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Nasalis among the odd-nosed colobines or The “Nasalis Paradox” (proboscis monkeys part II)

The views expressed are those of the author and are not necessarily those of Scientific American.

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Yay, more primates. Right?

Yet another well adorned male Proboscis monkey. Photo by Bjørn Christian Tørrissen, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.

Before moving on to other things (the list of subjects that need to be covered at Tet Zoo ASAP is now worryingly and impractically long), I must finish with the Proboscis monkey Nasalis larvatus [adjacent photo by Bjørn Christian Tørrissen].

In the previous article I discussed various aspects of this fascinating monkey’s distribution, ecology and behaviour. We also looked at the fact that – like so many Bornean endemics – it’s endangered by habitat loss and fragmentation. In this second article on the species we look at what I’ll call the “Nasalis Paradox”, and at the position of the species with respect to its relatives.

Despite frequent references in popular texts on primates to limb proportions and hand and toe form, surprisingly little technical information is available on the anatomy of the Proboscis monkey. Well, I shouldn’t really refer to this absence of information as ‘surprising’ given that anatomical data on any given animal is typically hard or impossible to find. Like so many animals, the Proboscis monkey is definitely full of surprises. Matsuda et al. (2011) recently showed that it practices merycism: that is, it regurgitates partially digested plant food, chews it, and swallows it again. That’s right – the Proboscis monkey is a ‘cud-chewing’ ruminant, convergent with artiodactyls (and those other mammals that chew the cud). So far as we know at the moment, the Proboscis monkey is unique among primates in this respect.

Many monkeys are highly flamboyant. This is one of the pig-tailed macaques (either Macaca leonina or M. nemestrina). Macaques like this are somewhat similar in coat colour, body proportions and so on to the Proboscis monkey.

Another thing that makes the Proboscis monkey especially interesting is the contention that it seems to be one of those animals that leads a lifestyle that it’s seemingly not well adapted for (regular readers will recall my recent mention of the “Anatomy is not destiny” maxim, one of my favourite concepts in historical biology). Its limb proportions, tooth anatomy (it exhibits strong alveolar prognathism*) and skin and coat colour are all of a sort normal for strongly terrestrial monkeys, like macaques, not arboreal ones. The strong sexual dimorphism present in the species is also more typical of terrestrial monkeys than arboreal ones. To quote Brandon-Jones (2006), “These adaptations indicate that the genus evolved in woodland characterized by an openness demanding considerably more terrestrial locomotion than the mangrove and lowland rainforest it currently inhabits” (p. 341). This is the “Nasalis Paradox”.

* That is, the sockets of its teeth are directed so that the teeth themselves project outwards from the jaws.

As I hope to explain here, we get a better perspective on this issue by thinking about things in a tree-based (that is, phylogenetic) context: how does the Proboscis monkey compare in morphology and habitat choice to its close relatives? Is it really such a paradox, or have we been duped by misleading anatomical similarities? In order to investigate this further, we need to visualise the Proboscis monkey within phylogeny [photo below by Frank Wouters].

Male and female Proboscis monkey engaging in allogrooming. Nice view of the pelage details. Photo by Frank Wouters, licensed under Creative Commons Attribution 2.0 Generic license.

Whereabouts do Proboscis monkeys belong within the Old World monkey radiation? They’re certainly colobines* but, beyond that, there has been a reasonable amount of disagreement; in fact, the phylogeny of Asian colobines has become a fairly hot topic within Old World monkey research since about 2003.

* There have been several efforts to get Colobinae – the sister-group of Cercopithecinae – ‘upped’ in rank to become Colobidae. Most texts, however, still list Colobinae and Cercopithecinae as ‘subfamilies’ of Cercopithecidae.

Many odd-nosed colobines are elaborately ornamented, colourful monkeys. This is a Red-shanked douc (Pygathrix nemaeus). Photo by Bjørn Christian Tørrissen, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.

The Proboscis monkey has frequently been considered a very close relative of the Simakobu, Pig-tailed langur or Pig-tailed snub-nosed langur Simias concolor of the Mentawai Islands off western Sumatra. Both are similar in limb proportions, pelage characters and in having narrow, long-faced skulls with long, narrow nasal bones. In fact some authors have included the Simakobu within Nasalis, the genus that is otherwise uniquely reserved for the Proboscis monkey. A sister-group relationship between the two is seemingly supported by molecular data (Whittaker et al. 2006); whether Simias and Nasalis are regarded as congeneric or as sister ‘genera’ is therefore down to preference. The Simakobu is a poorly known, strongly arboreal monkey and is reported to spend time in pairs rather than large groups.

The general idea that Asian colobines – grouped together as the clade Presbytina – can be divided into an ‘odd-nosed colobine’ and a langur and leaf monkey clade has been around since the 1970s (Groves 1970). An alternative hypothesis regarded the Proboscis monkey as an unusual colobine with an ‘isolated’ phylogenetic position: unlike the others, it has 48 chromosomes (the others have 44), so was regarded as ‘primitive’. Bigoni et al. (2003) argued that the high chromosome number is not a primitive character but the result of unusual splitting events that upped the ancestral number. These authors argued that the Proboscis monkey is deeply nested within the colobine radiation.

This has been given additional supported by more recent molecular work (Sterner et al. 2006, Whittaker et al. 2006, Osterholz et al. 2008, Perelman et al. 2011, Wang et al. 2012), all of which has shown that the Proboscis monkey is indeed part of that ‘odd-nosed colobine’ clade hypothesised by Groves (1970). However, several different topologies have been recovered for the different odd-nosed colobine taxa. Osterholz et al. (2008) found Nasalis to be in an unresolved polytomy with Rhinopithecus (snub-nosed monkeys) and Pygathrix (doucs), with Presbytis (surilis) and Trachypithecus (lutongs) belonging to a sister-group [douc photo above by Bjørn Christian Tørrissen]. Meyer et al. (2011) found Nasalis to be the sister-taxon to a douc + snub-nosed monkey clade while Perelman et al. (2011) and Wang et al. (2012) supported a closer relationship between the Proboscis monkey and the doucs rather than with the snub-nosed monkeys. As mentioned above, Simias is probably closer to Nasalis than to any other odd-nosed colobine (Whittaker et al. 2006).

Old World monkey phylogeny (with some hominoids too), from Wang et al. (2012). We're interested in the topology among Asian colobines.

As always, the recovery of a robust phylogeny does more than just allow us to hang species on branches; we can now formulate, and perhaps test, hypotheses about patterns of evolution. Living odd-nosed colobines are unlike other Asian colobines in being exclusive to Southeast Asia and Borneo, so the phylogeny strongly suggests that they’re always been limited to this region and are hence tied to its ecology and biogeography.

One of the prettiest monkeys (according to some): Golden snub-nosed monkey (Rhinopithecus roxellana). Photo by Jack Hynes, licensed under Creative Commons Attribution-Share Alike 2.0 Generic license.

You’ll recall from earlier that the Proboscis monkey is (supposedly) seemingly more ‘terrestrial’ in its anatomy than ‘arboreal’. What might the phylogeny tell us about the expected ancestral mode of life for this species, and about that “Nasalis Paradox”? Doucs and snub-nosed monkeys are both forest-dwellers, with populations inhabiting a diversity of coniferous, broadleaved temperate, and evergreen tropical habitats. The Pig-tailed langur is also very much a forest animal, and indeed is described as strongly arboreal [adjacent illustrations of Golden snub-nosed monkey pair by Jack Hynes].

So far as I can see, this could all means one of two things. The first possibility is that the Proboscis monkey comes from a long line of forest-dwelling, mostly arboreal, odd-nosed colobines. Its mostly arboreal, forest-dwelling lifestyle is thus normal for its clade, and those so-called terrestrial features have been misinterpreted: they aren’t indications of a former terrestrial life at all.

The second possibility is that, while it today occurs in forests and is mostly arboreal, the Proboscis monkey (or, at least, populations along its stem-lineage) really did go through a phase of being strongly terrestrial and hence very different from the other odd-nosed colobines – it’s just that this didn’t work out, and the species had to revert to the ancestral, forest-dwelling, mostly arboreal way of life.

Interested in primate diversity, phylogeny and evolutionary history? Then be sure to obtain Ian Redmond's excellent The Primate Family Tree, republished as Primates of the World.

Scientific hypotheses are meant to be led by parsimony (the concept that the simplest solution to a problem is the likely correct one). Viewed within the context of parsimony, the first hypothesis is the favourable one. But that doesn’t mean it’s the best hypothesis. One of the main points of Douglas Brandon-Jones’s article on Asian colobine evolution and history was that climatic fluctuations in Asia’s recent geological past may have had significant impacts on the distribution of the species concerned (Brandon-Jones 1996). He argued that palaeoclimatic data from the Bornean record indicates the existence of an arid phase coinciding with the last glacial maximum of the Late Pleistocene. Supposedly, the reduced forest cover and drier regime that resulted led to species like the Proboscis monkey, seemingly adapted for these more arid, drier woodland habitats. However, biogeographic data from gibbons, orangutans, forest-dwelling langurs and other animals directly contradicts this scenario: it seems instead that Borneo was consistently forested across this time (Earl of Cranbrook 2000, Meijaard & Groves 2004).

It seems appealing to me that there is indeed something in the “Nasalis Paradox” idea, and that members of the Nasalis lineage did go through a ‘dry forest’, semi-terrestrial phase at some stage in their evolution. But I now think that we’ve been duped: that the supposed terrestrial, ‘dry forest’ adaptations of the Proboscis monkey do not represent the vestiges of history, but convergent features with monkeys that evolved in wholly different environments.

For previous Tet Zoo articles on primates, do check out…

And if you are interested in obtaining Ian Redmond’s The Primate Family Tree, republished as Primates of the World, please help vital work on primate conservation by purchasing it from the Shop 4 Apes store. And… you don’t want to buy anything from amazon anyway, do you? Exactly.

Refs – -

Bigoni, F., Stanyon, R., Wimmer, R. & Schempp, W. 2003. Chromosome painting shows that the proboscis monkey (Nasalis larvatus) has a derived karyotype and is phylogenetically nested within Asian colobines. American Journal of Primatology 60, 85-93.

Earl of Cranbrook 2000. Northern Borneo environments of the past 40,000 years: archaeozoological evidence. The Sarawak Museum Journal 55, 61-109.

Groves, C., 1970. The forgotten leaf-eaters, and the phylogeny of the Colobinae. In Napier, J. R. & Napier, P. H. (eds) Old World Monkeys: Evolution, Systematics and Behavior. Academic Press, New York, pp. 555-587.

Matsuda, I., Murai, T, Clauss, M., Yamada, T., Tuuga, A., Bernard, H. & Higashi, S. 2011. Regurgitation and remastication in the foregut-fermenting proboscis monkey (Nasalis larvatus). Biology Letters 7, 786-789.

Meijaard, E. & Groves, C. P. 2004. The biogeographical evolution and phylogeny of the genus Presbytis. Primate Report 68, 71-90.

Meyer, D., Rinaldi, I. D., Ramlee, H., Perwitasari-Farajallah, D., Hodges, J. K. & Roos, C. 2011. Mitochondrial phylogeny of leaf monkeys (genus Presbytis, Eschscholtz, 1821) with implications for taxonomy and conservation. Molecular Phylogenetics and Evolution 59, 311-319.

Osterholz, M., Walter, L. & Roos, C. 2008. Phylogenetic position of the langur genera Semnopithecus and Trachypithecus among Asian colobines, and genus affiliations of their species groups. BMC Evolutionary Biology 2008, 8:58 doi:10.1186/1471-2148-8-58.

Perelman, P., Johnson, W. E., Roos, C., Seuanez, H. N., Horvath, J. E., Moreira, M. A. M., Kessing, B., Pontius, J., Roelke, M., Rumpler, Y., Schneider, M. P. C., Silva, A., O’Brien, S. J. & Pecon-Slattery, J. 2011. A molecular phylogeny of living primates. PLoS Genetics 7: e1001342.

Sterner, K. N., Raaum, R. L., Zhang, Y. P., Stewart, C. B., Disotell, T. R. 2006. Mitochondrial data support an odd-nosed colobine clade. Molecular Phylogenetics and Evolution 40, 1-7.

Wang, X. P., Yu, L., Roos, C., Ting, N., Chen, C. P., Wang, J. & Zhang, Y. P. 2012. Phylogenetic relationships among the colobine monkeys revisited: new insights from analyses of complete mt genomes and 44 nuclear non-coding markers. PLoS ONE 7(4): e36274. doi:10.1371/journal.pone.0036274

Whittaker, D. J., Ting, N. & Melnick, D. J. 2006. Molecular phylogenetic affinities of the Simakobu monkey (Simias concolor). Molecular Phylogenetics and Evolution 39, 887-892.

Darren Naish About the Author: Darren Naish is a science writer, technical editor and palaeozoologist (affiliated with the University of Southampton, UK). He mostly works on Cretaceous dinosaurs and pterosaurs but has an avid interest in all things tetrapod. His publications can be downloaded at He has been blogging at Tetrapod Zoology since 2006. Check out the Tet Zoo podcast at! Follow on Twitter @TetZoo.

The views expressed are those of the author and are not necessarily those of Scientific American.

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  1. 1. Heteromeles 9:47 pm 12/13/2012

    A couple of points: the real question that Brandon-Jones blew off are *how* the limb proportions, skin color, and coat color are related to a terrestrial habitat, and whether the same adaptive forces are present in the current mangrove forest. I’m having real trouble with the idea that a mangrove specialist recently and swiftly evolved from some generalist terrestrial species. The untested neutral hypothesis is that, from an primate evolutionary standpoint, perhaps mangroves look like terrestrial environments.

    A second issue: there’s a common evolutionary theme that, when body part comes under “odd” evolutionary modification, there’s often a plethora of different modifications. This is apparently true for proboscis monkey noses, gecko toes, Banksia leaves, the roots of ectomycorrhizal fagales, and many others. Is there a term for this kind of limited evolutionary exuberance?

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  2. 2. Hai~Ren 12:47 am 12/14/2012

    I wonder if the proboscis monkey’s supposed terrestrial features are seen in the colobines that DO spend a lot of time on the ground, the grey langurs (Semnopithecus spp.)

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  3. 3. SRPlant 2:57 am 12/14/2012

    Fascinating article as always.

    Just wondering; anyone know the etymology of ‘merycism’?

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  4. 4. Jerzy v. 3.0. 5:04 am 12/14/2012

    Proboscis monkey is supposed to be very specialized in eating mangrove leaves (but maybe not so, in one Asian zoo they raid rubbish bins), so it is a bit of a doubt if they could live in semi-open habitats.

    Maybe living in mangroves (especially long jumps over water channels) could produce adaptations similar to terrestrial lifestyle?

    Which is more broad question: when a lineage changes lifestyle, how long it takes before morphology evolves? Some data from Galapagos birds etc…?

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  5. 5. naishd 5:16 am 12/14/2012

    Lots of interesting comments, thanks. Jerzy (comment 4): excellent point (about the lag between behavioural and morphological adaptation). Some isotopic analysis on fossil proboscideans shows that animals with ‘browsing’ dentitions were eating silica-rich grasses of the sort they don’t look suited for. The suggestion is that they were taking advantage of this new food source, but were not (yet) specialised for it. I think that this is common – animals often do what they can, not what we think they ‘should’.


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  6. 6. Basandere 6:37 am 12/14/2012

    @SRPlant: Merycism is from Classical Greek μηρυκάζειν “mērykázein”: to ruminate. This actually is the same root as in merychippus, which apparently had (or was thought to have) ruminant-like teeth.

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  7. 7. SRPlant 7:02 am 12/14/2012

    And a very merychippus to you, Basandere. Thank you for such a thorough answer.

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  8. 8. Heteromeles 10:02 am 12/14/2012

    And a hippo gnu deer as well. Perhaps there’s a South American enigmatic fossil that fits this?

    Anyway, it’s amusing that regurgitation is considered pathological in humans, but adaptive in ruminants and proboscis monkeys. Structurally, I don’t think mercyism is that hard, evolutionarily.

    What I do wish someone would do is to characterize the gut bacteria of proboscis monkeys, and see where they got them. Did they somehow swipe the gut bacteria of some mangrove caterpillar or something? Yes, I do know why that would be hard, but I also know that such things have been suggested for birds (I think trogons?) who feed caterpillars to their young but eat the caterpillar’s host plants (or at least their fruits) as adults.

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  9. 9. Finback 5:58 pm 12/14/2012

    Red shanked douc is clearly working hard at becoming the new Fry-meme.
    “Not sure if colobine or not.jpg”?

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  10. 10. naishd 6:01 pm 12/14/2012

    Finback – - say what?


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  11. 11. David Marjanović 10:29 pm 12/14/2012

    those other mammals that chew the cud

    What are those???

    And what does meryx mean? It appears a lot in the names of fossil ruminants.

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  12. 12. BrianL 5:38 am 12/15/2012


    Sorry, but what do you mean by ‘a hippo gnu deer as well’? I don’t get it.

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  13. 13. Dartian 8:18 am 12/15/2012

    but what do you mean by ‘a hippo gnu deer as well’?

    Hippo gnu deer = happy new year. ’tis a pun. (And merychippus = merry Christmas.)

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  14. 14. Dartian 8:22 am 12/15/2012

    Maybe living in mangroves (especially long jumps over water channels) could produce adaptations similar to terrestrial lifestyle?

    Now that’s certainly an intriguing thought. But I have a hard time imagining what the selective similarities between mangrove forests and terra firma could be. Something about mangrove tree physical structure, perhaps?

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  15. 15. naishd 8:29 am 12/15/2012

    David (comment 11): which other mammals ‘chew the cud’ (or, that is, practise merycism) besides artiodactyls? (and Proboscis monkeys). Answer: marsupials! Various macropods, including quokka, pademelons and some Macropus wallabies, are reported to practise merycism (Hume 1982). It’s also been described for big kangaroos but other observers contest this. Bandicoots, dasyurids and koalas (Logan 2001) have also been reported to practise merycism.

    Because these animals do not have the same foregut specialisations as members of Ruminantia, this in fact explains why the term merycism was proposed by Barker et al. (1963) in the first place. It is derived from the Greek ‘merycismus’, meaning ‘rumination’.


    Refs – -

    Barker, S., Brown, G. D. & Calaby, J. H. 1963. Food regurgitation in the Macropodidae. Australian Journal of Science 25, 430-432.

    Hume, I. D. 1982. Digestive Physiology and Nutrition of Marsupials. Gustav Fischer Verlag, Stuttgart.

    Logan, M. 2001. Evidence for the occurrence of rumination-like behaviour, or merycism, in the koala (Phascolarctos cinereas Goldfuss). Journal of Zoology 255, 83-87.

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  16. 16. Basandere 9:45 am 12/15/2012

    [blockquote]A very merychippus and a hippo gnu deer [/blockquote]

    Thanks guys. :D I take it language and zoology geeks are not mutually exclusive groups after all — looks like I’ll feel right at home!

    @David (comment 11): I believe meryx- will be from just the same root as root a meryc-, thus Greek for ‘ruminate’. See above. :)

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  17. 17. David Marjanović 4:34 pm 12/15/2012

    I looked it up: “a ruminating fish, Scarus cretensis“, mentioned by Aristotle.

    Apparently, then, when used as part of scientific names, it’s more or less made up and is meant to mean “ruminant”.

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  18. 18. hkneoh 6:43 am 12/16/2012

    If at all there was a ‘terrestrial phase’ for Nasalis, it could have been during the last ice age when the Sunda Shelf was exposed by retreating sea levels. The resultant exposed land, being distant from the sea, could have supported open forest or even savannah. Could this have accounted for the supposedly terrestrial features of the odd-nosed group?

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  19. 19. Heteromeles 11:47 am 12/16/2012

    Hmmm. We’ve got two problems here. One is the problem of eating mangroves, and the other problem is a body plan seemingly poorly adapted for moving around in a generic arboreal environment.

    Mangroves tend to be toxic in ways that promote the existence specialist feeding guilds. One thing that hasn’t been studied (to my knowledge) is whether animals that eat mangroves share a common suite of gut bacteria, in which case there’s some sort of horizontal transmission of the appropriate gut microbes (through predation or scavenging), or whether there’s convergent evolution going on. This is complicated because, AFAIK, Indonesia is the heartland of mangrove diversity. Multiple clades of plants have evolved mangrove forms. Most of the eudicot mangroves are quite toxic, but not necessarily in similar ways, and that leads to yet another question of what species proboscis monkeys eat, and whether they’re ultra-specialized on a few mangroves, or generalized detox machines.

    Part of the solution is obviously to question whether there is such a thing as a generic arboreal environment so far as primates are concerned, and whether mangroves match this environment.

    The other part of the puzzle is to look at other vegetation specialists, and see what comes first, guts or limbs.

    Unless there’s another colobus monkey out there that specializes in toxic plants, the analogous group for proboscis monkeys that comes to my mind are bamboo lemurs, some of which eat strongly cyanogenic bamboos. What I don’t know is whether bamboo lemurs show any morphological specializations to living in bamboo, or whether they’re morphologically generalized lemurs with specialized digestive apparatuses. Hopefully someone can answer that question, because that will help us figure out which evolves first, guts or limbs.

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  20. 20. vdinets 8:01 pm 12/16/2012

    hkneoh: My understanding is that during the last ice age, the shorelines of Borneo were mostly formed by very flat lowlands, so mangroves were probably more extensive than they are today. On the other hand, there are still places on Borneo where the forest is fairly open and looks a bit like savanna, but proboscis monkeys prefer mangroves in such areas.

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  21. 21. naishd 8:35 pm 12/16/2012

    Thanks for more great comments.

    hkneoh (comment 18): yes, it has indeed been suggested that much of the Sundaland area was covered by savannah during the more arid phases of the Pleistocene (there is even a ‘Sundaland Savannah Corridor’ Hypothesis). This would indeed be consistent with the hypothesis that the Proboscis monkey was formerly suited for a ‘dry woodland’/semiterrestrial kind of lifestyle. The problem – as I said in the article – is that this is now seemingly contradicted by biogeographic data from orangutans, gibbons, moonrats and other mammals, all of which seem to show that the area integral to the evolution of Nasalis was forested and tropical throughout the time that this animal was around. Of course, that doesn’t remove the possibility that Nasalis came in from elsewhere but, to date, we have no evidence for this (so far as I know).


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  22. 22. naishd 8:48 pm 12/16/2012

    Heteromeles (comment 19): on bamboo lemurs, there isn’t much information out there. Some people say that they’re specialised for their bamboo diet, but the only specialisation ever mentioned is large gut size – I haven’t heard anything special about limb proportions or such.

    And the problem with the idea of bamboo specialisation for this group is that populations of some species live in places where there is scarcely any bamboo; they seem to be able to eat a diversity of grasses and hence to be flexible (among grass-eating herbivores, at least). Indeed, behavioural flexibility might be the key to their success: they’re said to be unusual among lemurs in being cathemeral (active at any hour)… though, to be honest, I thought that cathemerality was one of those things probably common in lemurs, just mostly unappreciated given that it’s a piece of behaviour rarely recorded by humans for obvious reasons. Anyway, see Eppley et al. (2011) for more.


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    Eppley, T. M., Verjans, E. & Donati, G. 2011. Coping with low-quality diets: a first account of the feeding
    ecology of the southern gentle lemur, Hapalemur meridionalis, in the Mandena littoral forest, southeast Madagascar. Primates 52, 7-13.

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  23. 23. Finback 8:22 am 12/17/2012

    Darren – in response to Fry meme..

    The douc is trying to replace the Frymeme with a newer doucmeme.

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  24. 24. naishd 8:25 am 12/17/2012

    Despite being a huge Futurama fan, and despite being very familiar with Frymemes, I didn’t get it until now. Thanks (smiley).

    And – - with that, we’ve over the required minimum of 23 comments. Time to move on, ha ha.


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