Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-25T10:53:58.267Z Has data issue: false hasContentIssue false
  • English
  • Français

Reconstructing dietary ecology of extinct strepsirrhines (Primates, Mammalia) with new approaches for characterizing and analyzing tooth shape

Published online by Cambridge University Press:  26 March 2021

Ethan L. Fulwood Open the ORCID record for Ethan L. Fulwood [Opens in a new window] ,
Shan Shan ,
Julia M. Winchester ,
Tingran Gao ,
Henry Kirveslahti ,
Ingrid Daubechies  and
Doug M. Boyer
Ethan L. Fulwood*
Affiliation:
Department of Neuroscience, Washington University in St. Louis School of Medicine, St. Louis, Missouri63110, U.S.A.; and Department of Evolutionary Anthropology, Duke University, Durham, North Carolina27708, U.S.A. E-mail: ethanfulwood@upike.edu
Shan Shan
Affiliation:
Department of Mathematics, Duke University, Durham, North Carolina27708U.S.A.
Julia M. Winchester
Affiliation:
Department of Evolutionary Anthropology, Duke University, Durham, North Carolina27708, U.S.A.
Tingran Gao
Affiliation:
Department of Statistics, University of Chicago, Chicago, Illinois60637, U.S.A.
Henry Kirveslahti
Affiliation:
Department of Statistical Science, Duke University, Durham, North Carolina27708, U.S.A.
Ingrid Daubechies
Affiliation:
Department of Mathematics, Duke University, Durham, North Carolina27708U.S.A.
Doug M. Boyer
Affiliation:
Department of Evolutionary Anthropology, Duke University, Durham, North Carolina27708, U.S.A.
*
*Corresponding author.
Get access Rights & Permissions [Opens in a new window]

Abstract

The morphological and ecological diversity of lemurs and lorisiformes once rivaled that of the rest of the primate order. Here, we assemble a dataset of 3D models representing the second mandibular molars of a wide range of extant and fossil strepsirrhines encompassing this diversity. We use these models to distill quantitative descriptors of tooth form and then analyze these data using new analytical methods. We employ a recently developed dental topography metric (ariaDNE), which is less sensitive to details of random error in 3D model quality than previously used metrics (e.g., DNE); Bayesian multinomial modeling with metrics designed to measure overfitting risk; and a tooth segmentation algorithm that allows the shapes of disaggregated tooth surface features to be quantified using dental topography metrics. This approach is successful at reclassifying extant strepsirrhine primates to known dietary ecology and indicates that the averaging of morphological information across the tooth surface does not interfere with the ability of dental topography metrics to predict dietary adaptation. When the most informative combination of dental topography metrics is applied to extinct species, many subfossil lemurs and the most basal fossil strepsirrhines are predicted to have been primarily frugivorous or gummivorous. This supports an ecological contraction among the extant lemurs and the importance of frugivory in the origins of crown Strepsirrhini, potentially to avoid competition with more insectivorous and folivorous members of Paleogene Afro-Arabian primate faunas.

Type
Articles
Information
Paleobiology , Volume 47 , Issue 4 , November 2021 , pp. 612 - 631
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of The Paleontological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Present address: Kentucky College of Osteopathic Medicine, Pikeville, Kentucky 41501, U.S.A.

‡

Present address: Department of Mathematics and Statistics, Mt. Holyoke College, South Hadley, Massachusetts 01075, U.S.A.

References

Literature Cited

Al-Aifari, R., Daubechies, I., and Lipman, Y.. 2013. Continuous Procrustes distance between two surfaces. Communications on Pure and Applied Mathematics 66:934–964.CrossRefGoogle Scholar
Allen, K.L., Cooke, S. B., Gonzales, L. A., and Kay, R. F.. 2015. Dietary inference from upper and lower molar morphology in platyrrhine primates. PLoS ONE 10:e0118732.CrossRefGoogle ScholarPubMed
Balko, E.A. 1998. A behaviorally plastic response to forest composition and logging disturbance by Varecia variegata in Ranomafana National Park, Madagascar. Ph.D. dissertation. Syracuse University, Syracuse, N.Y.Google Scholar
Bearder, S. K., and Martin, R. D.. 1980. Acacia gum and its use by bushbabies, Galago senegalensis (Primates: Lorisidae). International Journal of Primatology 1:103–128.CrossRefGoogle Scholar
Berthaume, M. A., Winchester, J., and Kupczik, K.. 2019. Effects of cropping, smoothing, triangle count, and mesh resolution on 6 dental topographic metrics. PLoS ONE 14:e0216229.CrossRefGoogle ScholarPubMed
Bhullar, B. A. S., Manafzadeh, A. R., Miyamae, J. A., Hoffman, E. A., Brainerd, E. L., Musinsky, C., and Crompton, A. W.. 2019. Rolling of the jaw is essential for mammalian chewing and tribosphenic molar function. Nature 566:528–532.CrossRefGoogle ScholarPubMed
Boyer, D. M. 2008. Relief index of second mandibular molars is a correlate of diet among prosimian primates and other euarchontan mammals. Journal of Human Evolution 55:1118–1137.CrossRefGoogle ScholarPubMed
Britt, A., Randriamandratonirina, N. J., Glasscock, K. D., and Iambana, B. R.. 2002. Diet and feeding behaviour of Indri indri in a low-altitude rain forest. Folia Primatologica 73:225–239.CrossRefGoogle Scholar
Bunn, J. M., and Ungar, P. S.. 2009. Dental topography and diets of four Old World monkey species. American Journal of Primatology 71:466–477.CrossRefGoogle ScholarPubMed
Bunn, J. M., Boyer, D. M., Lipman, Y., St. Clair, E. M., Jernvall, J., and Daubechies, I.. 2011. Comparing Dirichlet normal surface energy of tooth crowns, a new technique of molar shape quantification for dietary inference, with previous methods in isolation and in combination. American Journal of Physical Anthropology 145:247–261.CrossRefGoogle ScholarPubMed
Bürkner, P. C. 2017. brms: an R package for Bayesian multilevel models using Stan. Journal of Statistical Software 80:1–28.CrossRefGoogle Scholar
Bürkner, P. C. 2020. Estimating phylogenetic multilevel models with brms. https://cran.r-project.org/web/packages/brms/vignettes/brms_phylogenetics.html, accessed 7 January 2021.Google Scholar
Burrows, A. M., and Nash, L. T.. 2010. Searching for dental signals of exudativory in Galagos. Pp. 211–233 in Burrows, A. M. and Nash, L. T., eds. The evolution of exudativory in primates. Springer, New York.CrossRefGoogle Scholar
Charles-Dominique, P. 1977. Ecology and behaviour of nocturnal primates: prosimians of equatorial West Africa. Columbia University Press, New York.Google Scholar
Charles-Dominique, P. 1979. Field studies of lorisid behavior: methodological aspects. Study of Prosimian Behavior. Academic Press, Cambridge, Mass.Google Scholar
Crompton, A. W. 1970. Functional significance of the therian molar pattern. Nature 227:197–199.CrossRefGoogle ScholarPubMed
Cuozzo, F. P., and Yamashita, N.. 2006. Impact of ecology on the teeth of extant lemurs: a review of dental adaptations, function, and life history. Pp. 67–96 in Gould, L. and Sauther, M. L., eds. Lemurs: ecology and adaptation. Springer, New York.CrossRefGoogle Scholar
Dammhahn, M., and Kappeler, P. M. 2008. Small-scale coexistence of two mouse lemur species (Microcebus berthae and M. murinus) within a homogeneous competitive environment. Oecologia 157:473–483.CrossRefGoogle Scholar
Erhart, E. M., Tecot, S. R., and Grassi, C.. 2018. Interannual variation in diet, dietary diversity, and dietary overlap in three sympatric strepsirrhine species in southeastern Madagascar. International Journal of Primatology 39:289–311.CrossRefGoogle Scholar
Evans, A. R. 2013. Shape descriptors as ecometrics in dental ecology. Hystrix: Italian Journal of Mammalogy 24:133–140.Google Scholar
Evans, A. R., and Jernvall, J.. 2009. Patterns and constraints in carnivoran and rodent dental complexity and tooth size. Journal of Vertebrate Paleontology 29:24A.Google Scholar
Evans, A. R., and Pineda-Munoz, S.. 2018. Inferring mammal dietary ecology from dental morphology. Pp. 37–51 in Croft, D. A., Su, D., and Simpson, S. W., eds. Methods in paleoecology. Springer, New York.CrossRefGoogle Scholar
Evans, A. R., and Sanson, G. D. 2003. The tooth of perfection: functional and spatial constraints on mammalian tooth shape. Biological Journal of the Linnean Society 78:173–191.CrossRefGoogle Scholar
Evans, A. R., Wilson, G. P., Fortelius, M., and Jernvall, J.. 2007. High-level similarity of dentitions in carnivorans and rodents. Nature 445:78–81.CrossRefGoogle ScholarPubMed
Fietz, J., and Ganzhorn, J. U.. 1999. Feeding ecology of the hibernating primate Cheirogaleus medius: how does it get so fat? Oecologia 121:157–164.CrossRefGoogle ScholarPubMed
Fortelius, M., Eronen, J., Jernvall, J., Liu, L., Pushkina, D., Rinne, J., Tesakov, A., Vislobokova, I., Zhang, Z., and Zhou, L.. 2002. Fossil mammals resolve regional patterns of Eurasian climate change over 20 million years. Evolutionary Ecology Research 4:1005–1016.Google Scholar
Ganzhorn, J. U. 1992. Leaf chemistry and the biomass of folivorous primates in tropical forests. Oecologia 91:540–547.CrossRefGoogle ScholarPubMed
Ganzhorn, J. U., Abraham, J. P., and Razanahoera-Rakotomalala, M.. 1985. Some aspects of the natural history and food selection of Avahi laniger. Primates 26:452–463.CrossRefGoogle Scholar
Gao, T. 2015. Hypoelliptic diffusion maps and their applications in automated geometric morphometrics. Ph.D. thesis. Duke University, Durham, N.C.Google Scholar
Gao, T. 2021. The diffusion geometry of fibre bundles: horizontal diffusion maps. Applied and Computational Harmonic Analysis 50:147–215.CrossRefGoogle Scholar
Gao, T., Yapuncich, G. S., Daubechies, I., Mukherjee, S., and Boyer, D. M.. 2018. Development and assessment of fully automated and globally transitive geometric morphometric methods, with application to a biological comparative dataset with high interspecific variation. Anatomical Record 301:636–658.CrossRefGoogle ScholarPubMed
Godfrey, L. R. 2017. Subfossil lemurs. In Fuentes, A. et al. , eds. The international encyclopedia or primatology. Wiley, New York.Google Scholar
Godfrey, L. R., Semprebon, G. M., Jungers, W. L., Sutherland, M. R., Simons, E. L., and Solounias, N.. 2004. Dental use wear in extinct lemurs: evidence of diet and niche differentiation. Journal of Human Evolution 47:145–169.CrossRefGoogle ScholarPubMed
Godfrey, L. R., Semprebon, G. M., Schwartz, G. T., Jungers, W. L., Flanagan, E. K., Cuozzo, F. P., and King, S. J.. 2005. New insights into old lemurs: the tropic adaptations of the Archaeolemuridae. International Journal of Primatology 26:825–854.CrossRefGoogle Scholar
Godfrey, L. R., Jungers, W. L., and Schwartz, G. T.. 2006. Ecology and extinction of Madagascar's subfossil lemurs. Pp. 41–64 in Gould, L. and Sauther, M. L., eds. Lemurs: ecology and adaptation. Springer, New York.CrossRefGoogle Scholar
Godfrey, L. R., Winchester, J. M., King, S. J., Boyer, D. M., and Jernvall, J.. 2012. Dental topography indicates ecological contraction of lemur communities. American Journal of Physical Anthropology 148:215–227.CrossRefGoogle ScholarPubMed
Godfrey, L. R., Crowley, R. E., Muldoon, K. M., Kelley, E. A., King, S. J., Best, A. W., and Berthaume, A.. 2016. What did Hadropithecus eat, and why should palaeoanthropologists care? American Journal of Primatology 78:1098–1112.CrossRefGoogle Scholar
Goodman, S. M., and Ganzhorn, J. U.. 1997. Rarity of figs (Ficus) on Madagascar and its relationship to a depauperate frugivore community. Revue d'Ecologie 52:321–329.Google Scholar
Gould, L. 2006. Lemur catta ecology: what we know and what we need to know. Pp. 255–274 in Gould, L. and Sauther, M. L., eds. Lemurs: ecology and adaptation. Springer, New York.CrossRefGoogle Scholar
Gregory, W. K. 1922. Origin and evolution of the human dentition. Williams and Wilkins, Baltimore.Google Scholar
Harcourt, C. 1986. Seasonal variation in the diet of South African galagos. International Journal of Primatology 7:491–506.CrossRefGoogle Scholar
Harcourt, C. 1991. Diet and behaviour of a nocturnal lemur, Avahi laniger, in the wild. Journal of Zoology 223:667–674.CrossRefGoogle Scholar
Harcourt, C. S., and Nash, L. T.. 1986. Species differences in substrate use and diet between sympatric galagos in two Kenyan coastal forests. Primates 27:41–52.CrossRefGoogle Scholar
Hemingway, C. A. 1996. Morphology and phenology of seeds and whole fruit eaten by Milne-Edwards’ sifaka, Propithecus diadema edwardsi, in Ranomafana National Park, Madagascar. International Journal of Primatology 17:637–659.CrossRefGoogle Scholar
Herrera, J. P., and Dávalos, L. M.. 2016. Phylogeny and divergence times of lemurs inferred with recent and ancient fossils in the tree. Systematic Biology 65:772–791.CrossRefGoogle ScholarPubMed
Hladik, C. M. 1979. Diet and ecology of prosimians. Pp. 307–357 in Doyle, G. A., ed. Study of prosimian behavior. Academic Press, Cambridge, Mass.CrossRefGoogle Scholar
Hladik, C. M., Charles-Dominique, P., and Petter, J. J.. 1980. Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. Pp. 41–73 in Charles-Dominique, P., ed. Nocturnal Malagasy primates: ecology, physiology, and behaviour. Academic Press, Cambridge, Mass.Google Scholar
Housworth, E. A., Martins, E. P., and Lynch, M.. 2004. The phylogenetic mixed model. American Naturalist 163:84–96.CrossRefGoogle ScholarPubMed
Jardine, P. E., Janis, C. M., Sahney, S., and Benton, M. J.. 2012. Grit not grass: concordant patterns of early origin of hypsodonty in Great Plains ungulates and Glires. Palaeogeography, Palaeoclimatology, and Palaeoecology 365:1–10.CrossRefGoogle Scholar
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. Pp. 371–411 in Plavcan, J., Kay, R. F., Jungers, W., and van Schaik, C. P., eds. Reconstructing behavior in the primate fossil record. Springer, New York.CrossRefGoogle Scholar
Kay, R. F. 1975. The functional adaptations of primate molar teeth. American Journal of Physical Anthropology 43:195–215.CrossRefGoogle ScholarPubMed
Kay, R. F. 1977. The evolution of molar occlusion in the Cercopithecidae and early catarrhines. American Journal of Physical Anthropology 46:327–352.CrossRefGoogle ScholarPubMed
Kay, R. F. 1978. Molar structure and diet in extant Cercopithecidae. Pp. 309–339 in Teaford, M. F., Smith, M. M., and Ferguson, M. W. J., eds. Development, function, and evolution of teeth. Academic Press, New York.Google Scholar
Kay, R. F., and Covert, H. H.. 1984. Anatomy and behaviour of extinct primates. Pp. 467–508 in Chivers, D. J., Wood, B. A., and Bilsborough, A., eds. Food acquisition and processing in primates. Springer, New York.CrossRefGoogle Scholar
Kay, R. F., and Hiiemae, K. M.. 1974. Jaw movement and tooth use in recent and fossil primates. American Journal of Physical Anthropology 40:227–256.CrossRefGoogle ScholarPubMed
Kay, R. F., and Hylander, W. L.. 1978. The dental structure of mammalian folivores with special reference to Primates and Phalangeroidea (Marsupialia). Pp. 173–191 in Montgomery, G. G., ed. The ecology of arboreal folivores. Smithsonian Institution Press, Washington, D.C.Google Scholar
Kay, R. F., and Simons, E. L.. 1980. The ecology of Oligocene African Anthropoidea. International Journal of Primatology 1:21–37.CrossRefGoogle Scholar
Kay, R. F., and Ungar, P. S.. 1997. Dental evidence for diet in some Miocene catarrhines with comments on the effects of phylogeny on the interpretation of adaptation. Pp. 131–151 in Begun, D. R., Ward, C. V., and Rose, M. D., eds. Function, phylogeny, and fossils. Springer, New York.CrossRefGoogle Scholar
Kirk, E. C., and Simons, E. L.. 2000. Diets of fossil primates from the Fayum Depression of Egypt: a quantitative analysis of molar shearing. Journal of Human Evolution 40:203–229.CrossRefGoogle Scholar
Lahann, P. 2007. Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar. Journal of Zoology 271:88–98.CrossRefGoogle Scholar
López-Torres, S., Keegan, S. R., Prufrock, K. A., Lin, D., and Silcox, M. T. 2017. Dental topographic analysis of paromomyid (Plesiadapiformes, Primates) cheek teeth: more than 15 million years of changing surfaces and shifting ecologies. Historical Biology 30(1–2):76–88.CrossRefGoogle Scholar
López-Torres, S., Selig, K. R., Burrows, A. M., and Silcox, M. T.. 2020. The toothcomb of Karanisia clarki: was this species an exudate-feeder? Pp. 67–75 in Nekaris, K. A.-I. and Burrows, A. M., eds. Ecology and conservation of lorises and pottos. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Lucas, P. W. 2004. Dental functional morphology: how teeth work. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
MacPhee, R. D. E., and Jacobs, L. L.. 1986. Nycticeboides simpsoni and the morphology, adaptations, and relationships of Miocene Siwalik Lorisidae. Contributions to Geology, University of Wyoming Special Paper 3:131–161.Google Scholar
Marivaux, L., Ramdarshan, A., Essid, E. M., and Marzougui, W., Ammar, H. K., Lebrun, R., Marandat, B., Merzeraud, G., Tabuce, R., and Vianey-Liaud, M.. 2013. Djebelemur, a tiny pre-tooth-combed primate from the Eocene of Tunisia: a glimpse into the origin of crown strepsirrhines. PLoS ONE 9:e80778.CrossRefGoogle Scholar
Masters, J. C., Lumsden, W. H. R., and Young, D. A.. 1988. Reproductive and dietary parameters in wild greater galago populations. International Journal of Primatology 9:573–592.CrossRefGoogle Scholar
Masters, J. C., Génin, F., Couette, S., Groves, C. P., Nash, S. D., Delpero, M., and Pozzi, L.. 2017. A new genus for the eastern dwarf galagos (Primates: Galagidae). Zoological Journal of the Linnaean Society 181:229–241.CrossRefGoogle Scholar
McCrossin, M. L. 1992. New species of bushbaby from the Middle Miocene of Maboko Island, Kenya. American Journal of Physical Anthropology 89:215–233.CrossRefGoogle ScholarPubMed
McElreath, R. 2015. Statistical rethinking: a Bayesian course with examples in R and Stan. Chapman and Hall/CRC, New York.Google Scholar
Nash, L. T. 1986. Dietary, behavioral, and morphological aspects of gummivory in primates. American Journal of Physical Anthropology 29:113–137.CrossRefGoogle Scholar
Nekaris, K. A. I. 2005. Foraging behaviour of the slender loris (Loris lydekkerianus lydekkerianus): implications for theories of primate origins. Journal of Human Evolution 49:289–300.CrossRefGoogle ScholarPubMed
Nekaris, K. A. I., and Rasmussen, D. T.. 2003. Diet and feeding behavior of Mysore slender lorises. International Journal of Primatology 24:33–46.CrossRefGoogle Scholar
Norscia, I., Carrai, V., and Borgognini-Tarli, S. M.. 2006. Influence of dry season and food quality and quantity on behavior and feeding strategy of Propithecus verreauxi in Kirindy, Madagascar. International Journal of Primatology 27:1001–1022.CrossRefGoogle Scholar
Olson, E. R., Marsh, R. A., Bovard, B. N., Randrianarimanana, H. L., Ravaloharimanitra, M., Ratsimbazafy, J. H., and King, T.. 2013. Habitat preferences of the critically endangered greater bamboo lemur (Prolemur simus) and densities of one of its primary food sources, Madagascar giant bamboo (Cathariostachys madagascariensis), in sites with different degrees of anthropogenic and natural disturbance. International Journal of Primatology 34:486–499.CrossRefGoogle Scholar
Overdorff, D. J. 1992. Differential patterns in flower feeding by Eulemur fulvus rufus and Eulemur rubriventer in Madagascar. American Journal of Primatology 28:191–203.CrossRefGoogle ScholarPubMed
Overdorff, D. J., Strait, S. G., and Telo, A.. 1997. Seasonal variation in activity and diet in a small-bodied folivorous primate, Hapalemur griseus, in southeastern Madagascar. American Journal of Primatology 43:211–223.3.0.CO;2-#>CrossRefGoogle Scholar
Pampush, J. D., Spradley, J. P., Morse, P. E., Harrington, A. R., Allen, K. L., Boyer, D. M., and Kay, R. F.. 2016a. Wear and its effects of dental topography measures in howling monkeys (Alouatta palliata). American Journal of Physical Anthropology 161:705–721.CrossRefGoogle Scholar
Pampush, J. D., Winchester, J. M., Morse, P. E., Vining, A. Q., Boyer, D. M., and Kay, R. F.. 2016b. Introducing molaR: a new R package for quantitative topographic analysis of teeth (and other topographic surfaces). Journal of Mammalian Evolution 23:397–412.CrossRefGoogle Scholar
Patel, B. A., Boyer, D. M., Perchalski, B. A., Ryan, T. M., St. Clair, E. M., Winchester, J. M., and Seiffert, E. R.. 2017. New fossils and the paleobiology of Karanisia clarki from the late Eocene of Egypt. American Journal of Physical Anthropology 162:310–311.Google Scholar
Pineda-Munoz, S., Lazagabaster, I. A., Alroy, J., and Evans, A. R.. 2017. Inferring diet from dental morphology in terrestrial mammals. Methods in Ecology and Evolution 8:481–491.CrossRefGoogle Scholar
Powzyk, J. A., and Mowry, C. B.. 2003. Dietary and feeding differences between sympatric Propithecus diadema diadema and Indri indri. International Journal of Primatology 24:1143–1162.CrossRefGoogle Scholar
Rode-Margono, E. J., Nijman, V., Wirdateti, N. K., and Nekaris, K. A. I.. 2014. Ethology of the critically endangered Javan slow loris Nycticebus javanicus E. Geoffroy Saint-Hilaire in West Java. Asian Primates 4:27–41.Google Scholar
Sato, H., Santini, L., Patel, E. R., Campera, M., Yamashita, N., Colquhoun, I. C., and Donati, G.. 2016. Dietary flexibility and feeding strategies of Eulemur: a comparison with Propithecus. International Journal of Primatology 37:109–129.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Selig, R. S., Sargis, E. J., and Silcox, M. T.. 2019. The frugivorous insectivores? Functional morphological analysis of molar topography for inferring diet in extant treeshrews (Scandentia). Journal of Mammalogy 100:1901–1917.Google Scholar
Shan, S., Kovalsky, S. Z., Winchester, J. M., Boyer, D. M., and Daubechies, I.. 2019. aria DNE: a robustly implemented algorithm for Dirichlet energy of the normal. Methods in Ecology and Evolution 10:541–552.CrossRefGoogle Scholar
Sheine, W. S., and Kay, R. F.. 1982. A model for comparison of masticatory effectiveness in primates. Journal of Morphology 172:139–149.CrossRefGoogle Scholar
Simpson, G. G. 1933. Paleobiology of Jurassic mammals. Palaeobiologica Band V.Google Scholar
Spagnolo, S. 1976. Convergence in energy for elliptic operators. In Hubbard, B., ed. Numerical solution of partial differential equations III:469–499. Elsevier, New York.Google Scholar
Spradley, J. P., Pampush, J. D, Morse, P. E., and Kay, R. F.. 2017. Smooth operator: the effects of different 3D mesh retriangulation protocols on the computation of Dirichlet normal energy. American Journal of Physical Anthropology 163:94–109.CrossRefGoogle ScholarPubMed
Sterling, E. J., Dierenfeld, E. S., Ashbourne, C. J., and Feistner, A. T.. 1994. Dietary intake, food composition and nutrient intake in wild and captive populations of Daubentonia madagascariensis. Folia Primatologica (Basel) 62:115–124.CrossRefGoogle ScholarPubMed
Strait, S. G. 1993. Differences in occlusal morphology and molar size in frugivores and faunivores. Journal of Human Evolution 25:471–484.CrossRefGoogle Scholar
Strait, S. G. 1997. Tooth use and the physical properties of food. Evolutionary Anthropology 5:199–211.3.0.CO;2-8>CrossRefGoogle Scholar
Strait, S. G., and Vincent, J. F. V.. 1998. Primate faunivores: physical properties of prey items. International Journal of Primatology 19:867–878.CrossRefGoogle Scholar
Streicher, U. 2004. Aspects of the ecology and conservation of the pygmy loris Nycticebus pygmaeus in Vietnam. Ph.D. thesis. Ludwig Maximilians Universität, Munich.Google Scholar
Streicher, U. 2009. Diet and feeding behaviour of pygmy lorises (Nycticebus pygmaeus) in Vietnam. American Journal of Primatology 3:37–44.Google Scholar
Thalmann, U. 2001. Food resource characteristics in two nocturnal lemurs with different social behavior: Avahi occidentalis and Lepilemur edwardsi. International Journal of Primatology 22:287–324.CrossRefGoogle Scholar
Ungar, P. S. 2007. Dental functional morphology. Pp. 39–55 in Ungar, P. S., ed. Evolution of the human diet: the known, the unknown, and the unknowable. Oxford University Press, Oxford.Google Scholar
Ungar, P. S. 2010. Mammal teeth: origin, evolution, and diversity. Johns Hopkins University Press, Baltimore.Google Scholar
Ungar, P. S., and Williamson, M.. 2000. Exploring the effects of tooth wear on functional morphology: a preliminary study using dental topographic analysis. Palaeontologia Electronica 3:1–18.Google Scholar
Vasey, N. 2000. Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: I. Interspecific patterns. American Journal of Physical Anthropology 112:411–431.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Vasey, N. 2002. Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. Intraspecific patterns. American Journal of Physical Anthropology 118:169–183.CrossRefGoogle ScholarPubMed
Vehtari, A., Gelman, A., and Gabry, J.. (2017) Practical Bayesian model evaluation using leave-one-out cross-validation and WAIC. Statistics and Computing 27:1413–1432.CrossRefGoogle Scholar
Vincent, J. 1990. Structural biomaterials. Princeton University Press, Princeton, N.J.Google Scholar
Walker, A. 1969. True affinities of Propotto leakeyi Simpson 1967. Nature 223:647–648.CrossRefGoogle Scholar
Wiens, F., Zitzmann, A., and Hussein, N. A.. 2006. Fast food for slow lorises: is low metabolism related to secondary compounds in high-energy plant diet? Journal of Mammalogy 87:790–798.CrossRefGoogle Scholar
Winchester, J. M. 2016. MorphoTester: an open source application for morphological topographic analysis. PLoS ONE 11:e0147649.CrossRefGoogle ScholarPubMed
Winchester, J. M. 2020. hecate. https://github.com/JuliaWinchester/hecate, accessed 10 March 2020.Google Scholar
Winchester, J. M., Boyer, D. M., St. Clair, E. M., and Gosselin-Ildari, A. D., Cooke, S. B., and Ledogar, J. A.. 2014. Dental topography of platyrrhines and prosimians: convergence and contrasts. American Journal of Physical Anthropology 153:29–44.CrossRefGoogle ScholarPubMed
Wright, P. C., Razafindratsita, V. R., Pochron, S. T., and Jernvall, J.. 2005. The key to Madagascar frugivores. Pp. 121–138 in Dew, J. L., and Boubli, J. P, eds. Tropical fruits and frugivores. Springer, New York.CrossRefGoogle Scholar
Yamashita, N. 1998. Functional dental correlates of food properties in five Malagasy lemur species. American Journal of Physical Anthropology 106:169–188.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Yamashita, N. 2003. Food procurement and tooth use in two sympatric lemur species. American Journal of Physical Anthropology 121:125–133.CrossRefGoogle ScholarPubMed