As I’ve mentioned before, I spent a little time on the mudflats of Darwin a while back with Pat Backwell and her team of postdocs and PhD students. Pat invited me to complete a project that had already been started in a previous field season, looking at coercive mating in a very charismatic fiddler crab, Uca mjoebergi, sometimes called a banana crab.
If you’ve spent much time hanging out on beaches or estuaries in the tropics, you may have noticed hundreds of tiny little crabs with one oversized claw waving like mad – a rather peculiar sight. These are the aforementioned fiddler crab, a group of around 100 species that are united by their possession of one tiny claw and one giant Popeye-esque claw.
Males produce these huge claws and wave them around for two reasons: to ward off male competitors and attract females.
Banana crabs dig burrows across the mudflats which they use as shelter when not out foraging and when the tide rises each day to inundate the area. It’s a lot of work digging a burrow so the crabs will defend them from cheeky neighboring crabs that may want to kick them out and take over their sweet pad. Males stop burrow takeovers by first waving at any potential rivals to stay away using their big claw as a signal of strength and willingness to inflict injury if necessary. If rivals do try to enter a male’s burrow, they will use their big claws as weapons and grapple until the eventual loser decides to retreat.
Male burrows are also important real estate because this is where female fiddler crabs hang out after they have mated. Deep inside the burrow they extrude their eggs and wait for the embryos to develop on the underside of their abdomen before they pop up onto the mud flat and release their larval brood on the next spring tide.
Females are fussy about the burrows that they choose to rear their young. Because the burrows are only covered in water for a couple of nights each fortnight it is essential that her babies develop at the right speed so they don’t miss the chance to disperse into the ocean. Burrow width and depth directly influence temperature inside the shaft, such that narrow burrows are warmer and will speed up rate of embryo development in contrast to wider, cooler burrows.
So, just as a male waves to keep rival males away, he also waves to attract females as they wander over the mudflat in search of a mate. If the female likes the look of the male she’ll come in closer for a better look at his burrow by placing her feet at the entrance and checking out it’s suitability for raising her young. Often the female is not satisfied with the burrow conditions and will wander on in search of a better male and a better burrow, sometimes visiting up to 20 males before she finds one she likes.
Normally as the female approaches, the male will go down his burrow and wait for the female to follow him down. If she does enter this is usually a sign that she has given him the go-ahead to mate and will move in for the next couple of weeks.
However, sometimes the male will hang back and awkwardly continue waving at the female next to his burrow while she waits for him to go down the burrow shaft. Usually the female gives up and moves on if the male doesn’t go down the shaft first – but sometimes she will enter the burrow anyway.
At this point, the male will dash down the burrow after the female and trap her inside the narrow shaft. If the female does get trapped below the male, there is a much higher chance that she will stay down, presumably mate with the male, and remain in the burrow to hatch her eggs. In a paper that we published this week in PlosOne, we argue that the alternative male behaviour of entering the burrow after the female has gone down is a form of coercion.
To figure out whether males that trap females had a higher chance of mating success than those that used the more traditional behaviour of going down the burrow first, we tracked females as they went in search of mates on the mud flat. Pat Backwell has been working on a population of fiddler crabs at East Point Reserve in Darwin for a number of years now, and knows just about everything there is to know about them.
When I was visiting in September 2014, Pat had two PhD students and two other postdocs working on fiddler crab behaviour. During the neap tides we would spend our days under umbrellas in the baking heat, armed with binoculars and notebooks as we watched the crabs running around the mud flat.
As females approached waving male crabs, I would observe whether the male entered the burrow before or after the female, and then checked whether the female stayed down with the male to mate. If the female did stay down for a few minutes – a pretty sure sign she would mate – I marked burrows with a little flag and covered it with a plastic enclosure so that after a few days I could dig up the female and see if she had extruded eggs.
We don’t yet know why females would take the risk of entering the burrow first if there was the possibility of getting trapped, but we found a convincing benefit for males: females that entered first were 3 times more likely to stay down and mate with the male, making it a pretty successful strategy for tricky males. 90% of the females we checked later had extruded eggs, suggesting that they did indeed mate after being trapped inside.
So who are these coercive males? We thought that males that “step aside” and wait for a female to enter the burrow first would be of poorer quality, because they may use coercion to mate with females that may not otherwise have chosen them. However, we found no relationship between male body size and the mating tactic he used, nor did we find that small (and perhaps naive females) were those that were ‘fooled’ by these coercive males. One thing we did not check was whether males that step aside have crappier burrows, making coercive mating a way of getting around the problem of not providing the female with a great home to develop her embryos. This is something to look at in future.
Coercive mating has been observed in a number of other animals including insects and birds. Male camel crickets in the USA, for example, use big spines on their hind legs to pin a female down and force her to mate. Check out this video to see how they do it. Although it would be logical to assume that large males with the longest leg spines are best able to restrain females, coercion is actually a small-male behaviour. In this species, like what we predicted for the fiddler crabs, coercion is only done by males that probably wouldn’t have had much hope in attracting females anyway.
Male hihi (stichbirds) in New Zealand also appear to sometimes forcefully copulate with females, during which they pin the female to the ground and mate face-to-face, a unique behaviour among birds.
It’s really, really tricky to actually test the difference between female choice (i.e. she actually wants to stay down in the burrow) versus coercion (she is trapped and would leave if the male didn’t block her passage) in fiddler crabs. Given that mating happens underground we can’t witness any potential struggle between the pair, or if the female may even be using the struggle to test something about the male (like his strength or vigour). So, we may never know for sure if this alternative male mating tactic is truly coercion. What this study has shown is that male fiddler crabs will get up to all sorts of tricks to better their sex lives!