Correlation of metabolism with tissue carbon and nitrogen turnover rate in small mammals

Department of Biology, American University, Hurst Hall 101, 4400 Massachusetts Ave NW, Washington, DC 202-885-2186, USA.
Oecologia (Impact Factor: 3.09). 12/2006; 150(2):190-201. DOI: 10.1007/s00442-006-0522-0
Source: PubMed

ABSTRACT Stable isotopes have proven to be a useful tool for deciphering food webs, examining migration patterns and determining nutrient resource allocation. In order to increase the descriptive power of isotopes, an increasing number of studies are using them to model tissue turnover. However, these studies have, mostly by necessity, been largely limited to laboratory experiments and the demand for an easier method of estimating tissue turnover in the field for a large variety of organisms remains. In this study, we have determined the turnover rate of blood in mice and rats using stable isotope analysis, and compared these rates to the metabolic rates of the animals. Rats (Rattus norvegicus) (n=4) and mice (Mus musculus) (n=4) were switched between isotopically distinct diets, and the rate of change of δ13C and δ15N in whole blood was determined. Basal metabolic rates (as CO2 output and O2 consumption per unit time, normalized for mass) were determined for the rats and mice. Rats, which were an order of magnitude larger and had a slower metabolic rate per unit mass than mice (0.02 vs. 0.14 O2/min/g), had a slower blood turnover than mice for 13C (t 1/2=24.8 and 17.3 days, respectively) and 15N (t 1/2=27.7 and 15.4 days, respectively). A positive correlation between metabolic rate and blood isotopic turnover rate was found. These are the only such data for mammals available, but the literature for birds shows that mass and whole-body metabolic rates in birds scale logarithmically with tissue turnover. Interestingly, the mammalian data graph separately from the bird data on a turnover versus metabolic rate plot. Both mice and rat tissue in this study exhibited a slower turnover rate compared to metabolic rate than for birds. These data suggest that metabolic rate may be used to estimate tissue turnover rate when working with organisms in the field, but that a different relationship between tissue turnover and metabolism may exist for different classes of organisms.

Download full-text


Available from: Stephen E Macavoy, Sep 27, 2015
31 Reads
  • Source
    • "While it is essential to evaluate stable isotope dynamics across diverse species, there is a taxonomic bias in research on TDFs and isotopic incorporation rates within the vertebrates. Most studies have focused on fish, birds, and mammals (fish: Bosley et al. 2002; Logan et al. 2006; Suring and Wing 2009; Carleton and Martínez del Rio 2010; Hussey et al. 2010; Logan and Lutcavage 2010; Nelson et al. 2011; Kim et al. 2012; Heady and Moore 2013; birds: Hobson and Clark 1992a, 1992b; Bearhop et al. 2002; Ogden et al. 2004; Cherel et al. 2005; Hobson and Yohannes 2007; Bauchinger and McWilliams 2009; Connan et al. 2014; mammals: Tieszen et al. 1983; Roth and Hobson 2000; Lesage et al. 2002; MacAvoy et al. 2006; Stegall et al. 2008; Florin et al. 2011; Browning et al. 2014). Recent studies have also investigated TDFs and incorporation rates in reptiles (Seminoff et al. 2007, 2009; Reich et al. 2008; Fisk et al. 2009; Warne et al. 2010; Murrary and Wolf 2013). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Stable isotope analysis is an increasingly useful ecological tool, but its accuracy depends on quantifying the tissue-specific trophic discrimination factors (TDFs) and isotopic incorporation rates for focal taxa. Despite the technique's ubiquity, most laboratory experiments determining TDFs and incorporation rates have focused on birds, mammals, and fish; we know little about terrestrial ectotherms, and amphibians in particular are understudied. In this study we used two controlled feeding experiments to determine carbon (d 13 C) and nitrogen (d
    Physiological and Biochemical Zoology 07/2015; 88(5):576. DOI:10.1086/682576 · 2.40 Impact Factor
  • Source
    • "Future studies using a series of repeated feedings could be useful to study the rate of carbon turnover in the lipid stores of these animals. Presently most of our knowledge of carbon turnover in vertebrates comes from endothermic models /e.g.,(Voigt et al., 2003; MacAvoy and Arneson, 2006; Bauchinger and McWilliams, 2010)/. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Pythons digesting rodent meals exhibit up to 10-fold increases in their resting metabolic rates (RMR); this increase in RMR is termed specific dynamic action (SDA). Studies have shown that SDA is partially fuelled by oxidizing dietary nutrients, yet it remains unclear whether the proteins and the lipids in their meals contribute equally to this energy demand. We raised two populations of mice on diets labeled with either (13)C-leucine or (13)C-palmitic acid to intrinsically enrich the proteins and lipids in their bodies, respectively. Ball pythons (Python regius) were fed whole mice (and pureed mice three weeks later) after which we measured their metabolic rates and the δ(13)C in the breath. The δ(13)C in the whole bodies of the protein- and lipid-labeled mice were generally similar (i.e., 5.7±4.7‰ and 2.8±5.4‰, respectively) but the oxidative kinetics of these two macronutrient pools were quite different. We found that the snakes oxidized 5% of the protein and only 0.24% of the lipids in their meals within 14 days. Oxidation of the dietary proteins peaked 24 h after ingestion at which point these proteins provided ∼90% of the metabolic requirement of the snakes and by 14 d the oxidation of these proteins decreased to nearly zero. The oxidation of the dietary lipids peaked one day later at which point these lipids supplied ∼25% of the energy demand. Fourteen days after ingestion these lipids were still being oxidized and continued to account for ∼25% of the metabolic rate. Pureeing the mice reduced the cost of gastric digestion and decreased SDA by 24%. Pureeing also reduced the oxidation of dietary proteins by 43%, but it had no effect on the rates of dietary lipid oxidation. Collectively, these results demonstrate that pythons are able to effectively partition the two primary metabolic fuels in their meals. This approach of uniquely labeling the different components of the diet will allow researchers to examine new questions about how and when animals use the nutrients in their meals. © 2015. Published by The Company of Biologists Ltd.
    Journal of Experimental Biology 05/2015; 218(13). DOI:10.1242/jeb.118349 · 2.90 Impact Factor
  • Source
    • "As the SD and W rats had a range of RMR and m values, it is probable that there is a relationship between m and RMR, but the variation in RMR within a species is not great enough to be significantly reflected in m. Previous studies have shown that examining several different species (mice, rats, and birds) shows a significant relationship between m and RMR (reviewed in MacAvoy et al. 2006). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Ecologists interested in studying fluctuating relationships between consumers and nutrient sources are increasingly involved in modeling the rate at which consumers incorporate dietary components. In mammals a correlation between resting metabolic rate (RMR) and tissue turnover may exist across a range of species. Less is known about the variation of tissue turnover rate within a species, and how that correlates with RMR. Here we examine two strains of rats (Rattus norvegicus) with different RMR to test whether variation in RMR is positively correlated with tissue turnover rate within a species. If RMR, a relatively simple measurement, can be correlated with tissue turnover, then this relationship could be used to better interpret ecological functions, including impact of migratory or seasonally available nutrient sources. Here, the changing isotope signature in rat whole blood was modeled using a modified exponential decay equation and a reaction progress variable model. The modeled rate of turnover, metabolic rate (O-2 consumed), and mass were then compared between strains of rats. The mass and RMRs (conditions during which RMRs were determined modified from the ideal, as outlined in the Methods) were significantly different between strains, but half-life and the metabolic tissue replacement component of turnover (as opposed to turnover from mass gain) were not. No significant correlation was found between RMR and metabolic tissue replacement between the strains. Results suggest that within a species showing a range of RMRs, blood tissue turnover should not vary significantly.
    Ecological Research 07/2014; 29(5). DOI:10.1007/s11284-014-1182-x · 1.30 Impact Factor
Show more