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SEMINOFF ET AL.—STABLE ISOTOPES IN TRACHEMYS 539toward the d 13 C and d 15 N signatures of Diet Bafter the diet switch. The exponential decaymodels showed a significant fit for carbon inblood plasma, and nitrogen in blood plasma,whole blood, and liver (non-linear regression, P, 0.05; Fig. 1). For carbon, however, becauseblood plasma had not reached isotopic equilibriumwith Diet A during the acclimation period,we have low confidence in the exponential decaymodel results and therefore do not report thet 1/213C for this tissue. For nitrogen, the half-lifedurations in blood plasma, whole blood, andliver were 35.6 d, 38.7 d, and 52.5 d, respectively(Fig. 1; Table 3). Because turnover is reachedafter approximately four half-lives (Hobson,1993; Martínez del Rio and Wolf, 2005), weestimate that nitrogen turnover times in bloodplasma, whole blood, and liver are 142 d, 155 d,and 210 d, respectively. Although we did notestimate t 1/215N for the remaining tissues due totheir lack of significant curve fits, the fact thatstable-nitrogen changes did not show a significantfit to the exponential decay model indicates thatthe turnover times must be greater than192 days. Furthermore, the apparent lack ofstable carbon isotope diet–tissue equilibriumsuggests that carbon turnover time is longer than146 days, the duration of the acclimation period.DISCUSSIONMeasuring stable isotope discrimination andelemental turnover in emydid turtles is a necessaryprocess to enable the correct interpretationof field data generated for this group. In thisstudy we provide the first stable isotope informationfor Trachemys scripta, one of the mostabundant and widespread of all freshwater turtles(Gibbons, 1990). Although reliable stable carbonisotope values proved elusive, we were able toestimate nitrogen isotope discrimination andturnover values for T. scripta tissues that reachedisotopic equilibrium with the experimental diets.Of the seven tissues for which we calculatedDiet A D dt15N (range 5 +1.9% to +3.8%), allwere within the range of values established forother vertebrate taxa. In soft-tissues of birds andmammals, D dt15N factors range from +0.2% to+5.2% (Hobson and Clark, 1992a; Kurle, 2002;Klaassen et al., 2004), whereas those for fish are+2.3% to +5.0% (Hesslein et al., 1993; Pinnegarand Polunin, 1999). For the Green Sea Turtle,Chelonia mydas, D dt15N factors range from +0.22%to +2.92% (Seminoff et al., 2006). In addition tothe consistencies in the overall range of discrimination,we found similarities in the relativediscrimination levels between tissues of T. scriptawith homologous tissues of other vertebrates. Forexample, the pattern of greater D dt15N in T.scripta blood plasma (+3.8%) versus red bloodcells (+1.9%) was also found in a variety of bird(Pearson et al., 2003; Evans Ogden et al., 2004)and mammal species (Roth and Hobson, 2000;Lesage et al., 2002; Klaassen et al., 2004).The observed D dt15N differences among thetissues of T. scripta and in tissues of other specieslikely were caused, at least in part, by variations inthe protein and amino acid compositions ofdifferent tissues since these components candiffer in their nitrogen isotope content (Petersonand Fry, 1987). As suggested previously, thecompositional differences may result from selectiverouting of exogenous nutrients during tissuemaintenance and construction, and from differentialmobilization of endogenous resources intotissues or tissue components (Macrae and Reeds,1980; Peterson and Fry, 1987; Gannes et al.,1997). In addition, loss of heavier or lighterisotopes via cellular metabolism may have playeda role in the differences among tissues (Ganneset al., 1997; Martínez del Rio and Wolf, 2005).However, we are unable to ascertain the relativecontributions of these factors to our resultsbecause of the unknown isotopic differencesamong dietary nutrients and body tissue components.Elucidating the relationships between ananimal’s diet and the fate of assimilated dietarycomponents, synthesized components, and endogenousnutrients will be important to fullydetermine the biochemical mechanisms of isotopediscrimination.In addition to stable-nitrogen isotope discrimination,we derived estimates of elementalnitrogen turnover in three T. scripta soft tissuesthat showed a significant fit to the model curve.The half-lives found here (35.6–52.5 d) areamong the longest reported to date, and oftenan order of magnitude greater than those ofhomologous tissues in other vertebrate species.For example, half-lives among birds and mammalsrange from 1.7 d to 3.5 d in blood plasma(Hilderbrand et al., 1996; Pearson et al., 2003)and from 0.5 d to 15.7 d in whole blood(Bearhop et al., 2002; Hobson and Bairlein,2003; Pearson et al., 2003; Evans Ogden et al.,2004). Although the extended longevity ofnucleated red blood cells in T. scripta (#11 mo,Frische et al., 2001) likely affected the N half-lifein whole blood, we believe the greater N half-livesin T. scripta result from the lower basal metabolismand correspondingly slower protein turnoverin poikilotherms versus homeotherms (Bennettand Dawson, 1976; Else and Hulbert, 1981;McNab, 2002). In support, Martínez del Rio andWolf (2005) suggest that fractional isotopicincorporation into body tissues is roughly pro-
540 COPEIA, 2007, NO. 3portional to protein turnover and that slowmetabolism may thereby reduce the uptake ofendogenous protein components for tissuemaintenance and growth.With respect to carbon, our derivations ofdiscrimination and half-life were hampered bya lack of apparent isotopic equilibrium betweenturtle tissues and captive diets and the poor fits ofthe exponential decay model. The apparent lowrates of diet-derived carbon integration intobody tissues is intriguing, particularly for tissuesof high metabolic activity (blood plasma, liver).Assuming that consumer tissues maintain steadystate isotopic equilibrium with their diet, perhapsthe feeding trials were of insufficientduration to allow for d 13 C equilibration of T.scripta tissues with the captive diets. However,although no tissues equilibrated with the carbonisotope composition of the diet, the trialduration was sufficient for the integration ofDiet A d 15 N values into most tissues. Thisdichotomy suggests that carbon and nitrogenmay become decoupled during metabolic processesand raises interesting questions about themetabolic pathways responsible for uptake ofexogenous carbon and nitrogen. Interestingly,Hobson and Stirling (1997) report a lack ofintegration of dietary carbon into body tissues ofpolar bears (Ursus maritimus), and Voigt et al.(2003) report dramatically slow incorporation ofdietary carbon into tissues of two nectar-feedingbat species. However, there is little informationon the uncoupling of elemental carbonand nitrogen during metabolic processes, norare there sufficient data on the relativeinput of endogenous versus exogenous carbonand nitrogen to adequately interpret theseresults.The lack of apparent changes in the d 13 Cvalues of T. scripta tissues after the diet switchmay also relate to composition of the experimentaldiets. Perhaps the differences in d 13 Cvalues between Diet A and Diet B were not ofsufficient magnitude to adequately measureturnover (1.6% for Diet B-A with lipids; 3.3%for Diet B-A without lipids). This possibility isparticularly relevant considering the relativelyhigh variance in d 13 C values among tissues foreach sampling period (Fig. 1). However, a morelikely scenario relates to the high lipid concentrationin Diet B. Because lipids are depleted in13C relative to protein and carbohydrates (De-Niro and Epstein, 1978; Peterson and Fry, 1987),differential integration of these dietary macromoleculesinto body tissues may result in isotopediscrimination values that are unexpected basedon the isotopic compositions of whole diet. Inthis case, despite the overall lesser 13 C-depletionin Diet B (d 13 C 5 221.9%) versus Diet A (d 13 C5 223.5%), the extremely high lipid content ofDiet B (24%) may have resulted in tissue carbonreservoirs that were more depleted in 13 C, theresult of which may be tissue d 13 C values thatapproach the expected values for turtlesmaintained on Diet A. Thus, dietary carbonmay have been integrated but masked by lipidisotopic compositions. As with previous studiesemploying stable isotope analysis, our interpretationsof carbon and nitrogen turnover (or lackthereof) would benefit greatly from a betterunderstanding of animal nutritional ecology,particularly relating to lipid assimilation (Stottet al., 1997; Schlechtriem et al., 2004).The results of this study include two importantfindings that bear on the interpretation of fieldisotopic data for assessing trophic ecology offreshwater turtles. First, although D dt15N in thespecies is generally consistent with discriminationfactors established previously for homeothermicand poikilothermic vertebrates, the range invalues (61.9% for Diet A and 63.3% for DietB) has substantial consequences on the calculationof trophic structure, nutrient sources, anddiet composition. Recall that consumer tissuesare generally thought to be enriched in 15 N overtheir diet by 3–5% (DeNiro and Epstein, 1981;Miniwaga and Wada, 1984; Peterson and Fry,1987). With discrimination variability .3%, ourresults indicate that calculation of trophic positionscould be erroneous by up to a full trophicstep if the correct tissue-specific D dt value is notused. This underscores the importance of elucidatingthe isotope discrimination factors for eachtissue type prior to its use for making inferencesabout the trophic status of study organisms.Second, the turnover of blood and liver nitrogenis substantially slower than values reported previouslyfor most taxa. Our results indicate that thetemporal diet histories of T. scripta reflected byisotopic analyses of tissues will be of long termnature, ranging from˜ 5 to 7 months. While thissupports the value of using stable isotopes tomonitor dietary changes over the course of a yearor more, it indicates that this technique is notappropriate for addressing intra- and inter-seasonalvariability in diet intake. However, isotopicdiscrimination and turnover in T. scripta may varyunder different environmental circumstances,particularly for turtles that are nutrient limited(Hobson et al., 1993). Field metabolic rates inwildlife species are often substantially higher thanmetabolic rates of captive animals (McNab,2002), and it is thus possible that tissue componentsin wild turtles turnover more rapidly thanthose in captivity. Based on these considerations,we encourage additional studies of T. scripta
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