What Carbon Has To Do With It

This may go under the radar, so I consider it opportune to mention it. While it doesn’t directly consider fossil archosaurs in any fashion, or a ridiculously over-hyped but very popular group of bird-stem archosaurs, the study at hand does consider the methodology of 1) writing a good paper, 2) being exceptionally thorough in both summary of previous results and current methodology, and 3) analyzing a bulk of trends in consideration for how to assess diet when all you have are teeth.
Molars in mammals are one of the most heavily studied parts of mammalian biology, and one of the most influential in assessing phylogeny. But primarily, they are highly useful in ecological contexts, including but especially that of determining the types and process by which an animal feeds. This topic has eluded reasoning with much speculation when it comes to the fossil primate Paranthropus boisei, an “australopithecine” hominid with a pronounced cranial sagittal crest, robust jaw, and large, high-crowned and low-cusped molars. Among hominids, Paranthropus (including robustus and boisei) is exceptional in having particularly thick molar enamel, which is generally correlated with eating very hard foods. At the same time, the high-crowns and low-cusp aspect of these teeth are correlated with eating fibrous, durable plants, rich in silica, such as grasses. Most animals with flat molars typical are grinders, and are processing tough plants such as grasses, and as such the teeth would be useful and are dominantly found in grazers. High-crowned teeth are used for shearing and puncturing, and higher-crowned teeth than lower are correlated to browsers, with an intermediate aspect in browser-grazers, animals that forage both domains of plants.

Skull and mandible of Paranthropus boisei. Note the broad, flat molars and premolars. Stolen from Wikimedia Commons.

Interestingly enough, a substantial weight of data indicates that phytoliths — tiny particles formed of silica that are incorporated into the bodies, leaves, and fruits of plants due to absorption from the roots from the soil — are responsible for a form of wear forming numerous pitting on the surface of and long furrows into the enamel. SEM photography shows phytoliths in the ends of these furrows, providing direct correlation as causation: furrowing is caused by phytoliths, and the more numerous the furrows, the more numerous the phytoliths.

Plants such as grasses are typically extremely high in phytoliths, while softer foods tend to be fairly low. Pitting and furrowing are shown as evidence of high-phytolith consuming, and thus correlate to grazers, while low or absent pitting and furrowing to browsers. Paranthropus boisei, despite having the low-cusped, grinding-style molars of a grazer and phenomenally thick enamel, lacks substantive furrowing or pitting at all: the enamel remains particularly smooth. This has led to some debate over whether Paranthropus boisei was adept in any fashion at grazing, despite the developed structure of its jaws and teeth. However, there were problems with this: animals that consumed hard, high-phytolith food and had thick enamel could also show low pitting, and that there was no clear direct correlation that enamel thickness is associated with particular foods.

Diana Rabenold and Osbjorn Pearson have collated and developed an experiment to assess these differing factors, weighing in in particular on the case this peculiar animal. What they found was, after assessing the phytolith concentrations of a variety of foods and the relative enamel thickness (RET) of a score of mammals, that phytoliths and thick enamel are correlated: thick enamel and extensive wear due to phytoliths do not typically co-occur, and thus that the thickness can be developed a predictor of foods with phytoliths in them. Comparing this with food consumed and enamel thickness, it was found there is a positive correlation: animals such as the aye-aye (Daubentonia madagascariensis) consumed hard-shelled fruits, which were opened with the jaws prior to consumption using the fingers to scoop out the internal meat. Thus, the thickness of the enamel was the predictor to diet, rather than wear features, and that a thin enamel would more likely correlate to browsers such as folivores, thick enamel with grazers and frugivores.

USNM 199694, skull of Daubentonia madagascariensis (Gmelin, 1788). From Quinn & Wilson (2004).

Animals that eat leaves and “soft forage” will typically have thin enamel, which allows the enamel to wear quicker, exposing the harder dentine, and form distinct shearing edges to the cusps that allow inter-oral shredding the plants prior to swallowing, increasing the efficiency of digestion by reducing the energy spent breaking the food down in the stomach. The opposite is true for grazers, who grind the food orally into a pulp rather than shred it, and require thicker enamel.

A third element of the analysis is the carbon fixation photosynthetic pathway, based on the concentration of δ13C in enamel, where plants in dry, salty regions have developed a method of more efficient photosynthesis using more pervasive photosynthetic cells in their leaves and deeper tissues than in other plants. This is terms the C4 pathway, or the Hatch-Slack pathway. This process results in larger proportions of carbon fixated in the tissues of such plants, all angiosperms, including grasses, corn, cane and sages. Higher δ13C in enamel correlates to arid, aline regions and plants on land, and seaweed in water and the C4 pathway, while lower δ13C relates to the C3 pathway and freshwater plants (low saline). Animals adapted to the C3 pathway are predominately grazers, including manatees who consume algaes at sea or in brakish to fresh water, showing a proportion of carbon in their tooth enamel higher than in those whom are browsers or live in less arid environments; conversely, such browsers or exploiters of foods in wetter, non-xeric freshwater-dominated areas exploit plants that use the less-efficient C3 pathway.

Relative enamel thickness (RET) in primates from actual measurements and as predicted from phytolith density. From Rabenold & Pearson (2011).

Sampling both the ecology of Paranthropus boisei, it’s enamel carbon isotopic composition and morphology, Rabenold and Pearson suggest that “australopithecine diets consisted of plant foods high in phytoliths, few if any leaves, and included a substantial component (>50% if no leaves were consumed) of non-plant foods.”

They conclude in part:

“Extension of the model to P. boisei predicts a feeding ecology markedly different from any primate in the sample. There is always a danger of extrapolating beyond the range of a regression model, but an unusual diet may make sense because P. boisei also has substantially thicker enamel than any of the species in the comparative sample.”


“we propose that C4 sedges are more likely candidates for the predominant portion of P. boisei‘s plant diet. The flat, low-crowned molar morphology of P. boisei evinces the very opposite morphology of tall-crowned cheek teeth with the sharp, shearing edges formed along ridges of complex infolded occlusal enamel that are required to shred leaves of grass, and that characterize all grazers, including the sole higher primate grazer, Theropithecus gelada [51], [90]. P. boisei‘s dentition is consistent with the consumption of plant pith (i.e., parenchymatous ground tissue found in the center of stems) and rhizomes.”

It would seem then interesting that diet may not be perfectly extrapolated from wear features of the enamel. However, RET in enamel can be directly correlated to hard foods, thus that animals with seeming durophagous dentition can be compared to this relative scale to determine if it is useful or effective to determine diet by enamel thickness. Certainly, for example, enamel is exceptionally thicker in globidensine mosaurs than in other mosasaurs; the teeth are broader, relatively higher in aspect (lower-crowned), and possess mechanical advantages to compression, including infolding of the enamel into the dentine cavity.

Diplodocoid sauropods mapped to browse height, wear structure, and ecosystem recovered in. Snout shape is placed above the phylogeny. Modified from Whitlock (2011).

So what does this mean for more … interesting … things? What about the issues of “what did they eat?” when it comes to ornithischian and sauropod dinosaurs, animals considered dominantly herbivorous? Especially, how does it impact the consideration of what, if any, sauropods were grazers? Whitlock (2011) examined morphology and microwear in sauropods, while comparing it to snout shape, and found that wear (pitting and furrows) typically correlates to models of herbivorous mammals and the grazer-browser spectrum. Examining RET in sauropods, its relative thickness, in Nigersaurus tacqueti, for example, would be particularly interesting to the question of whether the RET in sauropods bears weight on the matter. In particular, Sereno & Wilson (2005) and Sereno et al. (2007) found that tooth enamel is uneven in Nigersaurus taqueti, with the thickness 10x greater on the lingual surface than the labial, but the relative thickness in comparison with other sauropods was not indicated. The teeth also bear fine scratches and furrows, but as implied above, this may have less relevance than has been implied before (e.g., Ungar, 1998; Nelson et al., 2005). So what gives? It is possible that the relative thickness of the enamel in these teeth is particularly relevant, and the work of Rabenold and Pearson may imply that wear is less instructive on diet than dietary carbon intake and enamel thickness.

An analysis directly assessing dietary carbon in enamel (Tütken, 2011) indicates that, for the most part, sauropods can be generally classed for high and low browse by the carbon isotopic composition in their teeth, with “horizontal neck” sauropods like Diplodocus carnegii and Apatosaurus ajax relegated to low-browse with moderate δ13C, while “vertical necked” sauropods like Brachiosaurus brancai and Janenschia robusta relegated to high-browse with low δ13C. Intriguingly, the extremely short-necked Dicraeosaurus hansemanni has a lower δ13C value than Brachiosaurus brancai, implying–not high browse–but very wet, low efficiency plants. However, in contrast to the hypothesis put forward by Stevens and Parrish (1999), the low posture of the neck is contradicted by the moderate-browse indicated by facial shape (Whitlock, 2011) and weak to moderate scratching suggestive of softer foods.

Sauropod vertical forage reach based on the maximum height attainable for sauropods as compared to a giraffe and an elephant. Vertical reach varies substantially in diplodocoid sauropods (DI, BA, AP, DIC). AP, Apatosaurus; BA, Barosaurus; BR, Brachiosaurus; CA, Camarasaurus; CE, Cetiosaurus; DI, Diplodocus; DIC, Dicraeosaurus; MAM, Mamenchisaurus. Black bars represent projected moderate heights, while grey bars indicate absolute maximums. From Tütken (2011).

Assessing enamel thickness in sauropods and other fossil reptiles, including broad-toothed crurotarsans, ornithischians, mosasauroids, etc., with respect to their enamel δ13C values. Respect to wear features, RET, snout shape, neck movement range may all directly compare to potential diet evaluation. I await more analyses, especially ones that tend to wander away from the sauropsidan side of Amniota, in order to qualify the variation in diet and ecology that may be useful in studying extinct animals.

Cerling, T. E., Harris, J. M., Leakey, M. G. & Mudida, N. 2003. Stable isotope ecology of northern Kenya with emphasis on the Turkana Basin. pp.583-594 in Leakey & Harris (eds.) Lothagam: The Dawn of Humanity. (Columbia University Press, New York City.)
Cerling, T. E., Mbua, E., Kirera, F. M., Manthi, F. K., Grine, F. E., Leakey, M. G., Sponheimer, M. & Uno, K. T. 2011. Diet of Paranthropus boisei in the early Pleistocene of East Africa. Proceedings of the National Academy of Sciences of the United States of America 108(23):9337–9341.
Nelson, S., Badgley, C. & Zakem, E. 2005. Microwear in modern squirrels in relation to diet. Palaeontologia Electronica 8(3):14A. [PDF]
Rabenold, D. & Pearson, O. M. 2011. Abrasive, silica phytoliths and the evolution of thick molar enamel in primates, with implications for the diet of Paranthropus boisei. PLoS ONE 6(12):e28379.
Sereno, P. C. & Wilson, J. A. 2005. Structure and evolution of a sauropod tooth battery. pp.157-177 in Curry-Rogers & Wilson (eds.) The Sauropods: Evolution and Paleobiology. (University of California Press, Berkeley).
Sereno, P. C., Wilson, J. A., Witmer, L. M., Whitlock, J. A., Maga, A., Ide, O. & Rowe, T. A. 2007. Structural extremes in a Cretaceous dinosaur. PLoS ONE 2(11):e1230.
Stevens, K. A. & Parrish, J. M. 1999. Neck posture and feeding habits of two Jurassic sauropod dinosaurs. Science 284:798–800.
Tütken, T. 2011. The diet of sauropod dinosaurs: Implications of carbon isotope analysis on teeth, bones, and plants. pp.57- 79 in Klein, Remes, Gee & Sander (eds.) Biology of the Sauropod Dinosaurs: Understanding the Life of Giants. (Indiana University Press, Bloomington.)
Ungar, P. S. 1998. Dental allometry, morphology, and wear as evidence for diet in fossil primates. Evolutionary Anthropology 6(6):205–217.
Whitlock, J. A. 2011. Inferences of diplodocoid (Sauropoda: Dinosauria) feeding behavior from snout shape and microwear analyses. PLoS ONE 6(4):e18304.

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