You are What You Eat: Using Stable Isotopes to Trace Dietary Shifts in Ancient African Hebivores
Today, the stereotypical image of eastern Africa features immense stretches of grasslands, dotted by herds of huge herbivores, chewing their way across the plains. It seems like a timeless scene, the world’s last glimpse of what it was like when megafauna spanned the globe.
In actuality, these wide grasslands are an extremely recent feature in the region’s history. There isn’t solid evidence of animals consuming C4 plants until a scanty 10 million years ago (mya), and grasslands did not become widespread until the late Pliocene and Pleistocene. This recent birth of what is now a dominant feature of the landscape brings to mind many important questions. Specifically, after C4 plants started to become a food source in the Oligocene, how long did it take different herbivore species to adapt to eating this new type of greenery? Which species were early adopters, and which made the most complete shift from C3 to C4 plants? The process of adapting to a new resource—the relatively young C4 plants—had profound effects on community ecology of eastern Africa, as it provided new ways for large herd animals to both exploit new food sources and partition resources in order to facilitate coexistence and/or higher densities.
First, a bit of review, please bear with me for this recapt of plant metabolism: what is the difference between a C3 and a C4 plant? The main distinction lies in 1) the enzyme used to fix CO2 during photosynthesis, and 2) the organic molecules that are the first products of the process. The enzyme used by C3 plants, RuBisCO, is not all that suitable for photosynthesis in hot, dry climates, because as temperatures warm, it incorporates more and more oxygen, which, through some chemical wizardry beyond the scope of this post, results in a high rate of water loss. C4 plants use a more desert-friendly method, isolating RuBisCO in special bundle sheath cells and using a more efficient enzyme, PEP carboxylase, to do the initial carbon fixation and shuttle the products to the sequestered RuBisCO for further reactions. Notably, C4 plants also run through photosynthesis at a rate about 6 times faster than C3 plants. The take home message of all of this is that C4 plants are better adapted to dry climates, although about 95% of all plants on earth still use C3 photosynthesis.
In general, in Uno et al. (2011), a diet of C4 plants is considered to indicate grazing (mostly grasses), and a diet of C3 plants indicates browsing from higher foliage (shrubs and trees).
Now the significance of all of that chemistry, for the purposes of tracking animal diets, is that stable isotope analysis can distinguish between C3 and C4 vegetation, due to different ratios of heavy to light carbon isotopes in the different types of plants. This means that, given a tissue sample from an animal (anything tissue, from blood to bone), one can look at the ratios of different carbon isotopes and determine the relative proportion of the animal’s diet comprised of either C3 or C4 plants. The basic gist of dietary stable isotope analysis is “you are what you eat”; your diet determines the chemical composition of your tissues, even millions of years after your death. This is useful for answering all sorts of questions, ranging from comparisons of interspecies dietary overlap to tracking intraspecies (or even intraindividual) changes in foraging patterns over time and/or ontogeny. All of which makes stable isotope analysis an ideal tool to elucidate the relative rates and degrees to which different species adapted to a new food source, such as the case of African herbivores once C4 grasses evolved in eastern Africa.
Previous studies have shown that herbivores started to consume C4 plants around 10 mya (Quade et al. 1992), but further work was needed to untangle exactly how the process happened over time and between taxa. Thus, a research group led by Kevin Uno at the University of Utah used enamel from fossilized teeth of a variety of east African herbivores to paint us a picture of how, from 10-3 mya, different species responded to the rise of C4 plants and concomitant changes in the local climate. Their findings give us significant new insights into the impact that climate change and shifting landscape ecology had on the diets of local large herbivores.
So, fairly straightforward, and here is what we learned for the different taxonomic groups:
It appears that equids, ancestors of the modern zebra, made a fast and dramatic shift, becoming the first of the taxa to switch over to a diet of primarily grass (C4) plants, sometime between 9.9 and 7.4 mya, becoming specialists on C4s and staying that way all the way up to today.
Bovids (ancestors of today’s gazelles, wildebeest, and cape buffalo) and ancestral rhinos were also fairly early adopters, beginning the switch to grass around 9.6 mya. They did not come to prefer C4s as exclusively as the equids did, however; some bovid species continued to have mixed or primarily C3 diets up to the 3 mya point that bookended this analysis. This heterogeneity is interesting, because it may have helped to facilitate species diversity within the family by reducing dietary overlap between sympatric species. It is notable that the Bovidae has become, by far, the most diverse herbivore family in Africa, an evolutionary accomplishment that may have been facilitated by this dietary niche partitioning.
In comparison to the rapid rate at which equids and bovids became consumers of the new C4 plants, ancestors of modern elephants (elephantids and the extinct gomphotheres) did not start to transition over to grasses until about 7.4 mya. Interestingly, the groups appear to have been grazers until only a million years or so ago, and yet now our only remaining members of this line, the African and Asian elephants, eat mostly trees and shrubs (C3). Another slight twist to the story is that the deinotheriids, also related to the elephant lineages, never showed any sign of switching to C4s. These behemoths were the second largest land mammal known to science, with males weighing up to ten tons. It is interesting to contemplate whether this extreme size was a limiting factor when it came to adopting a novel food resource, as extreme size is known to constrain dietary niche breadth in carnivorous mammals (see my previous post for more discussion on that). And in case you’re wondering, the gomphotheres were grouped with the elephantids in the analysis due to similarity of tooth morphology, apparently not shared to the same degree with the deinotheriids.
Ancient suids, forebears of modern warthogs and bushpigs, took quite a while to decide they liked the new vegetation, not showing signs of C4 in their diets until between 6.5 and 4.2 mya, and even then maintaining the consumption of both C3 and C4 plants.
Although the just-so story about giraffes having long necks in order to reach high foliage is not accurate (mutations and natural selection don’t happen with a future goal in mind), they did remain faithful to their treetop foraging strategy, and the data show that giraffids have been consistent tree browsers throughout the fossil record.
Morphological changes amongst these taxa appear to support the conclusions drawn from isotopic ratios. For example, during the period in which their carbon signatures were shifting, equids show a shift from the sharp, slicing cusps of browsers (which feed on C3 shrubs and trees) to the blunt, grinding dental cusps that are characteristic of modern grazers. Using several methods of analysis (morphological, biochemical, climatological, etc) creates the potential for an extremely robust set of conclusions, and stable isotope analysis is a powerful method to have in such a toolbox.
One limitation to the study is that samples from different sites did not necessarily overlap in time, meaning that the difference in carbon signatures could be due to either climate (temperature, precipitation, etc), geography (elevation and latitude) , composition of vegetation, or some combination of these factors. Keep in mind that it was not until very recently on the geological time scale that the climate in eastern Africa created overwhelmingly vast swaths of grassland; prior to that it would have been a patchier resource. The authors acknowledge this limitation and point out that the results are best utilized as a complement to other types of analysis, as metnioned above.
This study by Uno et al. is a great example of how stable isotopes can be applied to the study of many facets of ecology. With just small samples from the teeth of long-dead mammals, we can trace the shift of one ecosystem type to another, and construct a valuable timeline of how and when different taxa responded to the introduction and subsequent proliferation of a novel food resource. The implications of this for the community ecology of the region may very well underlie the patterns of biodiversity that we see amongst the herds of herbivores roaming these plains in the present day
Uno, K., Cerling, T., Harris, J., Kunimatsu, Y., Leakey, M., Nakatsukasa, M., & Nakaya, H. (2011). Late Miocene to Pliocene carbon isotope record of differential diet change among East African herbivores Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.1018435108
Quade, J. et al. (1992) A 16-Ma record of paleodiet using carbon and oxygen in fossil teeth from Pakistan. Chem Geol Isot Geosci Sect 94: 183-192.
Grassland image credit
All animal photos obtained from Wikimedia Commons
Figure from Uno et al. 2011