Going Underground

European (or "common") mole

Mammals have adapted to a wide range of habitats and lifestyles, from Arctic wastelands to the deep sea. In addition to taking to the water and to the air, there are a number of mammals that spend almost their entire lives underground. I'm not talking here about living in caves, or digging a burrow to sleep in, but animals that spend their whole lives burrowing through the ground.

There are a number of disadvantages to this lifestyle. You have to constantly dig for one, and your fur and other body parts will get constantly clogged with earth. There is no light, and its difficult to find food or mates. On the other hand, there are also some clear advantages. For one, burrowing animals are safe from most (though not all) predators. Anything small enough to get into their burrows is probably small enough not to want to eat them, and, being underground, they're pretty difficult for anything above ground to find. In addition to that, unless the ground really gets saturated, they don't have to worry much about the rain, and they are protected from extremes of heat and cold.

Although there are a lot of mammals that dig burrows, there are four main groups that have taken the subterranean lifestyle to an extreme. Perhaps the most familiar example are the moles. The mole family consists of forty-one species, although a number of them aren't truly underground creatures, and two of them are semi-aquatic. The group seems to have diverged from its closest relatives, the shrews, not long after the dinosaurs went extinct, and possibly even earlier, making them quite an ancient group. The true underground lifestyle probably evolved at least twice, because the "common mole" of Europe (Talpa europaea) and the "common mole" of North America (Scalopus aquaticus) are not particularly close relatives within the family.

  European      "American"    Star-nosed
& Asian moles     moles       mole, etc.
      ^             ^             ^
      |             |             |
      |             |             |       Desmans
      |             ---------------          ^
      |                    |                 |
      |                    |                 |       "True"
      ----------------------                 |     shrew-moles
                |                            |          ^
                |                            |          |
                ------------------------------          |
                              |                         |
                              |                         |
                              ---------------------------
                                           |
                                     Earliest moles
                                           |

The chart above is somewhat simplified; the "American" moles in fact include one species from China, while the close relatives of the star-nosed mole include some species commonly called "shrew-moles". Brown represents fully subterranean species, blue the semi-aquatic species.

Moles are reasonably widespread, being familiar animals across Europe, much of Asia, and North America. They avoid the colder environments where the ground freezes solid for much of the winter, and so truly subterranean moles are not found in places like Norway or most parts of Canada. They also avoid the deserts, which explains their absence in the Middle East, North Africa, and the central US, despite the presence of two species in the eastern US and three along the west coast. They've never colonised Africa or (less surprisingly) Australia, although there are other mammals with a similar lifestyle on both continents, which I plan on discussing in later posts. Perhaps more surprising is their absence over much of India and in South America; it's not that they dislike tropical environments because there are moles in South East Asia, from Vietnam and Myanmar down to southern Malaysia. For its size, there are also rather a lot of mole species in Japan, along with several species from China, Korea, and the warmer parts of southern Siberia.

True moles are well adapted to their burrowing life. They have powerful front legs with spade-like claws for digging through the earth, and their velvety fur clogs with soil less than that of most other animals would. Unlike bats, which can usually see pretty well when they need to, the eyesight of moles really is quite poor. The European mole (that is, the one we call the "common mole", and which is the only one found through most of Europe north of the Mediterranean) has eyes that superficially appear quite normal, but the cornea is degenerate, and has been compared to that found in humans with the rare visual disorder keratoconus.

Nonetheless, while it prefers to feel its way about with the help of sensitive whiskers and specialised touch receptors on the snout (the ears are also very small, again, to stop them clogging with dirt) the European mole can see, if not very well. The Iberian mole (Talpa occidentalis) of Spain and Portugal, and the eastern mole (that is, the American "common mole", which is found throughout much of the eastern US) are a different case. Their eyelids never open, permanently protecting their eyes from the dry gritty soil of their homelands at the cost of their vision. Still, while the fact that their eyes are permanently shut presumably prevents them from making out any shapes, they aren't completely blind.

The structure of the eyes in Iberian moles has been studied in some detail. The cornea is even more degenerate than in European moles, the iris has no muscle fibres to allow it to widen or narrow in response, and in any event is stuck to the lens, the lens itself has a disorganised structure and is less transparent than in most other animals, and the retina is unusually small. Nonetheless, apart from its size, the retina does look relatively normal, which suggests that it must be at least partially functional. Indeed, Iberian moles do respond to light - by running away from it, which makes sense if you live underground, where there really shouldn't be any.

Nor does the strangeness of moles end with their poor eyesight. In a further bid to stop holes filling with dirt, the female's vagina is sealed shut for most of the year, and only opens when they are sexually receptive. Rather odder, though, is the fact that female moles are, in a certain sense, actually hermaphrodites. This is perhaps rather stretching the term, but it is the case that the ovaries contain a large amount of what certainly looks like testicular tissue - indeed, there's rather more of it than there is ovary. It doesn't produce any sperm, but it does produce male hormones. Of course, all female mammals produce some male hormones - they're made by the adrenal glands - but the female mole produces considerably more than usual.

Eastern (or American "common") mole

This only seems to have been studied in detail in four of the five species of mole found in Europe - the European and Iberian moles, and the Balkan (Talpa stankovici) and Roman moles (Talpa romani) of the Balkans and Italy, respectively. Those four species are quite closely related, having diverged only a few million years ago after their ancestors left Asia, and with their current distributions probably having been heavily shaped by the need to avoid the advancing permafrost during the Ice Ages. But it isn't unique to them, and has also been reported in the star-nosed mole (Condylura cristata), that remarkably distinctive beast of the eastern US and Canada, and, for that matter, the Japanese mole (Mogera wogura) - although, not, apparently, in the eastern mole.

Quite what the point of this is is a little unclear, although the glands do shut down during the breeding season and when the female is pregnant. Being awash with male hormones for the rest of the year though, does lead female moles to develop some masculine anatomy as they grow; they have an enlarged clitoris, and what appears to be a prostate gland. None of this hampers their ability to be good mothers, though, because moles have a higher reproductive effort (that is, the mass of offspring one mother can produce in her lifetime) than their closest relatives, the shrews. This seems to be due, at least in part, to the production of some very nutritious milk, and may offset the high death rate of young moles when they leave home and make the dangerous journey above ground to find somewhere to establish their own burrow.

They have to make their own burrow, because moles are pretty anti-social animals, and adults normally only meet up to mate. Having said that, they don't need particular large burrow systems, so there can be several moles in a relatively small area. Population densities of 5 to 25 moles per hectare have been reported for the European mole, and 5 to 12 for the eastern mole. Moles, of course, are mostly carnivorous, eating insects and worms, largely, it would appear, by hoping that they accidentally wander into the tunnels.

While the less subterranean members of the mole family are basically nocturnal, its a little more complicated for the true moles. Day and night aren't really an issue for them, and they sleep three times each day for most of the year - although males can be active for rather longer periods when they're looking for a mate.

Because of the protection that hiding below ground offers them, and the fact that they generally don't mind agricultural land, most mole species are not overly threatened by human activity - which isn't to say that farmers don't poison them, just that they don't do it enough to place entire species at risk of extinction. The clearest exception is the Echigo mole (Mogera etigo), which lives in only one small area on the west coast of Japan's main island, Honshu. It prefers soft soils, and changes in agriculture in the region make those less common than they used to be, and the animal is officially considered Endangered.


[Pictures from Wikimedia Commons. Cladogram adapted from Mikko's phylogeny archive and Motokawa 2004]

Endangered Cats of the High Andes

A few weeks ago in the UK, we had the 10-yearly treat of filling in our national census forms. Once all the information from these forms is collected, we will have an official figure for the number of humans living in our country. Unfortunately, finding out the same figure for wild animals isn't quite so easy. Yet studying the population densities and numbers of wild animals is often of more than academic interest. A great many species are endangered, and without accurate ideas of how many of them are, we can't tell how endangered they might be, what strategies we might have to use to protect them, and whether or not those strategies are working.

Of course, animals can't fill in census forms, but there's more to it than that. If the animal lives in large, highly visible herds, it may not be so difficult - although even there, you have to be sure you're not counting the same animal twice, and that you're picking a suitably representative area to study (since, realistically, you're not going to go out there and do a head count of every such animal in existence). But many animals aren't so obliging. They may be small, they may actively hide from humans, they may be nocturnal or crepuscular, or they may just live somewhere its hard to get to, or in a jungle so full of plants its hard to spot anything. The rarer they are, the harder it becomes to find them, and yet those are exactly the ones we're most interested in.

Horns of the Thunder Beasts

Megacerops, one of the largest brontotheres

Today, the group of odd-toed ungulates - those large mammalian herbivores that support most of their weight on their middle toes - is represented by just sixteen species in three families: the horses, rhinos, and tapirs. But they were once much more extensive, with whole families of animals that didn't make it through to the present day. One of these was the brontotheres, a family whose name literally means "thunder beasts".

These were big, heavily built animals, some of them standing over six feet tall at the shoulder. In many respects, they would have looked quite like rhinos, having a rather similar body-shape, and crucially, large blunt horns on their snout. However, the horns weren't really so rhino-like as they appear, since the horns of rhinos are actually made of compacted hair, while those of brontotheres were made entirely of bone. The surface of the horns are rugged, suggesting that they were probably covered in skin during life, which perhaps makes the closest living parallel the projections on the heads of modern giraffes.

In the grand scheme of things, the brontotheres didn't last very long, dying out around 34 million years ago, but they must have been very impressive animals when they were alive. Despite their appearance, they seem to have been more related to horses than to rhinos. This is more apparent when you look at the very earliest brontotheres, which were relatively small and hornless, and do look rather more like the early multi-toed ancestors of the horses.

Muscular Jocks and Randy Nerds - the Sex Lives of Wild Guinea Pigs

Brazilian guinea pig

The domestic guinea pig (Cavia porcellus) is a fairly familiar animal, but they've changed enough in the 5000 years of their existence that we don't actually know quite what they were domesticated from. There are at least five species of wild guinea pig alive today, and while one of them was presumably the origin of the domesticated form, we don't know which it is. In addition, the guinea pig family includes eight other species with a fairly similar appearance, and three that are manifestly different, including the largest living rodent, the mighty capybara.

The guinea pig family therefore represents a fairly diverse group of South American rodents, adapted to a wide range of different habitats, and found across much of the continent. Considering that, by the standards of rodent families, there aren't very many species in the group, and that, with a few exceptions, they don't look all that different, its perhaps surprising just how variable their behaviour is. That's largely because they have adapted to so many different environments; there are forest dwelling species, a couple of semi-aquatic forms, and others living in mountains, deserts, and grasslands. The different ways that these species behave was the focus of a couple of recent reviews in the Journal of Mammalogy.

Guinea Pigs    Mountain    Yellow-toothed     Rock      Capybara
                Cavies         Cavies        Cavies
     ^             ^              ^             ^          |
     |             |              |             |          |
     |             |              |             |          |
     ---------------              |             ------------
            |                     |                  |
            |                     |                  |
            -----------------------                  |
                       |                             |
                       |                             |
                       -------------------------------
                                      |
                                      | 

The Brazilian guinea pig (Cavia aperea) is one of the ones that might be the wild ancestor of the domesticated animal. It prefers savannah with plenty of long grass and undergrowth. They are moderately sociable animals, where males live in a stable home range with one to three females. (One suspects those with a single partner just haven't been able to find any others, rather than having a preference for monogamy). Obviously, this means that there are some males left over, and these, which are generally younger and smaller individuals, wander about quite widely, although never too far away from the mated groups - presumably waiting for the male to die, or at least weaken.

As you might expect, this leads to quite a bit of violence between the males, and if you keep them together in captivity, they will try and kill each other. The females, on the other hand, tend to ignore each other, although males have been seen trying to break up fights between their partners. All of this means that males are quite effective at ensuring a female's pups are their own. As a result, Brazilian guinea pigs have evolved so that males are noticeably larger than females - their primary means of passing on their genes is to beat up their rivals, and for that, you need to be large and muscular.

The greater guinea pig (Cavia magna) lives in regularly flooded wetlands, and isn't a strong contender for the ancestor of the domestic forms, not least because it has webbed feet and enjoys swimming. Unlike the Brazilian guinea pigs, they don't seem to stick to a home territory, possibly because they can't predict when the ground is going to be flooded. Indeed, they are relatively antisocial for guinea pigs, largely ignoring each other and wandering about on their own. In their fast-changing environment, males have to mate with whatever females they can find, but they also need to fight off rivals, and so the males are larger and more muscular.

The common yellow-toothed cavy (Galea musteloides) has a third tactic. Although there is apparently some debate on how they live in the wild, they generally seem to be quite sociable, with several males and females living together, and communally raising their young. There is a dominance hierarchy, with an identifiable alpha male, and we might therefore expect that, as with the Brazilian guinea pigs, the males would be bigger, to fight off their many rivals. But they're actually slightly smaller and weedier than the females, and that's probably because of the way the females behave.

When they are ready to breed, the females get very excited, and dash about all over the place, something that the males notice quite quickly. Eventually one of the males will catch her, and mate, but that isn't enough for the female, who will immediately start running around again until another male manages to catch her. She often doesn't stop until everyone has had a go (and usually more than once each), which makes male dominance a bit pointless. There isn't much purpose fighting off rival males if it's the female that calls the shots, especially if she's going to mate with everyone else no matter what you do.

So, if they can't fight off rivals, how do the males ensure that they sire the most offspring? Well, they might not be able to out-compete rivals in physical combat, but they can try to do it sexually. Relative to its body size, the common yellow-toothed cavy has amongst the largest testicles of any mammal. In fact, they are about three times the size of those of Brazilian guinea pigs. As with most mammals, they shrink dramatically outside the breeding season (you'll probably have noticed that humans don't have a breeding season...), but that's par for the course. The individual sperm cells are also smaller, and less likely to be damaged, which means that not only can they produce a large quantity of the stuff, but it contains more healthy sperm for a given volume. If you can't beat your rivals with teeth and claws, you can try and do it by producing more, and better, sperm.

Capybara - a 140 pound "guinea pig"

What of the largest rodent of them all, the capybara (Hydrochoerus hydrochaeris)? As you might expect for something weighing 140 pounds, capybaras don't look that much like guinea pigs, and they were once thought to belong to a different family altogether. Nonetheless, genetic analysis has shown that they are, in fact, gigantic, semi-aquatic relatives of the rock and climbing cavies.

They live in herds, which can, at times, reach quite large numbers. The females in a herd tend to breed at around the same time, so that their young are born together, and can be raised in a nursery group, with all the females cooperating. Their testicles are not particularly large, and, when examined under the microscope, seem to have a high number of testosterone producing cells, rather than sperm-producing ones. That suggests that, despite the large number of potential rivals, breeding males can be confident nobody else will get at their females, and that they would rather divert their energy into being larger, muscular, and generally more aggressive.

Which is what we see; the males are larger than the females, and establish a clear dominance hierarchy, with an exceptionally large alpha male controlling access to the females. He isn't perfect at this, of course, and younger males do get a look in from time to time, but he does have a few advantages on his side. Females are only receptive to mating for a few hours at a time, which gives the male the chance to stand guard, and courtship and sex last around ten minutes - quite long enough for the alpha male to step in and put a stop to anything he doesn't like the look of.

Many other species of guinea pig show variants on these themes, with, for example, the southern mountain cavy (Microcavia australis) showing sperm competition, and having correspondingly large testicles, and the rock cavy (Kerodon rupestris) fighting off rivals. But there is a third way.

The Muenster yellow-toothed cavy (Galea monasterensis) was only identified in 2004, and is only known from one small location in Bolivia. In experiments, when females are given a choice between two or more males, they pick one and stick with him, largely ignoring the others. After they have been together for some time, if the female is removed, the male becomes stressed, and he visibly becomes much happier if she is returned. In short, the species appears to be monogamous.

The males are no larger than the females, since any potential rivals are likely to have mates of their own, so there's no need to fight them off. But equally, they don't need large testicles or increased sperm production, because the female is likely to be faithful. Significantly, and quite unlike the aggressive common yellow-toothed cavies, fathers of this species help to raise their young, something that makes sense in a monogamous partnership where you can be sure the child is your own. This may be explain why the behaviour evolved; Muenster yellow-toothed cavies inhabit the Andes mountains, where food is scarce, so having two adults to look after the young may well be advantageous.

Cooperation, for this species, beats sexual competition.

[Pictures from Wikimedia Commons. Cladogram adapted from Dunnam & Salazar-Bravo, 2010]