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Marmosets and tamarins: dwarfed monkeys of the South American tropics


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Marmosets and tamarins (callitrichids) are small platyrrhine monkeys: total lengths range from 40 cm for the Pygmy marmoset Cebuella pygmaea to 75 cm for the Golden lion tamarin Leontopithecus rosalia. The Pygmy marmoset can weigh as little as 120 g. Callitrichids are unique to tropical South [UPDATE: and Central!] America.

Cottontop tamarin (Saguinus oedipis), an endangered callitrichid of Colombia and Panama.

About 60 species are recognised, though – as always with extant primates – debate continues as regards which populations should be regarded as ‘species’ or ‘subspecies’. A dazzling array of manes, silky coats, long, tufted tails, ear tufts, moustaches and other visual display structures decorate their heads and bodies; indeed, the group name ‘Callitrichidae’ means ‘beautiful hair’.

Callitrichids have been extensively studied by primatologists interested in their complex social lives. Monogamy is common, (non-identical) twins are typically produced at a time, and males and females are similarly ornamented. All members of a social group assist in caring for babies, and fathers are attentive babysitters, even handling newborns the instant they are born. Sexual maturity is reached quickly – typically at about a year in age.

Phylogeny of platyrrhines plotted against a timescale, from Opazo et al. (2006). Saguinus and Leontopithecus are tamarins; Callimico is Goeldi's monkey; marmosets are represented by Callithrix.

Because the small body size of callitrichids is unusual compared to the majority of other platyrrhine lineages, it has often been supposed that they are dwarfed relative to the ancestral condition (Ford 1980). The alternative – that they’ve inherited small size directly from ancestral stem-platyrrhines – has also been suggested (Hershkovitz 1977). Goeldi’s monkey Callimico goeldii is unlike other callitrichids in producing single babies and in having three lower molar teeth (as opposed to two), so has sometimes been regarded as a sort of evolutionary intermediate between callitrichids and other platyrrhines. This view hasn’t been supported by phylogenetic studies, however, since these generally find Goeldi’s monkey to be the sister-taxon to marmosets, not to all other callitrichids (e.g., Canavez et al. 1999, Chaves et al. 1999, Opazo et al. 2006). Tamarins (Saguinus and Leontopithecus) appear to represent a callitrichid ‘grade’ outside the Goeldi’s monkey + marmoset clade (Opazo et al. 2006). While most workers have regarded callitrichids as a distinct ‘family’, close to, but separate from, cebid platyrrhines, others have regarded callitrichids as a cebid ‘subfamily’ (hence, Callitrichinae instead of Callitrichidae).

A selection of marmosets, as drawn by Gustav Mützel for the 1927 Brehms Tierleben. From left to right: Common marmoset (Callithrix jacchus), Silvery marmoset (Mico argentata), and Black tufted-ear marmoset (C. penicillata). From wikipedia.

It’s well known that primates have (mostly) switched claws for nails. Callitrichids are unusual in having claws on all digits except the hallux. This has to be an evolutionary reversal, given the ubiquity of nails elsewhere in primates. Further, callitrichids have apical pads on their digits. These seemingly aren’t used in locomotion and must be leftovers of an original nail-bearing condition (other anatomical features associated with nails are also present, and also seem to be redundant leftovers) (Rosenberger 1977).

These clawed digits are presumably beneficial for a lifestyle that involves speedy, squirrel-like scurrying in the trees as well as vertical clinging. Fruit, plant exudates like gum and latex, and animals including arthropods, snails, frogs and lizards are eaten, with tamarins eating more fruit, and marmosets eating more exudates. Marmoset dentition is specialised for exudate feeding: in some species the lower incisors are huge and curved, being similar in size to the canines, and with a thick outer layer of enamel. While the upper incisors are hooked into the bark, the lower ones repeatedly gouge into it, opening an oval cavity and thereby allowing the gum, sap or latex to seep out.

Has the small size of these monkeys evolved under selection for arboreal locomotion on small branches? Actually, a list of hypotheses have been invoked to explain the evolution of dwarfism in callitrichids, with extensive predation, a reduced availability of resources and/or ecological niche space, and a need to breed fast and breed young all being suggested as possible forces encouraging the dwarfing process (Ford 1980).

And, once again, so much for a ‘picture of the day’-type post. More primates soon.

Refs – -

Canavez, F. C., Moreira, M. A. M., Simon, F., Parham, P. & Seuanez, H. N. 1999. Phylogenetic relationships of the callitrichinae (Platyrrhini, Primates) based on 2-microglobulin DNA sequences. American Journal of Primatology 48, 225-236.

Chaves, R., Sampaio, I., Schneider, M. P., Schneider, H., Page, S. L. & Goodman, M. 1999. The place of Callimico goeldii in the callitrichine phylogenetic tree: evidence from von willenbrand factor gene intron II sequences. Molecular Phylogenetics and Evolution 13, 392-404.

Ford, S. M. 1980. Callitrichids as phyletic dwarfs, and the place of the Callitrichidae in Platyrrhini. Primates 21, 31-43.

Hershkovitz, P. 1977. Living New World Monkeys (Platyrrhini) with an Introduction to the Primates. Volume 1. University of Chicago Press, Chicago.

Opazo, J. C., Wildman, D. E., Prychitko, T., Johnson, R. M. & Goodman, M. 2006. Phylogenetic relationships and divergence times among New World monkeys (Platyrrhini, Primates). Molecular Phylogenetics and Evolution 40, 274-280.

Rosenberger, A. L. 1977. Xenothrix and ceboid phylogeny. Journal of Human Evolution 6, 461-481.

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 darrennaish.wordpress.com. He has been blogging at Tetrapod Zoology since 2006. Check out the Tet Zoo podcast at tetzoo.com!

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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. vdinets 8:58 am 11/27/2012

    Opazo et al. phylogeny makes it clear that they shouldn’t be considered a family, doesn’t it?

    Link to this
  2. 2. naishd 9:45 am 11/27/2012

    Well, it’s one of those subjective things. Cebidae is obviously anchored on Cebus, but Atelidae is already used by some workers for whatever lineages includes Ateles, and Pitheciidae for the Pithecia lineage. Thus, the phylogeny above could allow for the names Cebidae, Callitrichidae, Pitheciidae and Atelidae. Or, you could lump all lineages here into Cebidae and then recognise Cebinae, Callitrichinae, Pitheciinae and Atelinae for its constituent clades. Or you could have Atelidae and Cebidae, with Pitheciinae within Atelidae, and Callitrichinae within Cebidae.

    For the record, Opazo et al. (2006) preferred the three ‘family’ system, with Cebidae, Pitheciidae and Atelidae, and Callitrichinae within Cebidae.

    But, like I said, it’s all subjective. I think that keeping callitrichids as a ‘family’ is the most sensible decision, partly because it’s the commonest one in the literature, and also because it’s the one most frequently used in legislation, education and conservation.

    Darren

    Link to this
  3. 3. keesey@gmail.com 11:01 am 11/27/2012

    Don’t forget Aotidae!

    Link to this
  4. 4. Zoovolunteer 2:25 pm 11/27/2012

    Callitrichids also have rather odd preganancies. The developing twins or triplets exchange cells, resulting in most of the young having varying levels of chimaerism. I have read this may be influential in the development of the male supportive behaviour – several species at least are polyandrous and having infants with potentially two fathers may have encouraged all males in the group to evolve to care for young indiscriminately.

    Link to this
  5. 5. naishd 3:07 pm 11/27/2012

    Mike (comment 3) – yes, I forgot about Aotidae…

    Darren

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  6. 6. vdinets 4:05 pm 11/27/2012

    Darren: thank you. Personally, I don’t think having 4 families would be a good idea, in part because Cebidae would be a grouping of three genera that look totally different. Also, drawing a cutoff line for family recognition between 22.05 and 22.75 mya seems highly arbitrary. But it’s not something that can be constructively argued about :-)

    Link to this
  7. 7. John Harshman 6:42 pm 11/27/2012

    You should put in something about color vision, which is satisfyingly bizarre.

    Link to this
  8. 8. Heteromeles 8:16 pm 11/27/2012

    A dazzling array of manes, silky cats, long, tufted tails…

    I don’t think they have cats, although it is a charming image.

    [from Darren: d'oh! Now corrected, thanks.]

    Link to this
  9. 9. Heteromeles 8:44 pm 11/27/2012

    Since lemurs have (as I recall) a grooming claw on the second toe, while marmosets have claws on everything except thumb and hallux, I wonder two things:
    –are grooming claws also “nail reversals?”
    –are marmosets reverting to the lemur condition, except on more digits? Or are their digits structurally different than those of prosimians?

    Link to this
  10. 10. Allen Hazen 1:22 am 11/28/2012

    I find the continued use of the classical languages in zoological nomenclature… charming… but it does present potentially confusing features. Case in point: Callithrix (note h after t) being the nominate genus of the Callitrichidae (note absence of h after t). Other than David Marjanovic, how many zoologists and palaeontologists know enough about Greek phonology to explain — or for that matter, remember — that alternation?

    (Another nice post, b.t.w.: when does the collection, “Naish’s Encyclopedia of the Tetrapoda,” come out?)

    Link to this
  11. 11. Dartian 2:10 am 11/28/2012

    Darren:
    Callitrichids are unique to tropical South America.

    Strictly speaking, not entirely. Geoffroy’s tamarin Saguinus geoffroyi is found in Panama (and according to some sources, also in the southernmost part of Costa Rica) which, geographically, is not a part of South America.

    so much for a ‘picture of the day’-type post

    Aw, come on now, why do you even try to do those anymore? Ultimately you and we, your readers, will all be happier if you’ll just go ahead and keep writing those awesome full-length articles that we love to read. ;)

    Allen:
    “Naish’s Encyclopedia of the Tetrapoda,”

    IMO, “Naish’s Tetrapod Encyclopedia” has a nicer ring to it. ;)

    Link to this
  12. 12. David Kelly 5:25 am 11/28/2012

    I have seen Geoffroy’s Tamarin in the Parque Metropolitano in Panama City, so they definitely occur in Panama where they are confusingly called “titi monkeys”, in English this name is applied to the genus Callicebus which is exclusively South American.

    Link to this
  13. 13. naishd 8:14 am 11/28/2012

    Yes, I stupidly forgot when (hurriedly) writing this piece that Panama is not, technically, part of South America (I didn’t know about the presence of Geoffroy’s tamarin in Costa Rica until now: according to a book cited on this wikipedia page, those references are “likely erroneous”). Then again, some people say that Panama east of the canal is technically part of South America…

    Darren

    Link to this
  14. 14. SRPlant 2:00 pm 11/28/2012

    Darren, did you once say in a comment that some species of marmoset are left-handed and others right-handed, or am I misremembering?

    Link to this
  15. 15. naishd 4:52 pm 11/28/2012

    If I’ve said something about handedness in marmosets before, I’m afraid I can’t remember (I’ll have to check the Tet Zoo archives). Common marmosets reportedly display no statistical preference for left- or right-handedness, whereas the tamarins that have been studied generally seem right-handed. Check out Hook-Costigan & Rogers (2006).

    Hook-Costigan, M. A. & Rogers, L. J. 1996. Hand Preferences in New World Primates. International Journal of Comparative Psychology 9, 173-207.

    There may be more recent studies out there. Anybody know?

    Darren

    Link to this
  16. 16. Dartian 2:05 am 11/29/2012

    Darren:
    drawn by Gustav Mützel for the 1927 Brehms Tierleben

    Just for the record, lest there be any confusion: Gustav Mützel did indeed make that illustration for Brehms Tierleben, but originally for a much earlier edition than the 1927 one. Mützel died in 1893.

    Link to this
  17. 17. ggarbino 6:48 am 11/29/2012

    I particulary think the subject of “family” and “subfamily” a bit pointless. But I’m in favor of a subfamilial classification of Callitrichinae. In my view, Platyrrhini is composed of three main ecomorphological clades: Atelidae (with prehensile tails and big size); Pitheciidae (seed and leaf eaters, intermediate size and with Aotus included) and Cebidae, with reduced last molars (2nd or 3rd depending on the taxon) and also the most insectivorous group among the new world monkeys (in this I include the Cebinae Saimiri, which is also the smallest of the non-callitrichid new world monkey).
    There is an interesting nutritional fact that is not mentioned in the text and I’d like to add: Callimico goeldii and Callithrix flaviceps are known to consume a signifficant amount of fungi and maybe this is the reason Goeldi’s monkeys are so difficult to find (specific edible fungi are rare so the groups have large territory and the species has low densities).

    Link to this
  18. 18. Dartian 7:25 am 11/29/2012

    ggarbino:
    Pitheciidae (seed and leaf eaters, intermediate size and with Aotus included)

    Which phylogeny do you follow that supports the inclusion of Aotus in Pitheciidae/-nae? The source that Darren gives, Opazo et al. (2006), does not recover such a clade, and neither do any of the other recent studies on NW monkey phylogeny – at least not any one of those that I can think of off the top of my head (e.g., Wildman et al., 2009).

    Reference:
    Wildman, D.E., Jameson, N.M., Opazo, J.C. & Yi, S.V. 2009. A fully resolved genus level phylogeny of Neotropical primates (Platyrrhini). Molecular Phylogenetics and Evolution 53, 694-702.

    Link to this
  19. 19. ggarbino 12:11 pm 11/29/2012

    Hello,

    I am following the morphological evidence presented mainly by Marcelo Tejedor and Alfred Rosenberger. The sum of their evidence may be found in this reference:

    Rosenberger, A.L. and Tejedor, M.F. (in press) The misbegotten: long lineages, long branches
    and the interrelationhsips of Aotus, Callicebus and the saki-uakaris. In: Barnett, A., Viega, L.,
    Ferrari, S., Norconk, M. Cambridge University Press, Cambridge. Evolutionary Biology and
    Conservation of Titis, Sakis and Uacaris. Cambridge University Press, Cambridge.

    Which is scheduled to release in 2013.

    Link to this
  20. 20. naishd 12:32 pm 11/29/2012

    Wow, Aotus on the pitheciid branch, how interesting. ggarbino: thanks. How do you know about the contents of this unpublished work? The in-press book itself is well known (and I really hope I can get hold of a copy in time: very interested in sakis and uakaris in particular), but I haven’t read about the contents anywhere (not even in the new Pitheciine Action Group Newsletter).

    As regards other comments: yes, many interesting things about callitrichids were not mentioned in this article (fungivory, chimaerism, polymorphic colour vision etc.). Well, I never meant to say everything :)

    Darren

    Link to this
  21. 21. Dartian 12:46 pm 11/29/2012

    ggarbino:
    I am following the morphological evidence

    Hm, interesting – but that evidence better be really, really solid to ‘trump’ the molecular evidence.

    Link to this
  22. 22. ggarbino 1:31 pm 11/29/2012

    haha sure ! you can write a lot of things about these dwarves! Some researchers, like Susan Ford, have devoted many years of their lifes only studying them… I have asked to one of the authors for a copy (I am doing my master’s with callitrichids). The authors seems to argue for a “long branch attraction” and offer some postcranial (besides craniodental and behavioral) evidence for it. Unfortunately I do not know much about molecular phylogeny, so I can not tell how strong the support for (Aotus + Callitrichinae) is, but its a very recurrent clade in the molec. phylogenies…

    Link to this
  23. 23. John Harshman 10:55 pm 11/29/2012

    Long branch attraction: a technical term in phylogenetics whose essential meaning is “I didn’t like that result”.

    Link to this
  24. 24. Jerzy v. 3.0. 5:17 am 11/30/2012

    There is also lots of interesting stuff about hybridization between differently-colored subspecies in the wild (recently treated as species).

    Link to this
  25. 25. Heteromeles 11:53 am 11/30/2012

    Long branch attraction: a technical term in phylogenetics whose essential meaning is “I didn’t like that result”.

    Perhaps to some zoologists? It does depend on the length of the branch. I remember, back when they were arguing about the angiosperm phylogeny, that long branch attraction was a huge problem, because most of the extant primitive angiosperms were clades of a very few species that weren’t closely related to anything else. They’d been apart for so long (60-100 myr) that the multiple mutations per nucleotide site were to be expected, at least for commonly used sequences.

    I’m not so sure if the same thing applies to new world primates, though. AFAIK, they diverged somewhat more recently than the angiosperm orders did.

    Link to this
  26. 26. David Marjanović 10:21 am 12/3/2012

    Long branch attraction: a technical term in phylogenetics whose essential meaning is “I didn’t like that result”.

    The temptation to use it that way is always there; and of course I have no idea if long-branch attraction is going on in the case you’re talking about. But the problem is real – and it demonstrably also occurs with morphological data, even if perhaps not quite as frequently.

    Link to this

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