Sunday, 5 October 2014

Mini-Monkeys: Monkeys with Manes

Golden lion tamarin
The tamarins of the Amazon jungle and the forests bordering it to the north are sometimes known as "true" tamarins, to distinguish them from their relatives further south. Even when the marmoset family was first recognised as distinct from those of other South American monkeys, and all marmosets were placed into a single genus, the tamarins were already divided into two: the "true" tamarins in the north, and the lion tamarins in the south.

More recent molecular analysis, of the sort that also showed the clear difference between the Amazonian and Atlantic Forest marmosets, has shown that our initial instinct on the tamarins was correct. Indeed, it seems to be the case that lion tamarins are actually more closely related to marmosets than they are to other tamarins, something that makes the distinction unavoidable. Having said which, there's no dispute that, anatomically, they look much more like tamarins than they do their apparently closer relatives.

What this means is that it's the tamarins, not the marmosets, that most likely resemble the original members of their family. The marmosets are specialists, having changed further from their ancestor's body form because of their heavy reliance on gum as a food source, and the need to modify their teeth, jaw muscles, and bowel structure to accommodate this odd diet. Lion tamarins, which never did that, retain the original "tusked" teeth and fruit-digesting colons of their ancestors, just as true tamarins do.

Originally, we thought there was just one species of lion tamarin, the golden lion tamarin (Leontopithecus rosalia), distinguished from the true tamarins by a larger size, a different habitat and, of course, by living outside the Amazon. A close look showed that the different "subspecies" of this animal lived in entirely separate regions, never met up with one another, and, moreover, were easy to tell apart just by looking at them. It is now universally accepted that this is because they are different species. They are all physically rather similar, which suggests that, in evolutionary terms, they may not have split apart that long ago, but it seems  that they diverged during the Ice Ages, when the tropical forests shrank and fragmented, and they don't live apart just because we humans have chopped down the trees in between.

Even today, golden lion tamarins remain the best known, and the best studied, of the four species. They are clearly distinctive animals, with rich golden fur over their entire bodies, except for the face, and a thick mane around their heads. They are also large; while they're still quite a bit smaller than any other monkey in South America, they weigh about 700 to 800 g (25 to 28 oz.) as adults, which is at least half again the weight of most true tamarins. It's the females, incidentally, that are the larger of the two sexes.

Lion tamarins live in the Atlantic Forest, the coastal tropical to subtropical area of woodland that occupies Brazil's south-eastern coast, and that is separated from the Amazon by the sparser, savannah-like, Cerrado. More specifically, they are found along the coasts, inhabiting only lowland forests, rather than the higher forests further inland. The golden lion tamarin is the most southerly of the four species, living only in a very small patch of subtropical coastal forest just north of the Tropic of Capricorn.

They are restricted to such a small area - probably not much more than 100 km2 (40 square miles) - due to a combination of human activity, and having very specific needs when it comes to habitat. Their wild population numbers only around a thousand individuals, and while a herculean conservation effort over the last few decades means that that's now pretty stable, it isn't exactly a lot. As a result, they are still considered an endangered species... as are all the other lion tamarins.

So what are those requirements that they're so picky about? For a start, they inhabit only lowland forest, no more than 300 m (1000 feet) above sea level. They do their foraging, mostly for fruit and insects, in the higher parts of the forest canopy, which means that they need lots of tall trees. In order to get the food and shelter they need, those trees have to have lots of hanging vines and, in particular, tank bromeliads, flowering plants that grow only on tree branches and have tightly clustered leaves that collect pools of rainwater that encourage the tamarins' prey.

They only like sleeping in tree hollows at least ten metres (30 feet) above the ground,, although they will make do with vine tangles or the like if they absolutely have to. And, while they often tend to sleep on low hilltops, they do like being close to water, whether it be rivers, or, more often, swampland. They rely heavily on fruit for food, eating over fifty different kinds, and, somewhat unusually, particularly like to drink the nectar of the tree Symphonia globulifera. In some parts of their habitat, there is so much fruit that they can afford to spend as little as two or three hours a day foraging, mostly in the morning and evening, leaving at least seven hours of daylight free for lazing about and socialising.

Golden lion tamarins live in stable family groups, with a single mated pair and up to eight children (although three is more usual) that have yet to up sticks and leave home. Leadership of the group changes every three years or so, but typically only when the existing adult male dies; actual take-overs by intruders are apparently rare. Because of their strict requirements, once a group has found a suitable place to live, they are determined in defending it from outsiders, although for the same reason, they don't have to travel far, with home ranges of just 45 hectares (110 acres) in the richest forests. Interestingly, while they do use scent marking to indicate the location of food resources, they don't seem to do so to stake out their territory, as many other monkeys do. When they do clash, it seems to be rival females that do most of the fighting, which may explain why they're stronger than the males.

In about 90% of groups, the mated pair are strictly monogamous. This, however, does not seem to be maintained in the same way that it is in other tamarins, where hormones from the dominant female prevent her subordinates from being able to conceive. In lion tamarins, in contrast, the younger females in the group are all perfectly fertile, and even synchronise their ovarian cycles. However, they simply choose not to mate - presumably because, given the stable nature of the groups, the only males available are their father and brothers. Subordinate males, for their part, may show some degree of reproductive suppression, having low testosterone levels even when among females to whom they are not related - possibly, acting less masculine means they are less likely to get beaten up by the dominant male.

Black lion tamarin
Lion tamarins give birth primarily in the wet season, although sometimes, they can rear two sets of infants in a year. Pregnancy, at 125 to 132 days, is rather shorter than in other marmoset and tamarin species. The mother also looks after her children for rather longer, not immediately handing them on to others, but, by a few weeks of age, everyone is joining in with the caring. A particular feature, compared with other non-human primates, is that, once they start taking solid food, everyone joins in in feeding them, especially giving them food that might be difficult to find or to process prior to eating or that is particularly nutritious.

It's probably fair to say that the remaining species of lion tamarin are similar to their golden relative, although they have been not nearly so well studied. Still, that's not to say that we haven't identified a few differences.

Just inland from the golden species we find the black lion tamarin (Leontopithecus chrysopygus), inhabiting a long strip of forest rather further from the coast. They aren't entirely black, having a few patches of golden fur, especially on the rump, but it is their overwhelming colour. They formerly lived throughout the subtropical forest north of the Paranapanema River, but, while that's hardly a huge area (it's not a long river), continued deforestation has left them inhabiting just eleven patches of woodland . One of those is inside a national park, and so plausibly safe, but all ten of the others are under threat, and the populations there are unlikely to be sustainable. Thus, while the total wild population is about one thousand, the same as for the golden species, in this case, it's a population that is continuing to decline.

Black lion tamarins live in forests where bromeliads are uncommon, so this clearly isn't the requirement for them that it appears to be for their golden kin. They tend to forage closer to the ground, too, focussing on patches of dry palm leaves, loose bark, and so on, although still above the forest understory. The forest of their home is less rich than that along the coast, which probably explains why, although they live in similarly sized groups, they travel over much larger areas, with 90 hectares (220 acres) being one estimate of the average. During the dry season, they eat more insects and drink more nectar, switching to fruit when it becomes abundant again as the rains come. Like the golden species, adults voluntarily share food with infants that are not their own.

Golden-headed lion tamarin
Further north, we come to the golden-headed lion tamarin (Leontopithecus chrysomelas), living in a small patch of coastal forest rather similar to that of the golden species, but both hotter and wetter. They appear to have very similar diets and requirements to their golden kin, including the reliance on bromeliads. They may, however, be somewhat more adaptable, being common today in so-called "cabruca" forests, which are basically abandoned and overgrown rubber and cocoa plantations with a few tall, old-forest trees in among them. It is these latter that are likely particularly important, providing the monkeys with bromeliads and with the sleeping holes that they crave. On the downside, they may be at more risk from predators here than in virgin forest.

It may be because of this that their population is thought to be much higher than those of the two species I've previously described, although still declining fast enough for them to be considered an endangered species. They have mostly black fur, but, as their name suggests, they have a flare of golden hair on the front of their manes, as well as having golden limbs and a similarly coloured patch on the upper part of their tail. Like many other tamarins, they benefit from the presence of local marmosets (in this case, Wied's species), which gouge away tree bark, leaving trees dripping edible gum for the tamarins to eat once the marmosets have left. Perhaps with a greater need to identify ripe fruit for their young, some females, but no males, have been shown to have full-colour vision.

Although there isn't much of a dry season in this particular part of the world, births are still most common in the times of year when it occurs further south. Oddly, though, this pattern disappears when they're kept in captivity outside Brazil (though not inside that country). It isn't entirely clear why, although it presumably has something to do with the nature of the environment. Either way, females clearly signal to the males when they're ready to mate, and groups are, as with the golden species, almost exclusively monogamous.

Black-faced lion tamarin
For over a hundred years, these were the three kinds of lion tamarin we knew about. Then, in 1990, Maria Lorini and VG Persson described a fourth species: the black-faced lion tamarin (Leontopithecus caissara). For a while, there was debate as to whether this really was a species, or just an odd-looking and isolated population of black lion tamarins, but a genetic analysis in 2008 confirmed its status as a full species. With a total estimated population of just 400, and falling, it turns out to be even more endangered than any of its kin, literally on the verge of extinction.

We know very little about this new species, but what we do know makes it somewhat unusual. It looks normal enough, almost reversing the look of the golden-headed lion tamarin with a golden body and black head and limbs. But it lives further south than any other species of the marmoset family, the only one to live so far south it's actually in the temperate zone, not the tropics. It was first discovered on Superagui Island, which is about 37 x 7 km (22 x 4 miles) in size, although we now know that it also lives on in an even smaller area on the nearby mainland. It takes the insistence on lowland forest among lion tamarins to an extreme, not being found above 40 metres (130 feet) in altitude... although, in an area that small, it's not as if it has much choice.

Mind you, it probably cuts both ways. This far south, and with a range of mountains right next to the coast, you don't have to go very up, or very far inland, before it's simply too cold for monkeys. Down on their island, there are palm trees, with bromeliads, where they can shelter in the night, before going to forage in swampier land during the day. Even so, it's obviously very marginal, by tamarin standards, and they both live in smaller groups and, at 300 hectares (just over a square mile) each, occupy far larger areas  than any related species.They also spend almost all of their day either travelling or searching for food, with only about an hour or so left for social activities.

For the most part, they eat what other lion tamarins eat, but there is one major difference, in that they eat a surprisingly large amount of fungus, in particular a species found on the local bamboo plants. This is especially so in the dry season, when fruit is in particularly short supply. Evidently, they have adapted to eat what they can get.

And so, here, on the very edge of the places where we'd expect to find monkeys, or perhaps even a little beyond it, I reach the last of the species of tamarin. With all of the marmosets, and now all of the tamarins, described, I've almost finished the list of living species in the family of the "beautiful-haired monkeys". Almost, but not quite...

[Photos by Jeroen Kransen, "Ruth Flickr", "Mulhouseville", and Everton Leonardi, from Wikimedia Commons]

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