Indridae

Silky sifakas Propithecus diadema candidus, photographed by Jeff Gibbs.

Belongs within: Lemuriformes.

The Indridae is a family of lemurs including the indri Indri indri, woolly lemurs Avahi and sifakas Propithecus. They characterised by a relatively low number of teeth compared to other lemurs, and hind legs that are significantly longer than the forelegs.

There he goes!
Published 5 April 2010
Diademed sifaka Propithecus diadema. Most of the sifakas you see pictures or film of are P. verreauxi, so I’ll show you something different for a change. Photo from here.

The Indriidae (sometimes, just to be confusing, spelt as Indridae or Indrisidae) is a family of lemurs found in (of course) Madagascar. As generally recognised, the species of Indriidae are divided between three living genera, Indri (the indri), Avahi (the avahi[s]) and Propithecus (sifakas). Some authors (e.g. Marivaux et al., 2001) have included the bamboo lemurs of the genus Hapalemur in the Indriidae but most (e.g. Orlando et al. 2008) place Hapalemur in the Lemuridae. Also, two subfossil families of large lemurs, the Archaeolemuridae and Palaeopropithecidae, are closely related to the Indriidae and are included therein as subfamilies by some authors.

The three genera of indriids are united by a number of very distinct features. Perhaps the most obvious is that they all have the hind legs significantly longer than the fore legs, as demonstrated in countless nature documentary sequences featuring sifakas. Because of this disparity in limb length, the normally arboreal indriids cannot walk on all fours on the ground and, when forced to cross open spaces, hop upright on their hind legs only with the fore legs held upright. Indriids will also often sit upright with their arms held up in the same manner, leading to an old story that they are sun worshippers. Also noteworthy is the indriid dentition which has fewer teeth than many other primates*: two (pairs of) incisors, one canine, two premolars and three molars above and the same below except for the absence of the second incisors or the canines (depending who you ask) (Nowak 1999). All indriids are strict vegetarians.

*When this post was originally put up I said that indriids had the lowest number of teeth for primates but a number of commenters below have pointed out my mistake.

Avahi mooreorum, the most recently named of the Avahi species by Lei et al. (2008), from whence comes this photo.

The number of species in the family has been the subject of much recent activity. Nowak (1999) listed one species each of Indri and Avahi and three in Propithecus but recent publications and reviews have increased the number of species in Avahi and Propithecus to nine each (Mittermeier et al. 2008). In the case of Propithecus this increase has mostly been due to ‘subspecies’ being redefined as ‘species’ but most of the Avahi species have been named within the last ten years, mostly distinguished primarily or entirely by molecular evidence alone. The avahis are small, mostly brown and grey nocturnal lemurs that might be expected to be morphologically conservative but still, I can’t say as I’m entirely happy with the situation.

Indri, Indri indri. Need I say more. Photo from here.

The indri Indri indri is without a doubt the most remarkable of the indriids. The largest living lemur (up to 10 kg), the indri is immediately distinguished by its striking piebald coloration and vestigial tail. Indris live in small family groups. Groups communicate within themselves and with each other by means of loud calls that can be heard up to 2 km away. However, there seems to be no basis for the oft-repeated claim that the “indri” is miscalled and that the name is actually Malagasy for “there it goes” or “look at that” or something similar. As explained by Hacking (1981), the mistake was attributed to the naturalist Pierre Sonnerat, one of the first Europeans to observe the indri. However, Sonnerat’s experience with the indri was no brief encounter. Tame indri were often kept in the area in which he travelled (Markus Bühler, in a response to the “creepy Megaladapis” picture I posted a while back, informed me of a probably-apocryphal claim that tame indris were used to hunt birds) and Sonnerat himself took one back to France with him. Hacking (1981) points out that it strains credulity that Sonnerat could have become so familiar with the animal yet never had anyone correct him on a basic point. It is more likely that, as with a similar story about the kangaroo, the legend has developed from a failure to consider that different groups of people may use different names for the same animal.

The inside of an indri. Photo from here.
Why are there so many avahis?
Published 24 September 2013
Western woolly lemur Avahi occidentalis, photographed by Axeltelford.

One thing I briefly mentioned in the section above is that recent years have seen an apparent avalanche of new indriid species being described. But why has this happened, and how sturdy are these new distinctions?

In 1982, Tattersall provided an overview of Malagasy lemurs that recognised just four species of indriid: the indri Indri indri, the avahi Avahi laniger, Verreaux’s sifaka Propithecus verreauxi and the diademed sifaka P. diadema (Tattersall 2007). A fifth species was added in 2008, the golden-crowned sifaka P. tattersalli. But the real explosion has come in only the last ten years or so. Recent workers have proposed the recognition of seven species of sifaka (Mayor et al. 2004), and no less than nine species of avahi (Zaramody et al. 2006, Andriantompohavana et al. 2007, Lei et al. 2008). Each of the species within a genus is generally geographically separated from its congeners and some species are recorded only from very small ranges.

In the case of the sifakas, none of the new ‘species’ is actually a new taxonomic entity per se. With the exception of P. tattersalli, all were previously recognised previously as subspecies of either P. verreauxi or P. diadema. The most obvious differences between the various varieties of sifaka is coloration. As noted in the earlier post linked to above, popular depictions of sifakas are heavily biased towards P. [verreauxi] verreauxi, found in the south-west of Madagascar, with a white body and black skull-cap (photo below by Jouan & Rius):

However, the sifakas are much more varied than you might think from watching David Attenborough documentaries alone. As well as the red-and-black Propithecus [diadema] diadema illustrated in the earlier post, sifakas vary from the almost entirely black P. [diadema] perrieri of the far north of Madagascar (photograph by Pete Oxford):

to the almost entirely white north-eastern P. [diadema] candidus (photo by Kevin Schafer):

The various sifaka subspecies were analysed by Mayor et al. (2004), who identified them as genetically distinct as well as distinct in appearance, and therefore recommended treating them all as separate species. However, other authors such as Tattersall (2007) have pointed out that morphological distinctions between populations may become less clear when overall variation is considered.

The above photos, from Rakotonirina et al. (2014), show variation in sifakas at a single site in central-west Madagascar, near the boundary between the ranges of Propithecus [verreauxi] deckeni and P. [verreauxi] coronatus and including individuals that might be assigned on grounds of coloration to either taxon.

In the case of the avahis, things are even more convoluted than for the sifakas. While the diurnal sifakas may vary noticeably in external appearance, the nocturnal avahis keep to a more or less basic brown. There are some slight differences between avahis on the western and eastern sides of Madagascar that had lead to the recognition of two separate subspecies, Avahi laniger laniger in the east and A. l. occidentalis in the west. A. laniger and A. occidentalis were subsequently treated as separate species on the basis of differences in their karyotypes. Each has been further subdivided into multiple species largely on the basis of genetic data alone (though vocalisation data was also a factor in separating A. unicolor from A. occidentalis). What is more, the genetic distinctions have mostly been made on the basis of mitochondrial data only, and some ‘species’ have only been represented in analyses by data from a few individuals. Markolf et al. (2011) suggested that genetic species could not be distinguished reliably on the basis of such small samples because of the increased risk of confusing individual variation for species-level distinctions. In the majority of cases, differences in mitochondrial genes between Avahi samples have correlated with geographical separation, but there is at least one notable exception. The central-east Malagasy location of Ranomafana has provided samples that fall into three distinct haplotype clusters. Though recognised as a single species A. peyrierasi on the basis of their common distribution, these three clusters do not form a monophyletic group in phylogenetic analyses, and the geographically separate taxa A. betsileo, A. meridionalis and A. ramanantsoavana are all nested between the A. peyrierasi haplotypes (Lei et al. 2008).

Eastern woolly lemur Avahi laniger, photographed by Inaki Relanzon.

None of the Avahi species as currently recognised overlap in range. However, in a landmass that has lost four-fifths or more of its original forest cover, it is worth asking how much of this isolation is original, and how much man-made relictualism. As always in questions of scientific research, we are left noting that further investigation is required.

Systematics of Indridae

Characters (from Mivart 1866): Dental formula I2/2, C1/1, P2/2, I3/3. Ears short; muzzle long, moderate or short; hind legs much longer than fore limbs; index very short, much shorter than fifth digit; pollex short and placed far back; hallux very long and covered with hair; tail long, or very short and rudimentary; internal condyle of the humerus perforated; carpus destitute of an os intermedium; tarsus short; first upper molar with four large and four small prominences, no internal cingulum; last upper molar with two large anterior cusps and three very small posterior prominences; each lower incisor with its outer surface longitudinally grooved; lower premolar much antero-posteriorly extended; first lower molar with four or five cusps; last lower molar quinquecuspid; paramastoid process present; malar foramen absent; lachrymal foramen very near margin of orbit; masseteric surface of malar wide and ridged; process depending from zygoma just in front of, and external to, glenoid surface; postglenoidal foramen present; anterior palatine foramina very large; mandibular symphysis very long; condyle rounded, not transversely extended; articular surface prolonged somewhat down the back of ascending ramus; digastric fossa deep.

Indridae [Indriidae, Indriinae, Indrisinae]
    |  i. s.: Thaumastolemur Filhol 1895SM93
    |--Indri indriFS15
    `--+--Avahi Jourdan 1834FS15, N10 [incl. Semnocebus Lesson 1840N10]
       |    |--+--A. cleeseiFS15
       |    |  `--+--A. occidentalisFS15 [=A. laniger occidentalisPRM84]
       |    |     `--A. unicolorFS15
       |    `--+--A. peyrierasiFS15
       |       `--+--A. betsileoFS15
       |          `--+--A. ramanantsoavanaiFS15
       |             `--+--A. lanigerFS15 (see below for synonymy)
       |                `--A. meridionalisFS15
       `--Propithecus Bennet 1832FS15, SKS05
            |--+--P. diademaFS15
            |  |    |--P. d. diademaG91
            |  |    `--P. d. holomelasG91
            |  `--+--P. edwardsiFS15 [=P. diadema edwardsiG91]
            |     `--P. perrieriFS15 [=P. diadema perrieriBP87]
            `--+--+--P. coquereliFS15 [=P. verreauxi coquereliG91]
               |  `--+--P. candidusFS15 [=P. diadema candidusPRM84]
               |     `--P. tattersalliFS15
               `--+--P. verreauxiFS15 [incl. P. verreauxi majoriG91]
                  `--+--P. coronatusFS15 [=P. verreauxi coronatusBP87]
                     `--P. deckeniFS15 [=P. verreauxi deckeniBP87]

Avahi lanigerFS15 [=Lemur lanigerM66, Avahis lanigerM66, Indri lanigerM66, Indris lanigerM66, Lichanotus lanigerM66, Microrhynchus lanigerM66, Semnocebus lanigerM66; incl. Li. avahiM66, S. avahiM66, Lemur lanatusM66, Hadrocebus lanatusM66, Indris longicaudatusM66]

*Type species of generic name indicated

References

Andriantompohavana, R., R. Lei, J. R. Zaonarivelo, S. E. Engberg, G. Nalanirina, S. M. McGuire, G. D. Shore, J. Andrianasolo, K. Herrington, R. A. Brenneman & E. E. Louis Jr. 2007. Molecular phylogeny and taxonomic revision of the woolly lemurs, genus Avahi (Primates: Lemuriformes). Special Publications, Museum of Texas Tech University 51: 1–59.

[BP87] Burton, J. A., & B. Pearson. 1987. Collins Guide to the Rare Mammals of the World. Collins: London.

[FS15] Faurby, S., & J.-C. Svenning. 2015. A species-level phylogeny of all extant and late Quaternary extinct mammals using a novel heuristic-hierarchical Bayesian approach. Molecular Phylogenetics and Evolution 84: 14–26.

[G91] Groves, C. P. 1991. A Theory of Human and Primate Evolution revised ed. Clarendon Press: Oxford.

Hacking, I. 1981. Was there ever a radical mistranslation? Analysis 41 (4): 171–175.

Lei, R., S. E. Engberg, R. Andriantompohavana, S. M. McGuire, R. A. Mittermeier, J. R. Zaonarivelo, R. A. Brenneman & E. E. Louis. 2008. Nocturnal lemur diversity at Masoala National Park. Special Publications, Museum of Texas Tech University 53: 1–41.

Marivaux, L., J.-L. Welcomme, P.-O. Antoine, G. Métais, I. M. Baloch, M. Benammi, Y. Chaimanee, S. Ducrocq & J.-J. Jaeger. 2001. A fossil lemur from the Oligocene of Pakistan. Science 294: 587–591.

Markolf, M., M. Brameier & P. M. Kappeler. 2011. On species delimitation: yet another lemur species or just genetic variation? BMC Evolutionary Biology 11: 216.

Mayor, M. I., J. A. Sommer, M. L. Houck, J. R. Zaonarivelo, P. C. Wright, C. Ingram, S. R. Engel & E. E. Louis Jr. 2004. Specific status of Propithecus spp. International Journal of Primatology 25 (4): 875–900.

Mittermeier, R. M., J. U. Ganzhorn et al.. 2008. Lemur diversity in Madagascar. International Journal of Primatology 29 (6): 1607–1656.

[M66] Mivart, St. G. J. 1866. On the structure and affinities of Microrhynchus laniger. Proceedings of the Zoological Society of London 1866: 151–167.

[N10] Naish, D. 2010. Tetrapod Zoology: Book One. CFZ Press: Bideford (UK).

Nowak, R. M. 1999. Walker’s Mammals of the World 6th ed. vol. 1. JHU Press.

Orlando, L., S. Calvignac, C. Schnebelen, C. J. Douady, L. R. Godfrey & C. Hänni. 2008. DNA from extinct giant lemurs links archaeolemurids to extant indriids. BMC Evolutionary Biology 8: 121.

[PRM84] Pollock, J. I., A. F. Richard & R. D. Martin. 1984. Lemurs. In: Macdonald, D. (ed.) All the World’s Animals: Primates pp. 24–35. Torstar Books: New York.

Rakotonirina, L. H. F., F. Randriantsara, A. H. Rakotoarisoa, R. Rakotondrabe, J. Razafindramanana, J. Ratsimbazafy & T. King. 2014. A preliminary assessment of sifaka (Propithecus) distribution, chromatic variation and conservation in western central Madagascar. Primate Conservation 28: 43–53.

[SKS05] Scherf, H., B. Koller & F. Schrenk. 2005. Locomotion-related structures in the femoral trabecular architecture of primates and insectivores (Mammalia, Primates and Insectivora). Senckenbergiana Biologica 85 (1): 101–112.

[SM93] Stucky, R. K., & M. C. McKenna. 1993. Mammalia. In: Benton, M. J. (ed.) The Fossil Record 2 pp. 739–771. Chapman & Hall: London.

Tattersall, I. 2007. Madagascar’s lemurs: cryptic diversity or taxonomic inflation? Evolutionary Anthropology 16: 12–23.

Zaramody, A., J.-L. Fausser, C. Roos, D. Zinner, N. Andriaholinirina, C. Rabarivola, I. Norscia, I. Tattersall & Y. Rumpler. 2006. Molecular phylogeny and taxonomic revision of the eastern woolly lemurs (Avahi laniger). Primate Report 74: 9–23.

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