Oxygen isotopes in orangutan teeth reveal recent and ancient climate variation

  1. Griffith Centre for Social and Cultural Research, Griffith University, Australia
  2. Australian Research Centre for Human Evolution, Griffith University, Australia
  3. Department of Environmental Medicine and Public Health, Icahn School of Medicine at Mount Sinai, USA
  4. School of Earth and Environmental Sciences, University of Queensland, Australia
  5. Centro Nacional de Investigación sobre la Evolución Humana (CENIEH), Spain
  6. Palaeoscience Labs, Dept. Archaeology and History, La Trobe University, Australia
  7. Department of Geology, Universiti Malaya, Malaysia
  8. School of Archaeology and Anthropology, The Australian National University, Australia
  9. Department of Geology, Naturalis Biodiversity Center, The Netherlands
  10. Research School of Earth Sciences, The Australian National University, Australia
  11. Radiogenic Isotope Facility, School of Earth and Environmental Sciences, University of Queensland, Australia
  12. Lamont-Doherty Earth Observatory, Earth Institute and Climate School, Columbia University, USA

Peer review process

Not revised: This Reviewed Preprint includes the authors’ original preprint (without revision), an eLife assessment, public reviews, and a response from the authors (if available).

Read more about eLife’s peer review process.

Editors

  • Reviewing Editor
    Justin Yeakel
    University of California, Merced, Merced, United States of America
  • Senior Editor
    George Perry
    Pennsylvania State University, University Park, United States of America

Reviewer #1 (Public Review):

Summary:
The authors measured the oxygen stable isotope ratios in six orangutan teeth using a state-of-the-art micro-sampling technique (SHRIMP SI) to gather substantial multi-year isotopic data for six modern and five fossil orangutan individuals from Borneo and Sumatra. This fine-scale sampling technique allowed them to address the fundamental question of whether breastfeeding affects the oxygen isotope ratios in teeth forming in the first one to two years of life, during which orangutans are assumed to largely depend on breastmilk. The authors provide compelling evidence that the consumption of milk does not appear to affect the overall isotopic profile in early-forming teeth. They conclude that this allows us to use these teeth as terrestrial/arboreal isotopic proxies in paleoenvironmental research, which would provide an invaluable addition to otherwise largely marine climate records in these regions.

Strengths:
The overall large sample size of orangutan dental isotope records as well as the rigorous dating of the fossil specimens provide a strong dataset for addressing the outlined questions. The direct comparison of modern and fossil orangutan specimens provides a valuable evaluation of the use of these modern and past environmental proxies, with some discussion of the implications for the environmental conditions during the expansion of early modern humans into this region of the world.

Weakness:
Although the overall conclusions of this paper are well supported and discussed, one important aspect could have more detailed consideration: the ecology and behavior of orangutans. As one example, orangutans are almost exclusively (~96%) arboreal creatures foraging for plant foods in the forest canopy, and as such they mostly meet their water requirements from the plants they eat, only very rarely drinking surface water (Ashbury et al. 2015). As a result, all orangutan water and foods are strongly affected by the so-called canopy effect, which could have found stronger consideration in this study. The canopy effect in primate plant foods has been demonstrated to easily exceed 5‰ within the same forest canopy and even within the same tree, mainly depending on stratigraphy/height (Lowry et al. 2021). This variation may explain the noise in the isotopic data within a given orangutan tooth, which lies well within this 5% range, and could easily obscure any possible breastfeeding effect in dental isotope ratios. If the canopy effect may indeed introduce so much noise in the oxygen isotope data, this should be also considered in the use of the data as a climate proxy. The question arises if a terrestrial long-lived mammal species may be a more suitable proxy than an arboreal one.

Reviewer #2 (Public Review):

Summary:
This manuscript provides microprobe serial oxygen isotope data from thin-sectioned modern and fossil orangutan teeth in an effort to reconstruct the seasonality of rainfall in Borneo and Sumatra. The authors also explore the hypothesis that nursing could affect early tooth (first molar) isotope values. They find that all molars yield similar oxygen isotope values and therefore conclude that future research need not exclude the use of first molars. With regard to seasonality, the modern orangutans yield similar results from both islands. The authors suggest differences between modern and fossil orangutan teeth, but the comparisons could be more fully explored.

Strengths:
The study employs a sampling method that captures serial isotope values within thin sections of teeth using a microprobe that provides a much higher resolution than traditional hand-held drilling.

Weaknesses:
The study only examines six modern and six fossil orangutan individuals. Of those, only four modern individuals were samples across multiple molars. The comparisons between modern and fossil teeth are difficult to follow, making unclear the conclusion that climate has changed.

Author Response

We appreciate the opportunity to publish our research in eLife. Both reviewers highlight our state-of-the-art oxygen isotope sampling approach, which has allowed us to establish that early-formed primate enamel does not show a large or consistent isotopic offset due to intensive nursing. This means we can be more confident in employing early-forming teeth to probe environmental conditions—an issue that has handicapped past paleoenvironmental studies—documenting seasonal rainfall variation in the tropics at an extremely fine-scale.

Reviewer 1 requests that we elaborate on the ecology and behavior of orangutans, particularly in reference to the issue of isotopic enrichment within forest canopies—a topic we devote a paragraph to in the discussion. We appreciate the opportunity to add additional context during revision, noting here that our previous comparisons of terrestrial baboons and semi-terrestrial tantalus monkeys in the Bushenyi District (Uganda) do show modest isotopic differences between species, consistent with a canopy effect (Green et al. 2022). However, this is less of an issue for comparisons of Sumatran and Bornean orangutans given their ecological and behavioral similarities. We agree that variation in the canopy heights/positions of orangutan food sources may contribute to enamel oxygen isotope variation, in addition to the seasonal rainfall trends we observe in our datasets. Importantly, our published and on-going work on western chimpanzees has revealed strong annual oxygen isotope trends concordant with local rainfall patterns. The consistency and amplitude of seasonal oxygen isotope oscillations in such datasets suggest that arboreal primates are not less useful than terrestrial primates for reconstruction of rainfall seasonality.

We clarify that while Reviewer 1 states that we measured 6 teeth, Tables 1 and 2 and the first sentence of the results make it clear that we measured 18 teeth in this study.

Reviewer 2 asks for further detail about comparisons between modern and fossil orangutan teeth that support inferences of climate variation, which we will endeavour to add in the revised manuscript.

  1. Howard Hughes Medical Institute
  2. Wellcome Trust
  3. Max-Planck-Gesellschaft
  4. Knut and Alice Wallenberg Foundation