Within trophic level shifts in collagen–carbonate stable carbon isotope spacing are propagated by diet and digestive physiology in large mammal herbivores

Abstract

Stable carbon isotope analyses of vertebrate hard tissues such as bones, teeth, and tusks provide information about animal diets in ecological, archeological, and paleontological contexts. There is debate about how carbon isotope compositions of collagen and apatite carbonate differ in terms of their relationship to diet, and to each other. We evaluated relationships between δ13Ccollagen and δ13Ccarbonate among free‐ranging southern African mammals to test predictions about the influences of dietary and physiological differences between species. Whereas the slopes of δ13Ccollagen–δ13Ccarbonate relationships among carnivores are ≤1, herbivore δ13Ccollagen increases with increasing dietary δ13C at a slower rate than does δ13Ccarbonate, resulting in regression slopes >1. This outcome is consistent with predictions that herbivore δ13Ccollagen is biased against low protein diet components (13C‐enriched C4 grasses in these environments), and δ13Ccarbonate is 13C‐enriched due to release of 13C‐depleted methane as a by‐product of microbial fermentation in the digestive tract. As methane emission is constrained by plant secondary metabolites in browse, the latter effect becomes more pronounced with higher levels of C4 grass in the diet. Increases in δ13Ccarbonate are also larger in ruminants than nonruminants. Accordingly, we show that Δ13Ccollagen‐carbonate spacing is not constant within herbivores, but increases by up to 5 ‰ across species with different diets and physiologies. Such large variation, often assumed to be negligible within trophic levels, clearly cannot be ignored in carbon isotope‐based diet reconstructions.

Comparative isotope ecology of western Amazonian rainforest mammals

“…The lower than expected values in ε* bioapatite-keratin observed in some Amazonian primary consumers might be explained in a similar way. Other studies have also shown highly variable ε* bioapatite-protein values within a free-ranging herbivore mammalian community ( 39 ), as well as ε* bioapatite-protein poorly distinguishing trophic levels ( 40 ), suggesting that the ε* bioapatite-protein within dietary categories (especially among primary consumers) should not be expected to be uniform.…”

Review: Comparative methane production in mammalian herbivores

“…One possible approach to determine the CH 4 strategy of a larger number of species could be the diet-bioapatite carbon isotope enrichment offset. Studies in which such data have been applied to herbivores have implied a difference in CH 4 emissions between herbivore digestion types (Codron et al, 2018;Tejada-Lara et al, 2018). However, the data from Codron et al (2018) suggest little differences between the hindgut fermenters rock hyrax, black and white rhinoceros (Diceros bicornis, Ceratotherium simum), warthog (Phacochoerus africanus) or even a zebra species (Equus quagga) and ruminants.…”

“…Studies in which such data have been applied to herbivores have implied a difference in CH 4 emissions between herbivore digestion types (Codron et al, 2018;Tejada-Lara et al, 2018). However, the data from Codron et al (2018) suggest little differences between the hindgut fermenters rock hyrax, black and white rhinoceros (Diceros bicornis, Ceratotherium simum), warthog (Phacochoerus africanus) or even a zebra species (Equus quagga) and ruminants. The data from Tejada-Lara et al (2018) potentially corroborate the finding of CH 4 emission in arvicoline rodents (voles) of the present study and indicate little difference between the hindgut fermenters African elephant (Loxodonta africana), the black rhinoceros, the horse, a zebra species (Equus burchelli ) and the pig and the ruminants giraffe (Giraffa camelopardalis), Bactrian camel and guanaco (Lama guanicoe).…”

Carbon isotope differences between grassland and savanna herbivores reveal environmentally driven rather than phylogenetically conserved niches

“… Ref, literature sources: 1 – this study; 2 – Codron et al (); 3 – Codron et al (, and sources therein)); 4 – Sponheimer et al (); 5 – Cerling et al (); 6 – Cerling et al (). …”

“…These data represent 11 of the 19 species for which faecal data are available, comprising data from specimens collected in the field or sampled from the skeletal collections at the Florisbad Quaternary Research Station of the National Museum, Bloemfontein, South Africa. Most ( n = 75) of these data were from the literature (Codron et al , ; Codron et al , ) with a smaller subset of unpublished data ( n = 58) analysed following the procedures, including isolation of the collagen phase and lipid extraction, described in Codron et al ().…”