Differentiating diets of new world monkeys using dental topographic analysis

Differentiating diets of new world monkeys using dental topographic analysis

Carrie A. Healy1, Aleksis Karme2, Mikael Fortelius2, and Peter S. Ungar1Carrie A. Healy1, Aleksis Karme2, Mikael Fortelius2, and Peter S. Ungar1

1Department of Anthropology, University of Arkansas, 2Department of Geosciences and Geography, University of Helsinki

High resolution replicas were coated with graphite (The B’Laster Corp., Valley View, OH) and Teflon (CRC Industries, Warminster, PA) to reduce the translucency of the epoxy casts.

Maxillary M2’s were mounted on a horizontal plate with the occlusal plane parallel to the plate. A 3D point cloud of each occlusal surface was generated using an XSM multi-sensor scanning machine (Xystrum Corp., Turino, Italy) with an integrated OTM3 laser head (Dr. Wolf & Beck GmbH, Wangen, Germany). Three-dimensional data were collected at 25 µm intervals in the x- and y-axes. The point cloud data were saved in ASCII format using Digiline software (Xystrum Corp., Turino, Italy) and processed using ArcGIS 10.2 (ESRI Corp., Redlands, CA).

Each ASCII file was imported into ArcMap as a table, interpolated using inverse distance weighting, and cropped to include only the occlusal table, defined as the surface above the lowest point on the occlusal basin (Fig 1). Klukkert et al. (2012) explains the process in detail. Mean occlusal surface angularity and relief were calculated for the occlusal table of each specimen. See Bunn and Ungar (2009) for definitions of these variables. Each specimen was scored for wear using a modified version of Scott’s (1979) method to characterize wear (average wear score per cusp was used as the callitrichines had three cusps per tooth, and other taxa had four); specimens were grouped by average wear score per cusp. Topographic relief and angularity data were ranked and compared by wear stage and taxa using a one-way ANOVA model. Diet category assignments for the taxa were made based on food preference data reported in the literature.

Tukey’s HSD and Fisher LSD post hoc tests were used to determine sources of significant variation.

METHODSMETHODS

REFERENCESREFERENCES

Maxillary M2’s of sympatric platyrrhines from Para, Brazil were analyzed. Sample sizes are as follows:

MATERIALSMATERIALS

Alouatta belzebul n = 54Alouatta seniculus n = 6Aotus infulatus n = 9Ateles belzebuth n = 27Ateles paniscus n = 5Callicebus moloch n = 35Callithrix argentata n = 15Callithrix humeralifer n = 14

Cebus apella n = 30Chiropotes albinasus n = 14Chiropotes satanas n = 21Lagothrix lagotricha n = 16Pithecia irrorata n = 11Pithecia monachus n = 8Saguinus midas n = 41Saimiri ustus n = 35

Dental topographic analysis distinguishes among platyrrhine species with variably worn molars in a manner consistent with their reported diet differences.

Relief separates insectivores and folivores from frugivores and hard-object feeders.

Angularity separates insectivores from folivores and frugivores. Hard-object feeders have intermediate angularity.

Dental topographic analysis results are consistent with results from Kay’s shearing crest studies (Kay, 1978; Kay, 1984) with the additional benefit that it allows comparisons of variably worn specimens.

DISCUSSIONDISCUSSION

Fig 1: Three-dimensional rendering of a representative maxillary M2 from each of the species, not to scale.

Relief

Ang

ular

ity

Table 3: Pair-wise comparison of genera (angularity comparison in blue, relief comparison in orange).

** denotes significant differences using Tukey’s HSD* denotes significant differences using Fisher’s LSD, but not Tukey’s HSD.

Fig 2: Comparison of relief and angularity by wear stage. Folivores are green, frugivores are red, hard-object feeders are brown, and insectivores are gray.

Bunn JM, Ungar PS. 2009. Dental topography and diets of four old world monkey species. Am J Primatol 71:466-477.

Dennis JC, Ungar PS, Teaford MF, Glander KE. 2004. Dental topography and molar wear in Alouatta palliate from Costa Rica. Am J Phys Anthropol 125:152-161.

Kay RF. 1977. Evolution of molar occlusion in Cercopithecidae and early catarrhines. Am J Phys Anthropol 46:327–352.

Kay RF. 1984. On the use of anatomical features to infer foraging behavior in extinct primates. In: Rodman PS, Cant JGH, editors. Adaptations for foraging in nonhuman primates: contributions to an organismal biology of prosimians, monkey and apes. New York: Columbia University Press. p 21–53.

Klukkert ZS, Dennis JC, M'Kirera F, Ungar PS. 2012. Dental topographic analysis of the molar teeth of primates. In: Bell LS, editor. Forensic microscopy for skeletal tissues: methods and protocol. Methods in molecular biology, Vol. 915. New York: Springer. p145–152.

M’Kirera F, Ungar PS. 2003. Occlusal relief changes with molar wear in Pan troglodytes and Gorilla gorilla gorilla. Am J Primatol 60:31-41.

Scott EC. 1979. Dental wear scoring technique. Am J Phys Anthrop 51:213-218.

Ungar PS, Bunn JM. 2008. Primate dental topographic analysis and functional morphology. In: Irish JD, Nelson GC, editor. Technique and Application in Dental Anthropology. Cambridge: Cambridge University Press. p253-265.

Ungar PS, M’Kirera F. 2003. A solution to the worn tooth conundrum in primate functional anatomy. Proc Natl Acad Sci USA 100:3874-3877.

RESULTSRESULTSThere are significant differences between taxa for both angularity and relief (Table 1, 2).

There is no significant interaction between angularity and wear stages, but there is between relief and wear stage.

A separate one-way ANOVA for each wear category indicates the sources of significant variation for both angularity and relief (Table 1, 2).

Relief differentiates insectivores and folivores from frugivores and hard-object feeders, with insectivores and folivores having a higher value than frugivores and hard-object feeders (Fig 2).

Angularity differentiates insectivores from folivores and frugivores, with insectivores having a higher value than folivores and frugivores (Fig 2).

Post hoc hypothesis tests using Tukey's HSD and Fisher LSD found angularity and relief identifies different aspects of diet (Table 3).

Angularity F p value

All wear stages 113.390 <0.001

Wear stage 1 39.450 <0.001

Wear stage 2 44.378 <0.001

Wear stage 3 14.408 <0.001

Table 1: Comparison of angularity by wear stage.

Relief F p value

All wear stages 39.581 <0.001

Wear stage 1 18.707 <0.001

Wear stage 2 15.413 <0.001

Wear stage 3 14.408 <0.001

Table 2: Comparison of relief by wear stage.

INTRODUCTIONINTRODUCTIONPlatyrrhines differ in their diets, both in terms of food preferences and supplemental items.

This study examines dental topography of variably worn upper second molars of 340 individuals representing 16 species with an eye toward how occlusal surface relief and angularity relate to diet, and how patterns might change with gross tooth wear.

H1:

H2:

As teeth wear, relief will decrease, but angularity will not change within taxa (as previously observed for other primates -- Bunn and Ungar, 2009; Dennis et al., 2004; M’Kirera and Ungar, 2003; Ungar and Bunn, 2008; Ungar and M’Kirera, 2003).

Angularity and relief (at a given wear stage) can be used to discriminate taxa in a manner consistent with differences in diet reported in the literature.

ACKNOWLEDGMENTSACKNOWLEDGMENTSWe thank Mark Teaford for help gathering molds of these specimens, museum curators from the American Museum of Natural History, the Field Museum, the Museu Paraense Emilio Goeldi, and the National Museum of Natural History for their permission to replicate these specimens, and the LSD Leakey Foundation for funding this study.

Pithecia irrorata

Cebus apella

Ateles paniscus

Alouatta belzebul

Saimiri ustus

Lagothrix lagotricha

Callithrix humeralifer

Ateles belzebuth

Pithecia monachus

Chiropotes albinasus

Callicebus moloch

Alouatta seniculus

Saguinus midas

Chiropotes satanas

Callithrix argentata

Aotus infulatus

RELIEF

WEA

R S

TAG

E 1

WEA

R S

TAG

E 2

WEA

R S

TAG

E 3

0

100

200

300

400

0

100

200

300

400

0

100

200

300

400

0

100

200

300

400

ANGULARITY

0

100

200

300

400

0

100

200

300

400

Alouatta Aotus Ateles Callicebus Callithrix Cebus Chiropotes Lagothrix Pithecia Saguinus Saimiri

Alouatta 108.9** 39.5** 40.1** 163.5** 84.2** 55.2** 27.1* 21.6 196.3** 143.3**

Aotus 66.7* 148.4** 68.9** 54.6* 193.1** 53.7** 81.3** 87.4** 87.4** 34.4*

Ateles 175.1** 108.8** 79.6** 203.0** 44.7** 94.8** 66.6** 61.2** 235.8** 182.9**

Callicebus 192.5** 126.2** 17.4 123.4** 124.2** 15.2 12.9 18.4 156.2** 103.3**

Callithrix 119.3** 53.0* 55.8** 73.2** 247.6** 108.2** 136.4** 141.8** 32.8* 20.1

Cebus 163.7** 97.4** 11.4 28.8 44.4* 139.4** 111.3** 105.8** 280.5** 227.5**

Chiropotes 145.3** 79.0** 29.8* 47.2** 26.0 18.4 28.1* 33.6* 141.0** 88.1**

Lagothrix 33.3* 33.0 141.8** 159.2** 86.0** 130.5** 112.0** 5.5 169.2** 116.3**

Pithecia 215.3** 149.0** 40.2* 22.8 96.0** 51.6* 70.0** 182.0** 174.6** 121.7**

Saguinus 56.0** 10.3 119.1** 136.5** 63.3** 107.7** 89.3** 22.8 159.3** 52.9**

Saimiri 47.5** 18.7 127.5** 144.9** 71.7** 116.2** 97.7** 14.3 167.7** 8.5*