Carbon and nitrogen stable isotopic offsets between diet and hair/feces in captive orangutans

Tsutaya, Takumi; Ogawa, Nanako O.; Nomura, Toshiya; Shimizu, Mika; Ohkouchi, Naohiko; Kuze, Noko

doi:10.1007/s10329-021-00940-8

Cited by 6 publications

(15 citation statements)

References 61 publications

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Section: Resultsmentioning

confidence: 96%

“…The Louys and Roberts (2020) data set consists of previously reported data (Bacon et al, 2018; Bocherens et al, 2017; Pushkina et al, 2010; Qu et al, 2014) and newly obtained data from paleontological and historical orangutan fossil specimens from the Pleistocene and Holocene in Southeast/East Asia. In this study, carbon isotope offset values of diet–bioapatite and diet–feces were set as −11.8‰ (Malone et al, 2021) and − 1.84‰ (Tsutaya, Ogawa, et al, 2021), respectively, adopting ratios reported in previous literature. The Suess effect was considered when comparing fecal δ 13 C with fossil δ 13 C, and 1.5‰ was subtracted from ratios of fossil specimens (Friedli et al, 1986).…”

Section: Methodsmentioning

confidence: 99%

“…Bark samples were cut into tiny pieces using a pair of scissors. Applying the method described by Tsutaya et al ( 2017 ) and Tsutaya, Ogawa, et al ( 2021 ), we crushed fecal samples mildly, sieved them with 0.5‐mm mesh, and used the dropped powder for analysis. The freeze‐dried samples of ~0.03–0.04 mg were placed in pre‐cleaned tin capsules.…”

Section: Methodsmentioning

confidence: 99%

“…The Suess effect was considered, and 1.5‰ was subtracted from δ 13 C values of fossil specimens (Friedli et al, 1986) to compare modern fecal δ 13 C with fossil δ 13 C values. Typical error ranges of isotopic offsets between diet and apatite (Malone et al, 2021) and between diet and feces (Tsutaya, Ogawa, et al, 2021) are also shown Carbon and nitrogen stable isotope analysis was applied to feces and plant foods of wild Bornean orangutans in DVCA to characterize their feeding ecology. Stable carbon and nitrogen isotope ratios of plant species consumed by wild Bornean orangutans were homogenous, contrary to Hypothesis 1 (isotopic variation among plant parts).…”

Section: Limitations Of This Study and Future Directionsmentioning

confidence: 99%

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Stable isotopic investigation of the feeding ecology of wild Bornean orangutans

Tsutaya

Wong

Malim

et al. 2022

American Journal of Biological Anthropology

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Objectives We applied stable carbon and nitrogen isotope analyses to wild Bornean orangutans (Pongo pygmaeus morio) to investigate the feeding ecology of wild orangutans. Compared with African great ape species, orangutans are adapted to environments with chronic lower nutrition. But the usefulness of stable isotope analysis in the study of wild orangutan feeding ecology has not been fully explored. Methods The study site was a primary lowland dipterocarp forest in the Danum Valley, Sabah, Malaysia. A total of 164 plant and 94 fecal samples collected across 18 months were analyzed. Results Carbon and nitrogen stable isotope ratios of plant food samples do not systematically vary by plant parts (i.e., bark, fruits, and leaves). Elemental composition and stable isotope ratios of orangutan feces do not systematically vary by orangutans' sex and age classes, although fecal stable isotope ratios showed seasonal fluctuations. No isotopic contribution of breast milk was found in fecal samples collected from individuals at 2.7–6.5 years of age. Conclusions This study revealed key characteristics of the stable isotope ecology of wild orangutans living in a primary lowland forest. Although there was little isotopic variation among plant foods and orangutan individuals, seasonal fluctuations in baseline isotope ratios or orangutans' diet were found in Danum valley.

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Section: Resultsmentioning

confidence: 96%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Limitations Of This Study and Future Directionsmentioning

confidence: 99%

See 2 more Smart Citations

Stable isotopic investigation of the feeding ecology of wild Bornean orangutans

Tsutaya

Wong

Malim

et al. 2022

American Journal of Biological Anthropology

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“…However, it is labor intensive as well as cost expensive and often uses large amounts of water that could or should be considered biohazardous waste. It may also be for the latter reason that the few studies that conducted dry sieving before isotope analysis were those on captive primates housed in zoos under veterinary care, in which aerosols from dried feces do not pose a considerable health risk (Reitsema, 2012; Tsutaya et al, 2017, 2021). Even more importantly for the study of wild primates, systematic wet sieving of fecal matter requires rather large sample amounts of >15 g, often much more than what primatologists can cost‐effectively store and later transport out of the field.…”

Section: Discussionmentioning

confidence: 99%

A skew in poo: Biases in primate fecal isotope analysis and recommendations for standardized sample preparation

Oelze

O'Neal

Wittig

et al. 2022

American J Primatol

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Feces are a treasure trove in the study of animal behavior and ecology. Stable carbon and nitrogen isotope analysis allows to assess the dietary niches of elusive primate species and primate breastfeeding behavior. However, some fecal isotope data may unwillingly be biased toward the isotope ratios of undigested plant matter, requiring more consistent sample preparation protocols. We assess the impact of this potential data skew in 114 fecal samples of wild bonobos (Pan paniscus) by measuring the isotope differences (Δ13C, Δ15N) between bulk fecal samples containing larger particles (>1 mm) and filtered samples containing only small particles (<1 mm). We assess the influence of fecal carbon and nitrogen content (ΔC:N) and sample donor age (subadult, adult) on the resulting Δ13C, Δ15N values (n = 228). Additionally, we measure the isotope ratios in three systematically sieved fecal samples of chimpanzees (Pan troglodytes verus), with particle sizes ranging from 20 μm to 8 mm (n = 30). We found differences in fecal carbon and nitrogen content, with the smaller fecal fraction containing more nitrogen on average. While the Δ13C values were small and not affected by age or ΔC:N, the Δ15N values were significantly influenced by fecal ΔC:N, possibly resulting from the differing proportions of undigested plant macroparticles. Significant relationships between carbon stable isotope ratios (δ13C) values and %C in large fecal fractions of both age groups corroborated this assessment. Δ15N values were significantly larger in adults than subadults, which should be of concern in isotope studies comparing adult females with infants to assess breastfeeding. We found a random variation of up to 3.0‰ in δ13C and 2.0‰ in nitrogen stable isotope ratios within the chimpanzee fecal samples separated by particle sizes. We show that particle size influences isotope ratios and propose a simple, cost‐effective filtration method for primate feces to exclude larger undigested food particles from the analysis, which can easily be adopted by labs worldwide.

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Dogs occupying grassy habitat near protected areas in eastern Madagascar rely on foods from forests

Hixon

Neelin

Chan

et al. 2022

Plants People Planet

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Societal Impact StatementIdentifying where introduced animals fit in a food web relative to each other and to endemic species is key for biodiversity conservation planning. Using a multiproxy study of dog feces from eastern Madagascar, we infer that even dogs that spend time in derived grasslands typically eat forest‐derived foods. Regardless of the time that dogs spend in cleared forest, their impacts are likely concentrated on forest‐dwelling prey. If dogs in forests mostly consume threatened endemic animals (and not other introduced animals such as rats), then the exclusion of dogs from protected forests should be a priority.Summary Introduced predators on islands can help control invasive species yet can also contribute to the extirpation and extinction of endemic taxa. The spread of dogs on Madagascar by ~1000 years ago coincided with the introduction of livestock and spread of grazer‐adapted grasslands, and we help evaluate the extent to which modern dogs are part of novel grassland food webs. To infer dog diet, we identified food remains, where possible, and conducted stable isotope ratio analysis for n = 100 modern dog feces collected in derived grassland at varying distances from protected forest edges around Analamazoatra and Andasibe‐Mantadia National Park in eastern Madagascar. Animal remains in feces and the observed range of fecal δ15N values are consistent with dog meals at multiple trophic levels. However, the observed distribution of fecal δ13C values suggest that few dogs in the study area consumed food derived from open C4 grasslands. Existing data suggest that dogs rely primarily on C3 consumers inhabiting forest biomes (forest‐dwelling animals) for their prey, which may include endemics such as tenrecs, Malagasy rodents, and lemurs and introduced rodents such as rats. These findings indicate that dogs are not confined to the anthropogenic niche defined by grazer‐adapted grasslands, but rather use and impact animal food resources associated with protected forests. Higher resolution study of dog diet and mobility can further clarify the potential for dogs to exploit endemic prey, compete with endemic predators, and spread disease across ecotones.

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Carbon and nitrogen stable isotopic offsets between diet and hair/feces in captive orangutans

Cited by 6 publications

References 61 publications

Stable isotopic investigation of the feeding ecology of wild Bornean orangutans

Stable isotopic investigation of the feeding ecology of wild Bornean orangutans

A skew in poo: Biases in primate fecal isotope analysis and recommendations for standardized sample preparation

Dogs occupying grassy habitat near protected areas in eastern Madagascar rely on foods from forests

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