Fish faking orgasms and other lies animals tell for sex

"The course of true love never did run smooth," according to Shakespeare in A Midsummer Night's Dream. Boy, was he right. There are all sorts of obstacles to a successful relationship, but perhaps there's none bigger than our tendency to lie all the time.

Animals are just as deceitful towards their lovers. The drive to attract a mate, make sure no one else gets near them, and have offspring has driven animals to get up to all sorts of trickery.

Take a female brown trout. Males court her by quivering their trunk muscles, and the most powerful will drive off all the others. While this is going on, the female digs a small bed in the river bottom for her eggs. Then she starts quivering. It looks like she is going to lay eggs, so the male quivers furiously and releases his sperm. But the female does nothing. She has faked it.

It's not clear why the female does this. She might be holding back until more males arrive, either so that she can find a better father or simply to ensure that her eggs are fertilised by multiple males. But it's clearly bad news for the male, who has wasted precious sperm.

Whatever the reason, faked orgasms are just one example of the tricks animals pull on each other during the mating game. From ludicrously overlong courtships to fake eggs, anything goes.

Courting a mate is fraught with uncertainty. Will all of that time and effort be worth it? But while it's bad enough for humans, it's atrocious for Panama's poison frogs. And once again, it's the males that get the worst of it.

Among green and black poison dart frogs, the males alone usually care for the kids: they have reversed the typical sex roles. Studying them in the wild, Dr. Kyle Summers of East Carolina University in Greenville noticed that "they would engage in these very long courtships".

Summers found that female frogs would pursue males through the leaf litter on the forest floor, and lavish attention on them. While a male was presumably looking for a place to deposit eggs, a female would stroke him with her forefeet, nudge him, crouch in front him, and bob up and down. She would even jump on the male, sit on him, and rub her belly against him.

During breaks in this pestering, another female might show up. The original female would then spring into action, alternating between attacking her rival and courting the male even more. The males didn't seem to mind which female they consorted with, but normally the first female would drive off the intruder.

She would then continue to court the male, but only for 20 or 30 minutes before slowing down and apparently losing interest. Then the tables would turn and it would be the male that lavished interest on the female. Eventually, the courtship would end, most often with the female rejecting the male - temporarily. A mate-guarding female would ultimately copulate with her chosen male, but only after a long time.

After hours of watching this, Summers realised what was going on. "It kind of jumped out at me," he says. Females were deceiving males with this "pseudo-courtship", to prevent them from going off with someone else. The game often went on for months.

In other species, the roles are reversed. Among topi antelopes, it is the males that trick the females into sticking around.

Topi antelopes live on the savannahs of Africa. This open habitat gives them a clear view of potential predators like lions, leopards, and cheetahs. So the predators have taken to mounting sneak attacks, and the antelopes must be constantly vigilant.

When an antelope spots a stalking predator, it will almost always give an alarm snort. These snorts may have several functions, says Dr Jakob Bro-Jorgensen of the University of Liverpool in the UK. As well as warning fellow antelopes, it may send a signal to the predator, effectively saying "you've been spotted".

The antelopes must pay attention to the alarm snorts. An antelope that ignored one could end up a lion's dinner. But the importance and power of these messages has opened them up to corruption.

During the two-month rutting season, males show off in arenas called leks. Each male defends a territory about 30m across, where they strut their stuff and display their dung piles to females. The competition is intense, as females are only fertile for one day. A fertile female will visit many males, mating an average of 11 times with around 4 males.

Studying the antelopes' courtship, Bro-Jorgensen noticed that males sometimes snort in alarm when there are no predators around. They are crying wolf, or rather, "lion". Bro-Jorgensen found that these lying snorts were a way of reducing the number of other males a female mated with, by persuading females to stay with him rather than go wandering.

It seems to work. According to a 2010 study, males achieve almost three extra copulations by tricking females into staying. The females can't tell the difference between false and true alarm calls, and males use that to their advantage.

Other species deceive their mates in a different way. Much as some human males like to pretend that certain parts of their anatomy are larger than they are, female long-tailed dance flies inflate the truth.

David Funk of the Stroud Water Research Center in Avondale, Pennsylvania discovered the flies' trick by accident. "I was sitting outside one summer evening at dusk on the patio and I noticed these flies," he says. Funk didn't recognize them, so he netted a few and put them in a jar. It was almost dark, so he waited until morning to take a look. When he did, he noticed that the flies weren't as big and fat as they had been the night before. They were also all female.

Working with Douglas Tallamy of the University of Delaware in Newark, Funk found that the females were temporarily inflating their abdomens with air before gathering in swarms to display to males. "They have a sphincter between the mid- and the hindgut that they close off," says Funk. This allows their abdomen to expand sideways until it is up to four times its normal width. While swarming, the females also position their legs concentrically around the inflated abdomen, accentuating its size.

Why do the females do it? Funk found that they are weak fliers and can't hunt their own prey. They "basically hide out all day," says Funk, and must rely on gifts of food from the males. We're not talking about chocolates: the males bring insects for the females to devour. Males can't force matings, so if there's no gift, there's no copulation.

When a female is reproductively mature, the eggs in her body swell to about ten times their previous size, advertising her status. Males prefer to give gifts to these females, as their eggs can be fertilised straight away. If the eggs are still immature, the female may store his sperm – but she might store several other males' sperm too, reducing the number of her eggs that the male gets to fertilise.

Faced with the threat of starvation, and finicky males, the females have evolved to fake having mature eggs. By inflating their abdominal air sacs, they fool males into thinking their eggs are mature when they're not. This female ruse ensures gifts of food, but often dupes males hoping to get in on paternity.

Perhaps the male dance flies should take some tips from the male nursery-web spider, which has found a way to use worthless gifts to get what it wants.

Female nursery web spiders build a special web where they tend their young. When they find a female, males often wrap up a nuptial gift for her: a delicious insect exquisitely wrapped in white silk. If the female accepts it, she lets the male copulate with her. Males can secure matings without giving gifts, but the copulations are 30% shorter. The longer it takes the female to unwrap and eat the gift, the longer the male gets to copulate.

For the males, gifts are expensive. It takes time and energy to capture and stun prey, transport it, and gift-wrap it in silk. So some males wrap up worthless items, like the remains of already-eaten prey or bits of plants.

Trine Bilde of Aarhus University in Denmark found that in one population, 38% of the gifts are worthless. Even though males with real gifts might get up to 45 minutes of mating, the fake gift still distracts the female for 10 to 15 minutes. That's "long enough that the male actually does get to mate and transfer some sperm," says Bilde.

The females do catch on, but not right away. "The female has to start eating the gift in order to discover what's inside," says Bilde, and the silk wrapping makes that difficult. Males giving fake gifts only get a partial mating, but it doesn't take them much effort either, which is probably why the strategy has survived alongside the honest one.