Does Oxygen Stable Isotope Composition in Primates Vary as a Function of Vertical Stratification or Folivorous Behaviour?

Abstract

Stable isotopes of oxygen often vary within a community of primates. For example, folivorous monkeys that forage in the upper reaches of the forest canopy tend to evince high δ 18 O values, whereas those that prefer the understory tend to have lower δ 18 O values. Given that leaves also have high δ 18 O values, particularly higher in the canopy, there is uncertainty as to which behavioural variable -vertical stratification or folivory -is the primary determinant of variation in δ 18 O values. Here, we explore further δ 18 O values from the Taï Forest monkeys (n = 7 species; n = 33 individuals) by examining the interaction between diet and vertical stratification, thereby allowing us to differentiate the effects of each covariate. We found that δ 18 O values varied as a function of mean canopy height, but not folivory, resolving uncertainty about the primary cause of δ 18 O variation. This outcome revolves largely, but not entirely, on the behaviours of Procolobus verus, a highly folivorous but understory forager. Relatively elevated values in Cercopithecus diana, a frugivorous but middle-to-high canopy forager, raises the possibility that plant reproductive tissues (e.g., fruits, flowers) may be increasingly sensitive to evaporative fractionation at higher forest canopy levels. Overall, our results further affirm the value of using δ 18 O values to estimate the vertical behaviour of primate species in a fossil assemblage.

Environmental drivers of megafauna and hominin extinction in Southeast Asia

“…This 'canopy effect' has been observed in temperate, subtropical, and tropical forests [42][43][44][45][46][47] . The distribution of δ 13 C in tropical forest mammal communities has a long left tail (highly negative skew) reflecting the abundance of browsers feeding in the canopy top, gaps in the canopy, and subcanopy frugivores who have higher δ 13 C values than browsers feeding only in the subcanopy [23][24][25] .…”

“…Conversely, higher δ 13 C values (-25.6 to -23.0‰) occur in open canopy forests or woodlands. High δ 18 O values are also found in folivores that forage in the upper canopy, whereas those that prefer the understory have lower δ 18 O values 25 . In Southeast Asia, the distribution of δ 13 C and δ 18 O in browsers are significantly different across all sub-epochs (Kruskal-Wallis, H C =25.23, p <0.001; H o =27.34, p <0.001).…”

“…A shift from low amplitude 41,000-year to high amplitude 100,000-year cycles between 1. 25 Ma and 700 ka were accompanied by significant decreases in sea surface temperatures, increases in ice volume, and heightened Asian aridity and monsoonal intensity 26 . The change in glacial cycles, recorded in the benthic oxygen isotope record, coincides with our observed peak in δ 13 C and δ 18 O values in Southeast Asian mammals (Extended Data Fig.…”

Stratigraphy of stable isotope ratios and leaf structure within an African rainforest canopy with implications for primate isotope ecology

“…This suggests that the δ 18 O data should correspond well to the δ 18 O values of primate consumers. Indeed, the best predictor for feeding height in primate skeletal remains was previously shown to be δ 18 O, irrespective of the degree of folivory or frugivory 34 , 60 . We can confirm this here when we compare our results with the carbonate δ 18 O values of arboreal primates feeding at different heights in the same forest (Fig.…”

“…And indeed, the most folivorous primate at Taï, the olive colobus monkey ( Procolobus verus ) had the lowest δ 13 C values among all taxa 34 . In sum, the degree of folivory versus frugivory should be accounted for when using δ 13 C in reconstructing canopy strata use 60 .…”