Intrapopulation Variability Shaping Isotope Discrimination and Turnover: Experimental Evidence in Arctic Foxes

Abstract

BackgroundTissue-specific stable isotope signatures can provide insights into the trophic ecology of consumers and their roles in food webs. Two parameters are central for making valid inferences based on stable isotopes, isotopic discrimination (difference in isotopic ratio between consumer and its diet) and turnover time (renewal process of molecules in a given tissue usually measured when half of the tissue composition has changed). We investigated simultaneously the effects of age, sex, and diet types on the variation of discrimination and half-life in nitrogen and carbon stable isotopes (δ15N and δ13C, respectively) in five tissues (blood cells, plasma, muscle, liver, nail, and hair) of a top predator, the arctic fox Vulpes lagopus.Methodology/Principal FindingsWe fed 40 farmed foxes (equal numbers of adults and yearlings of both sexes) with diet capturing the range of resources used by their wild counterparts. We found that, for a single species, six tissues, and three diet types, the range of discrimination values can be almost as large as what is known at the scale of the whole mammalian or avian class. Discrimination varied depending on sex, age, tissue, and diet types, ranging from 0.3‰ to 5.3‰ (mean = 2.6‰) for δ15N and from 0.2‰ to 2.9‰ (mean = 0.9‰) for δ13C. We also found an impact of population structure on δ15N half-life in blood cells. Varying across individuals, δ15N half-life in plasma (6 to 10 days) was also shorter than for δ13C (14 to 22 days), though δ15N and δ13C half-lives are usually considered as equal.Conclusion/SignificanceOverall, our multi-factorial experiment revealed that at least six levels of isotopic variations could co-occur in the same population. Our experimental analysis provides a framework for quantifying multiple sources of variation in isotopic discrimination and half-life that needs to be taken into account when designing and analysing ecological field studies.

Slow Isotope Turnover Rates and Low Discrimination Values in the American Alligator: Implications for Interpretation of Ectotherm Stable Isotope Data

“…Ectotherms generally exhibit slower metabolic rates than do endotherms (Hulbert and Else 2004); thus, we would expect ectotherm tissues to be characterized by isotope turnover rates slower than those for endotherm tissues. Dalerum and Angerbjorn (2005), in a review of mammal and bird isotope studies, reported no estimated complete turnover rates (t 1/2 # 4) for plasma or RBCs greater than 160 d, with all but two rates less than 20 d. More recent studies have also found relatively Lecomte et al 2011). In contrast, reptile plasma and RBC tissues can display short estimated complete turnover rates (e.g., 19 d for Caretta caretta; table 2) but also much longer rates (e.g., 1,109 d for Alligator mississippiensis; table 2) that have never been found in endotherms.…”

Anthropogenic food use and diet overlap between red foxes (Vulpesvulpes) and arctic foxes (Vulpeslagopus) in Prudhoe Bay, Alaska

“…We used values from Roth and Hobson (2000) for red foxes (red blood cells: ⌬␦ 13 C = 0.7‰ and ⌬␦ 15 N = 2.6‰; muscle: ⌬␦ 13 C = 1.1‰ and ⌬␦ 15 N = 3.3‰; hair: ⌬␦ 13 C = 2.6‰ and ⌬␦ 15 N = 3.2‰) and from Lecomte et al (2011) for arctic foxes (red blood cells: ⌬␦ 13 C = 0.5‰ and ⌬␦ 15 N = 1.8‰; muscle: ⌬␦ 13 C = 0.4‰ and ⌬␦ 15 N = 1.8‰; hair: ⌬␦ 13 C = 2.2‰ and ⌬␦ 15 N = 3.3‰). No fractionation estimate of fox bone collagen exists, so we used the mean fractionation estimates (⌬␦ 13 C = 1.0‰ and ⌬␦ 15 N = 3.6‰) calculated from wolf (Canis lupus L., 1758) bones (Bocherens and Drucker 2003).…”

“…No fractionation estimate of fox bone collagen exists, so we used the mean fractionation estimates (⌬␦ 13 C = 1.0‰ and ⌬␦ 15 N = 3.6‰) calculated from wolf (Canis lupus L., 1758) bones (Bocherens and Drucker 2003). We accounted for uncertainty in fractionation estimates in our mixing model analysis by using estimates from Lecomte et al (2011) for red blood cells and muscle (SD of ⌬␦ 13 C = 0.1‰ and SD of ⌬␦ 15 N = 0.5‰) and for hair (SD of ⌬␦ 13 C = 0.4‰ and SD of ⌬␦ 15 N = 0.6‰); we used these values for both fox species. Bocherens and Drucker (2003) did not estimate error for their wolf bone collagen fractionation values; therefore, we used large values (SD of ⌬␦ 13 C = 1.0‰ and SD of ⌬␦ 15 N = 1.0‰) to account for uncertainty in the red fox bone collagen fractionation.…”

“…We used stable isotope ratios of red blood cells (or muscle) from foxes captured in April and May to infer diet during late winter, depending on which was available. Because red blood cells and muscles have similar turnover rates and diet-tissue fractionation in foxes, we use them interchangeably as measures of the winter diet (Roth and Hobson 2000;Lecomte et al 2011). We also analyzed the stable isotopic composition of bone collagen in red foxes, as an averaged measure of lifetime diet (Tieszen et al 1983).…”

Monitoring Least Weasels after a Winter Peak of Lemmings in Taimyr: Body Condition, Diet and Habitat Use

“…The stable isotope values of a consumer are equal to the mean values of its diet minus a discrimination factor, which reflects the fact that certain biochemical processes discriminate against the heavy isotope ( Deniro and Epstein, 1981). Discrimination factors are likely to be tissue-and species-specific, and the results of mixing models have been shown to be sensitive to changes in discrimination factors (Bond and Diamond, 2011 Lecomte et al, 2011): 1.1 and 3.0 for muscle and 2.4 and 3.4 for fur, for δ 13 C and δ 15 N, respectively. The estimation of the mixing proportions in SIAR is based on Markov Chain Monte Carlo resampling (Parnell et al, 2010).…”