Why Are There So Many Avahis?

Western woolly lemur Avahi occidentalis, photographed by Axeltelford.

A few years back, I wrote a post on the lemur family Indriidae: the indri, the avahis, the sifakas. One thing I briefly mentioned in that post 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. (2013), 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.

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.

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.

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.

Rakotonirina, L. H. F., F. Randriantsara, A. H. Rakotoarisoa, R. Rakotondrabe, J. Razafindramanana, J. Ratsimbazafy & T. King (in press, 2013). A preliminary assessment of sifaka (Propithecus) distribution, chromatic variation and conservation in western central Madagascar. Primate Conservation.

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.