Sunday 10 January 2021

The Sexy Face-Masks of Lekking Bats

The mating behaviour of mammals is, unsurprisingly, highly varied across different groups and species. We would hardly expect the behaviour of dolphins to resemble that of reindeer, for example, or hedgehogs to resemble cheetahs. Reproductive information is one of the key biological factors we tend to look at when describing a species, even if it isn't quite as easy to evaluate as, say, diet or habitat. (Or anatomy, of course, which doesn't even necessarily require the animal to be alive). Look at almost any write-up of a mammal species in an encyclopedia, and there'll be something on reproduction - assuming we know it.

But, for a great many mammal species, we don't. This may be because it's rare, or difficult to observe in the wild, or perhaps that it's a newly discovered species that we can reasonably assume isn't that different from close relatives we already knew about. But, at least when it comes to reproductive behaviour, one of the biggest gaps in our knowledge concerns the bats.

Bats constitute the second-largest "order" of mammals, after the rodents, in terms of the number of known species. Indeed, we continue to discover new species of bat all the time, so many that it's hard to keep up with just how many there are. Yet they remain relatively little-studied for a group of their size, not least because it's rather difficult to do so. We have reasonably good ideas of where they live and what they eat, but less so about how they behave, and reproduction is no exception.

This is not to say that it's a complete mystery, of course, or that there aren't other, more obscure, groups of mammals, about which we know even less. We know, for example, that bats tend to give birth to only a single infant at a time, much as most primates do, a factor illustrated by the fact that female bats only have two nipples (which, again as in primates, are on the chest). If you're not going to give birth to litters, and even twins are rare, why have more?

It's also possible to obtain basic reproductive information about bats by, well, looking at them. This typically involves "mist nets". Originally developed by 17th-century Japanese hunters, the modern sort are composed of fine nylon threads, making them almost invisible when strung between trees. The bottom part of the net is folded up to form a loose pocket, and when a flying animal hits the net it drops into the pocket, where it gets tangled up. Hopefully, somebody soon comes along to examine it, and then let it free. Such nets are mostly used by ornithologists, but, naturally, they work pretty well for bats, too.

If the bat captured in a mist net is female, we can examine it to see whether it is pregnant or lactating, and, if it's male we can examine the size of its testicles. The latter is relevant since male gonads typically expand during the mating season; there's little point making sperm at times of the year when you're not going to use it. And this information will tell us when that mating season is and when mothers give birth, which, in turn, might give us some idea as to the gestation period. 

What it won't tell you, though, is how suitably interested males and females find another, how they court, or how many sexual partners they typically have. This requires more detailed study of animals in the wild. Clearly, this isn't impossible, but a review in 2000 estimated that this sort of information was known for only about 7% of species. Given that we've discovered something like 500 new species of bat since then, the percentage may well not be much higher now, and quite possibly, it's lower.

Still, given the large number of species in total, even 7% is quite a few in absolute terms. From this, we can tell that the majority of bat species that we've studied are polygynous. That is to say, dominant males mate with as many females as they can get away with and most other males don't get a look in. However, there are exceptions. The little brown bat (Myotis lucifugus), one of the most common species in North America, is sexually promiscuous, with both sexes having multiple partners. At the opposite extreme, the spectral bat (Vampyrum spectrum), the world's largest carnivorous bat, is apparently monogamous. Even among bats that are polygynous, some species, such as the greater spear-nosed bat (Phyllostomus hastatus) physically defend their harem from rivals, while others, such as the vampire bat (Desmodus rotundus) fight one another for the best roosting sites and hope that females will come to them.

The wrinkle-faced bat (Centurio senex) is an unusual bat species found from Mexico to Venezuela, with an additional isolated population on Trinidad, far to the east. It mainly eats soft fruit, although it does have unusually powerful jaws for a bat, that it can use to crack open hard seeds other bats would avoid. It is a phyllostomid, or "leaf-nosed" bat, a group named for the presence of prominent leaf-like structures on their noses that help direct the sonar beam (which is emitted through the nostrils in these species, not the mouth). One of the things that's unusual about the wrinkle-faced bat, however, is that, unlike other leaf-nosed bats... it doesn't have a nose-leaf.

What they do have, as their name implies, is a very wrinkled face. Indeed, the scientific name means something like "elderly centenarian", which gives some idea of what John Edward Gray thought it looked like when he named it in 1842. What's significant for our purposes today, though, is that, in addition to all the wrinkles, males have an extra flap of skin on their chin that's so large they can flip it up with their thumbs to cover the lower half of their face like a mask. Which is kind of freaky, but must surely have something to do with reproduction.

The problem is, the wrinkle-faced bat, for all its oddity, is one of the 93% of bats whose mating habits remain a mystery. That's largely because they're quite rarely seen, living in relatively small, widely scattered groups throughout areas of dense lowland jungle. So there hasn't really been much opportunity to observe any of their behaviour... until recently.

In September of 2018, researchers at the Unversity of Costa Rica spotted a group of 17 wrinkle-faced bats that had chosen to roost together at a site close to one of their research centres. More joined them over the next few weeks, and, perhaps wisely, the researchers decided to simply watch them, rather than doing anything that might disturb them and make them decide to go elsewhere. They eventually left at the end of October, but even so, this is a unique observation for this particular species.

It soon became clear that all of the bats at the roost were male. Except when they went off to feed, the bats simply hung there on the branches, flipping their masks up over their faces for the duration. They weren't fighting one another, just hanging about and making repeating trilling sounds. As soon as another bat happened to fly past, however, they became excited, twitching their ears, loudly beating their wings and pushing their face as far down into the mask as they could, before making long whistling sounds that were so loud and deep in pitch (for a bat) that they could be heard by humans. And then the other bat would leave and they went back to their normal behaviour.

What was all that about? So far as the researchers could tell, on most occasions, that was all that happened. But, one time, the other bat circled round and immediately flew back to the hanging male. The visitor turned out to be female and, after a slightly different series of calls from the male, mated with him before flying off again.

This implies that the male's behaviour had been in some way attractive to the female. The underside of the mask - visible only when it is flipped up - is white, and so likely quite visible to any other bat flying past. The calls are surely also relevant and, for all we know, there could be something scent-based going on that a remote observation wouldn't reveal. The bats did, for instance, sometimes rub themselves against nearby branches, and previous observations have noted a smelly secretion on the chins of bats of this species - and putting a mask over it might actually concentrate such a smell, if only at very short range.

But the other thing that's worth noting about this is that the males were in a group. So the female could have picked any one of them to mate with, and there was no fighting or other visible competition between him and the other males during or after his successful courtship. Wrinkle-faced bats, it seems, don't get jealous.

This is strongly suggestive of lekking. Lekking is quite common in birds and insects, and is also seen in some deer and antelope species, and possibly also sea lions. It is, however, very rare in bats (so far as we know), being known in only one other species. Lekking occurs where a group of males gather together in some area that otherwise has no particular significance, such as a high-quality food supply, and display to attract mates. The females are then entirely free to pick whichever male they like the look of.

For the male, this has the advantage of allowing him to display his genetic fitness and health. In this case, he is losing several hours of valuable foraging time by simply hanging about doing nothing, demonstrating that he can go hungry and still be fit enough to make better calls than his immediate neighbours. For instance, it may be that the final call is so loud, even with the muffling effect of a mask over the mouth, precisely so that the male can show off his prowess.

For the female, the benefit is clearer. She only has to go to one place to meet the maximum number of potential partners, and then gets a free choice among them. That's win-win if you're a bat looking for a one-night stand.

[Photo by "Jplevraud", from Wikimedia Commons.]

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