, S. (2009). Cool Sex? Hibernation and Reproduction Overlap in the Echidna PLoS ONE, 4 (6) DOI: 10.1371/journal.pone.0006070
Photo by me, taken at Tower Hill Game Reserve in Victoria
More on animal sex and reproduction:
Why do female seed beetles prefer the sperm of inferior males?
Skinks set their sex in three ways - genes, temperature and egg size
Traumatic insemination - male spider pierces female's underside with needle-sharp penis
