The measurement data collected and compared for this study show that tooth size is correlated with body size which probably explains in part the polarization of Microcebus and
Palaeopropithecus on Canonical Scores Axis 1 (Figure 7). An eclectic diet probably characterized Megaladapis as indicated by predicted fruit and leaf gradients (Table 11).
Megaladapis is separated from the other taxa on Canonical Scores Axis 2 (Figure 7), perhaps from the emphasis on folivorous resources over fruit compared to the other subfossil lemurs
examined, as well as the relatively large mesiolingual and buccolingual lengths of M3 (Table 11).
The multiple linear regression coefficients from extant taxa help reinforce the
discriminant function analysis with both living and extinct lemurs. The coefficients which are the most extreme include the mesiodistal length of M1, the metric dimensions of M3, coarse scratches and hypercoarse scratches (Table 9). All of these variables are important in distinguishing extant and extinct taxa along canonical scores axes (Table 10).
Size is certainly important in differentiating taxa on the first canonical scores axis given the relatively larger loadings for some of the dental measurements (Table 10). However, dental microwear features also load heavily on both canonical scores axes suggesting they are
influential in separating individuals, and predicting the diet of subfossil lemurs. Classification rates of fruit and leaf gradients based on the dental microwear of extant taxa are rather low overall (Tables 7 and 8). However, for those taxa with more specialized folivorous diets with little fruit (leaf gradient = 3 and fruit gradients 1 and 2) have much higher classification rates (Tables 7 and 8). For this reason, there is more confidence in predicting the diet of Megaladapis
(leaf gradient = 3) than the other subfossil lemurs (Table 11).
Megaladapis, had the greatest number of scratches compared to the other taxa. Similar results in previous research suggest that the diet of Megaladapis was dominated by leaf
consumption with some fruit consumed as well. The most similar results for extant lemurs was that of Hapalemur, which displayed far more scratches than pits from the exploitation of bamboo (Ganzhorn et al. 2006; Godfrey et al. 2004; Godfrey et al. 2006; Gould et al. 2011).
The Archaeolemur specimens examined have a large variance in number of pits and scratches, which could indicate the processing of more hard-object foods, as the literature
suggests and possibly a diet that features a large amount of grit. These findings could indicate that site location plays an important factor in determining past diet for Archaeolemur and that information about the grit content at past sites can impact the amount of variation in microwear features for Archaeolemur (Ungar et al 1995; Godfrey et al 2004).
Of the Palaeopropithecidae examined, Palaeopropithecus and Mesopropithecus were a mixture of folivory and frugivory based on the microwear analysis. These findings were
supported by previous research (Ganzhorn et al. 2006, Godfrey et al. 2004, Godfrey et al. 2006; Gould et al. 2011) and confirmed in Table 11.
Pachylemur had a varied number of pits for the majority of the specimen examined, but overall a larger number of scratches were observed. The differences in these observed features can partially be attributed to the small number of Pachylemur specimens within this study. Using the results from this study, it is suggested that Pachylemur fed on leaves and fruit as predicted in Table 11, although an accurate proportion of each in the diet, cannot be determined (Godfrey et al. 2004, Godfrey et al. 2006).
The subfossil lemurs grouped most closely with Propithecus which has a diet comprising folivorous and frugivorous resources. Prolemur consumes bamboo and does have more
scratches, indicative of their pith-dominated diet. Microcebus is the only taxon examined identified as an insectivore and a preference for fruit. Eulemur samples were mixed between frugivory and folivory, which is to be expected with the fluctuation of diet based on seasonal food availability (Ganzhorn et al. 2006; Godfrey et al. 2004; Godfrey et al. 2006; Gould et al. 2011).
4 CONCLUSIONS
In summary, grit does accumulate more frequently on leaves that are on a trail when compared to leaves collected off of main trails in a fragmented forest. Based on these
conclusions, the presence of open space, no matter the size, critically affects the amount of grit that accumulates in the canopy of a forest. Edge environments and forests that are extremely fragmented are most affected by this phenomenon and would be expected to affect the wear on the dentition of primates frequenting these areas. Edge habitats accumulate a significantly greater grit density in comparison to the nonsignificant differences in grit with respect to canopy height. This could have major implications for the way that microwear is formed on the teeth of primates living in these forests or any environment that is affected by humans. Forests that are made up entirely of fragments are drier environments and would be expected to be greatly affected by this phenomenon. Primates living in these areas would be expected to exhibit greater density of microwear features, particularly those associated with hard object consumption, because of the greater accumulation of grit than is observed in the canopy.
A study such as this provides invaluable information about the effects of grit and
microwear creation. A more complete reconstruction of diet of extinct primates could be formed by studying the fragmentation of their habitats and could also aid in aging specimens in degraded habitats. More dental microwear would be expected on dentition of primates living in a more fragmented area that contains more edge habitats. The arrival of humans in places such as Madagascar should show an increase in heavy dental microwear features on the dentition of subfossil lemurs.
REFERENCES
Ankel-Simons, F. 2007. Primate Anatomy. Pp 248-391. Elsevier Academic Press.
Burney, D.A., Burney, L.P., Godfrey, L.R., Jungers, W.L., Goodman, S.M., Wright, H.T., Jull, A.J.T. 2004. A chronology for late prehistoric Madagascar. Journal of Human Evolution 47: 25-63.
Crowley, B.E., Godfrey, L.R., and Irwin, M.T. 2011. A glance to the past: subfossils, stable isotopes, seed dispersal, and lemur species loss in southern Madagascar. American Journal of Primatology 73: 25-37.
Crowley, B.E. and Godfrey, L.R. 2013. Why all those spines? Anachronistic defences in the Didiereoideae against now extinct lemurs. South African Journal of Sciences 109: 1-2. Dewar, R.E., Radimilahy, C., Wright, H.T., Jacobs, Z., Kelly, G.O., and Berna, F. 2013. Stone
tools and foraging in northern Madagascar challenge Holocene extinction models. PNAS 110: 12583-12588.
Dumont, E.R., Ryan, T.M., and Godfrey, L.R. 2011. The Hadropithecus conundrum
reconsidered, with implications for interpreting diet in fossil hominins. Proceedings: Biological Sciences 278: 3654-3661.
Ganzhorn, J.U., Goodman, S.M., Nash, S., and Thalmann, U. 2006. Lemur biogeography. In
Primate Biogeography: Progress and Prospects. Pp. 229-254. New York: Springer Science+Business Media, LLC.
Gingerich, P.D., Smith, H., and Rosenberg, K. 1982. Allometric Scaling in the Dentition of primates and prediction of body weight from tooth size in fossils. American Journal of Physical Anthropology 58: 81-100.
Godfrey, L.R., Semprebon, G.M., Jungers, W.L., Sutherland, M.R., Simons, E., and Solounias, N. 2004. Dental use wear in extinct lemurs: evidence of diet and niche differentiation. Journal of Human Evolution 47: 145-169.
Godfrey, L.R., Jungers, W.L., and Schwartz, G.T. 2006. Ecology and extinction of Madagascar’s
subfossil lemurs. In Lemurs: ecology and adaptation. Lisa Gould and Michelle Sauther, eds. Pp. 41-64. New York: Springer Science + Business Media, LLC.
Godfrey, L.R., Jungers, W. L., and Burney, D.A. 2010. Subfossil Lemurs of Madagascar. In
Cenozoic Mammals of Africa. Werdelin, L. and Sanders, W., eds. Pp. 351-367. University of California Press.
Godfrey, L.R., Crowley, B.R., Muldoon, K.M., Kelley, E.A., King, S.J., Best, A.W., and Berthaume, MA. 2016. What did Hadropithecus eat and why should paleoanthropologists care? American Journal of Primatology 78:1098-1112.
Gould, L., Sauther, M., and Cameron, A. 2011. Lemuriformes. In Primates in Perspective. C.J. Campbell, A. Fuentes, K.C. MacKinnnon, S.K. Bearder, and R.M. Stumpf, eds. Pp. 55-79. Oxford: Oxford University Press.
Hapke, A., Schülke, O., Zischler, H. 2003. Microsatellite markers for paternity testing in fork- marked lermurs (Phaner furcifer). Molecular Ecology Notes 3: 438-440.
Hillson, S. 1996. Dental anthropology. Cambridge: University Press.
Irwin, M. 2007. Living in forest fragments reduces group cohesion in diademed sifakas
(Propithecus diadema) in Eastern Madagascar by reducing food patch size. American
Journal of Primatology 69:434–447.
Irwin, M. 2008. Feeding Ecology of Propithecus diadema in Forest Fragments and Continous Forest. International Journal of Primatology 29: 95-115.
Jungers, W.L., Godfrey, L.R., Simons, E.L., Wunderlich, R.E., Richmond, B.G., and Chatrath, P.S. 2002. Ecomorphology and behavior of giant extinct lemurs from Madagascar. In
Reconstructing Behavior in the Primate Fossil Record. Plavcan et al., eds. Pp. 371-411. New York: Kluwer Academic/Plenum Publishers.
Junge, R.E., Barrett, M. A., and Yoder, A. D. 2011. Effects of anthropogenic disturbance on Indri (Indri indri) health in Madagascar. American Journal of Primatology 73: 633-642. King, T., Andrews, P., and Boz, B. 1999. Effect of taphonomic processes on dental microwear.
American Journal of Physical Anthropology 108:359-373.
Kistler, L., Ratan, A., Godfrey, L.R., Crowley, B.R., Hughes, C.E., Lei, R., Cui, Y., Wood, M.L., Muldoon, K.M., Andriamialison, H., McGraw, J.J., Tomsho, L.P, Schuster, S.C., Miller, W., Louis, E.E., Yoder, A.D., Malhi, R.S., Perry, G.H. 2015. Comparative and population mitogenomic analyses of Madagascar’s extinct, giant ‘subfossil’ lemurs. Journal of
Human Evolution 79: 45-54.
Lehman, S.M. and Fleagle, J.G. 2006. Madagascar. In Primate Biogeography: progress and prospects. Pp. 225-228. New York: Springer Science+Business Media, LLC.
Lucas, P. W., Omar, R., Al-Fadhalah, K., Almusallam, A. S., Henry, A. G., Michael, S., Thai, L. A., Watzke, J., Strait, D. S. and Atkins, A. G. 2013. Mechanisms and causes of wear in tooth enamel: implications for hominin diets. Journal of the Royal Society Interface 10: 20120923.
Orlando, L., Calvignac, S., Sechnebelen, C., Douady, C.J., Godfery, L.R., and Hänni, C. 2008. DNA from extinct giant lemurs links archaeolemurids to extant indriids. BMC
Perez, V.R., Godfrey, L.R., Nowak-Kemp, M., Burney, D.A., Ratsimbazafy, J. Vasey, N. 2005. Evidence of early butchery of giant lemurs in Madagascar. Journal of Human Evolution 49: 722-742.
Richard, A.F. and Dewar, R.E. 1991. Lemur Ecology. Annual Review of Ecology and Systematics 22:145-175.
Scott, R.S., Ungar, P. S., Bergstrom, T.S., Brown, C.A., Grine, F.E., Teaford, M. F., and Walker, A. 2005. Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436(4): 693-695.
Scott, J.R., Godfrey, L.R., Jungers, W. L., Scott, R. S., Simons, E.L., Teaford, M. F., Ungar, P. S and Walker, A. 2009. Dental microwear texture analysis of two families of subfossil lemurs from Madagascar. Journal of Human Evolution 56:405-416.
Simons, E.L., Godfrey, L.R., Jungers, W.L., Chatrath, P.S., and Rakotosamimanana, B. 1992. A new giant subfossil lemur, Babakotia, and the evolution of the sloth lemurs. Folia
Primatologica 58: 197-203.
Simons, E.L. 1994. The giant aye-aye Daubentonia robusta. Folia Primatologica 62:14-21. Swindler, D.R. 2002. Primate Dentition: An introduction to the teeth of non-human primates.
Pp.60-83. United Kingdom: Cambridge University Press.
Tattersall, I. 1982. Primates of Madagascar. Pp. 206-245. New York: Columbia University Press. Tattersall, I. 2006. Origin of the Malagasy Strepsirhine Primates. In Lemurs: ecology and
adaptation. Lisa Gould and Michelle Sauther, eds. Pp. 3-17. New York: Springer Science + Business Media, LLC.
Ungar, P.S., Teaford, M.F., Glander, K. E., and Pastor, R. F. 1995. Dust Accumulation in the Canopy: A Potential Cause of Dental Microwear in Primates. American Journal of Physical Anthropology 97: 93-99.
Williams, F. L. and Holmes, N. A. 2012. Dental microwear texture analysis of late Pliocene
Procynocephalus subhimalayanus (Primates: Cercopithecidae) of the Upper Siwaliks, India. Central European Journal of Geosciences 4(3): 425-438.
Williams F.L. and Geissler E. 2014. Reconstructing the diet and paleoecology of Plio-
Pleistocene Cercopithecoides williamsi from Sterkfontein, South Africa. Palaios 29: 483- 494.
APPENDICES Appendix A
Appendix A.1 Specimen
number
Site name Genus
Tsiandroina Pachylemur UA 5300 Tsirave Pachylemur UA 5310 Tsirave Pachylemur Tsirave Pachylemur Tsirave Pachylemur UA 5308 Tsirave Pachylemur
UA5306 Tsirave Pachylemur
UA 5290 Ampasambazimba Pachylemur UA 5289 Ampasambazimba Pachylemur UA 5309 Tsirave Pachylemur UA 5299 Tsirave Pachylemur UA 5307 Tsirave Pachylemur UA 5312 Tsirave Pachylemur UA 5301 Tsirave Pachylemur UA 5461 Paleopropithecus UA 5447 Ampasambazimba Paleopropithecus UA 5452 Ampasambazimba Paleopropithecus PpH7 Paleopropithecus
UA 5451 Paleopropithecus UA 4467 Paleopropithecus UA 5449 Betioky Paleopropithecus UA 5459 Paleopropithecus UA 5453 Paleopropithecus UA 5454 Paleopropithecus UA Y Archaeolemur UA 5399 Archaeolemur UA 3338 Anj? Archaeolemur Archaeolemur UA 5351 Ampasambazimba Archaeolemur UA 5348 Ampasambazimba Archaeolemur
UA5366 Beloha Anavoha Archaeolemur
UA 5397 Archaeolemur
UA 5373 Beloha Anavoha Archaeolemur
UA 5376 Bemafandry Archaeolemur UA 5349 Ampasambazimba Archaeolemur UA 5350 Ampasambazimba Archaeolemur UA 5387 Tsirave Archaeolemur UA 5400 Archaeolemur UA 5377 Bevoha Archaeolemur UA 5166 Ampasambazimba Archaeolemur UA 5398 Ampasambazimba Archaeolemur
UA 5363 Beloha Anavoha Archaeolemur UA 5417 Tsirave Archaeolemur UA 5386 Morarano Archaeolemur UA 2827 Ankarana Archaeolemur UA X Bemafandry Archaeolemur UA 5352 Ampasambazimba Archaeolemur UA 5346 Ampasambazimba Archaeolemur UA 5169 Ampasambazimba Hadropithecus UA 5173 Tsirave Hadropithecus
UA 5174 Belo Sur Mer Hadropithecus
Tsirave Megaladapis
UA5484 Beloha Anavoha Megaladapis
UA 5492 Beloha Anavoha Megaladapis
MpH2 Ampasambazimba Mesopropithecus
Beloha Anavoha Mesopropithecus
Ankarana Mesopropithecus
Subfossil lemurs by genus and specimen number in this study3
Appendix A.2 Genus N Archaeolemur 9 Cheirogaleus 3 Eulemur 23 Hapalemur 3 Prolemur 15 Propithecus 42 Megaladapis 3 Mesopropithecus 2 Microcebus 14 Pachylemur 4 Palaeopropithecus 2