Effect of seasonal dormancy on turnover rate and isotopic discrimination factor in Salvator merianae (Tegu lizard)

Effect of seasonal dormancy on turnover rate and isotopic discrimination factor in Salvator merianae (Tegu lizard) | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL This is a preprint and has not been peer reviewed. Data may be preliminary. 5 June 2025 V1 Latest version Share on Effect of seasonal dormancy on turnover rate and isotopic discrimination factor in Salvator merianae (Tegu lizard) Authors : Luciana M. Beloto , Marina Sartori , Thiago S. Marques , Augusto Shinya Abe , Barbara Protocevich 0009-0007-7350-4831 [email protected] , Ronnie Von M. Ferreira , Marcelo Moreira 0000-0001-6769-5570 , and P Camargo Authors Info & Affiliations https://doi.org/10.22541/au.174911956.64150159/v1 195 views 123 downloads Contents Abstract Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract This study explores the effects of seasonal dormancy on the turnover rate and isotopic discrimination factors of carbon (δ 13 C) and nitrogen (δ 15 N) in the tissues of Salvator merianae , also known as the Tegu lizard. Both adult and juvenile lizards were monitored through various phases, including pre-dormancy, active periods, and arousal from dormancy. The isotopic analysis revealed that plasma has a faster turnover rate compared to red blood cells, with adults exhibiting turnover half-lives of 23 days for δ 13 C in plasma, while juveniles showed a broader range due to slower adaptation. Interestingly, the study found that the isotopic discrimination factors varied between the two tissues, with adults displaying greater enrichment of δ 15 N in plasma during dormancy arousal, suggesting significant mobilization of endogenous amino acids. Additionally, the results highlight the role of facultative endothermy during reproduction, which appears to accelerate isotopic turnover in both adults and juveniles. Despite minimal body mass loss during dormancy, the metabolic processes involved, such as lipid mobilization and protein catabolism, were crucial in sustaining the lizards. The variability in isotopic discrimination factors observed in this study underscores the complexity of metabolic adaptations in Salvator merianae , particularly in response to prolonged fasting and seasonal dormancy. These findings provide deeper insights into the physiological strategies employed by ectotherms to cope with extreme environmental conditions. Introduction In studies with wild species, estimating the turnover rate of animal tissues is essential for determining the discrimination factor, which must reflect a condition of balance between the diet and the tissues. The isotopic turnover rate can be defined as the time in which a tissue or the entire consumer takes to reflect the isotopic composition of its diet (TIESZEN et al., 1983; GANNES; MARTINEZ DEL RIO; KOUCH, 1998), in a process that occurs due to tissue growth and replacement (MACAVOY; MACKO; ARNESON, 2005). Knowledge of the differences in turnover rates is essential for choosing the appropriate tissue according to the objectives of the study, since turnover rates vary between the types of tissues that reflect different time scales (DALERUM; ANGERBJÖRN, 2005). Tissues with high turnover rate reflects the isotopic composition of foods eaten recently, on the other hand, the tissues with lower turnover rates reflect the isotopic composition of food consumed over long periods (HOBSON; CLARK, 1992; 1993). However, information on the discrimination factors and turnover estimates of different animal tissues under experimental conditions are scarce in the literature, especially in relation to reptiles (WARNE; GILMAN; WOLF, 2010). Pioneer studies point out that the difference in the isotopic composition between the animal and its diet is represented by the discrimination factor, and its flow can vary from 1‰ for carbon and 3‰ for nitrogen (CAUT; ANGULO; COURCHAMP, 2007). Over the years, other studies have suggested that the difference between the animal and its diet may vary between vertebrate taxa. The range of variation can be 0.4‰ - 7.9‰ for carbon and 0.1‰ - 4.0‰ for nitrogen (CAUT; ANGULO; COURCHAMP, 2009). In addition, studies have elucidated that both the turnover rate and consequently the isotopic discrimination factor can vary beyond the taxa and between tissues. It can also vary in relation to age, growth rates, quality of the diet, proportion of the diet, size and temperature (CAUT; ANGULO; COURCHAMP, 2007, MARTINEZ DEL RIO et al., 2009). Martinez Del Rio et al. (2009) proposed that the turnover rate can vary strongly depending on the body size, being that it would be faster for smaller animals and the opposite for larger animals. Zanden et al. (2015) found in their study that for ectotherms the half-life of δ 13 C and δ 15 N predictably increased with smaller body size, proposing a simple empirical model to estimate it. Several studies show that the turnover rate of 13 C and 15 N associated with prolonged fasting or food restriction can change significantly (HOBSON et al., 1993; POLISCHUK; HOBSON; RAMSAY, 2001; CHEREL et al. 2005; FULLER et al. 2005; GAYE-SIESSEGGER et al. 2007). The incorporation of macronutrients is influenced by the rates of tissue catabolism, anabolism and the metabolic pathways being used (CARLETON; MARTINEZ DEL RIO, 2005). Polar bears are physiologically adapted to fast for long periods during hibernation, to do so, they mobilize lipids and recycle urea nitrogen and, thus, minimize the loss of muscle mass (STENYINKEL et al., 2013). The mobilization of lipids has been aimed at releasing endogenously produced water, thus reducing water intake (COSTA, 2009; ORTIZ, 2001), which is advantageous for an animal in a dormant period under metabolic depression. Tegus lizards mobilize lipids during the period of seasonal dormancy and during reproduction that occurs after they emerge (ABE, 1983; 1995; ANDRADE et al. 2004; TATERSALL et al. 2016). In king penguins found depletion at δ 13 C in the plasm (CHEREL et al. 2005), suggesting a relationship with the mobilization of lipids during prolonged fasting. The decrease in δ 13 C values occurs because the lipids are depleted by 13 C, and thus, the δ 13 C values of consumers become depleted (GAYE-SIESSEGGER et al. 2004). On the other hand, enrichment at δ 15 N in animals that have prolonged fasting or food restriction may occur (HERTZ, 2015). This finding may be related to the catabolism of muscle tissues. These results indicate that animals can use endogenous amino acids at that moment, even if protein synthesis is reduced, it is still sufficient to raise δ 15 N. Hertz (2015) found in his work an average increase of 0.5 ‰ in δ 15 N concomitantly with nutritional restriction. These data are in accordance with the model proposed by Martinez Del Rio and Wolf (2005), called negative nitrogen balance, used for both food restriction and prolonged fasting related to migration, seasonal dormancy, hibernation and aestivation. This model predicts that the incorporation of nitrogen in tissues is less than the loss of nitrogen by excreta (MARTINEZ DEL RIO; WOLF, 2005). In this context, studies aimed at determining the turnover rate and the discrimination factor are extremely important. Because the use of inaccurate data of the discrimination factor for a given taxon can result in problems in the evaluation of the contribution of dietary sources in the diet or in the establishment of the trophic level (CAUT; ANGULO; COURCHAMP, 2009). The objective of this work was to determine the turnover rate and the discrimination factor of Salvator merianae adults and juveniles during the activity phase, pre-dormancy and in the arouse of seasonal dormancy. Material and Methods Experimental Protocol This study was carried out with 8 adults and 8 juveniles individuals of Salvator merianae held captive in Jacarezário dependencies of the Department of Zoology of the State. This breeding facility for scientific purposes at UNESP in Rio Claro is registered in Brazilian Institute of the Environment and Renewable Natural Resources (IBAMA). Experimental procedures were conducted according to Ethics Committee on the Use of Animals (protocols: CEUA/CENA 003/2015 and CEUA/UNESP 5888/2015) and license of the Biodiversity Authorization and Information System (Sisbio nº 47958-1). The enclosures (two units) that housed the individuals had dimensions of 4.66 m x 3 m with masonry burrows centrally (85 x 63 x 30 cm) with depth partially below the ground. The lizards were fed daily and had free access to water. Tegus were individualized with the aid of microchips throughout the experiment. Biometric measurements (total length) were taken with a measuring tape (precision: 0.1 cm), and body mass (BM) was recorded with a dynamometer (precision: 10 g). Experiments to estimate the turnover rate and the isotopic discrimination factor of animal tissues involve changing diets with widely different isotopic composition. In this way, the tegu lizards were initially fed with a controlled diet of ground chicken necks from the same company, and the chickens are fed commercial feed [composition: corn (C4) and soy (C3)], supplemented with feed of rabbit, representing 92% and 8% respectively throughout their lives. Soon after the initial experimental collection, the diet was changed with the addition of soybean in the protein (chicken) in the proportion of 1: 1. Blood samples were collected from individuals through puncture of the caudal vein (KAPLAN, 1968). Blood aliquots were collected (1 ml for adults and 300 µl for juveniles) and immediately centrifuged for five minutes at 13000 rpm (Sigma, UK) in order to separate red blood cells and plasm. The first collection was in September 2016 in the wake of prolonged fasting called zero time, afterwards, there was a change of diet and new samples collections occurred at times 15, 30, 45, 60, 75, 90, 105, 135, 165, 195 and 225 days. After 225 days, the animals started seasonal dormancy again and arouse up in September 2017, generating 345 days fasting collection. Red blood cells, plasm samples and diet were dried in an oven at 50ºC until they reached constant mass, macerated with the aid of a mortar and placed (0.8–1.0 mg) in small tin capsules. The isotopic compositions of carbon and nitrogen were determined by the on-line combustion of the sample by CF-IRMS in an elementary analyzer Carlo Erba (CHN-1110) coupled to the Thermo Scientific mass spectrometer (Delta Plus), in the Isotopic Ecology Laboratory, Center for Nuclear Energy in Agriculture University of São Paulo. The calculation of the isotopic composition of carbon and nitrogen was performed using the equation: \begin{equation} \delta^{13}C\ \textperthousand\ \ ou\ \ \delta^{15}N\ \textperthousand\ =\frac{R_{\text{sample}}-R_{\text{standard}}}{R_{\text{standard}}}\nonumber \\ \end{equation} where R is the 13 C / 12 C or 15 N / 14 N molar ratio in the sample and in the standard, the results were presented in delta (δ) per thousand (‰). The standards used for carbon and nitrogen were Vienna-PeeDee Belemnite (PDB) and atmospheric air (AIR), respectively. The analytical error of the isotopic measurements 0.3 ‰ and 0.5 ‰ for carbon and nitrogen, respectively. Data analysis method The isotopic turnover rate of 13 C and 15 N for red blood cells and plasm were determined using exponential decay curves applied to the set of isotopic data as a function of time and represented by the equation: y = a + b e ct where: y is the value of δ 13 C and δ 15 N at time t (days after changing the diet), a is the asymptotic isotopic value of the tissue, b is the total change in the values of δ 13 C or δ 15 N after changing the diet and c is fractional tissue turnover (HOBSON; CLARK, 1992). The turnover rate was expressed in terms of half-life. The half-life estimate was determined by equation: t 1/2 = (ln 0,5) / c where: t 1/2 represents the time in days that half of stable isotopes of carbon or nitrogen were replaced in the corresponding tissue. The complete isotopic turnover was estimated by multiplying each value of t 1/2 by 7 (SEMINOFF; BJORDAL; BOLTEN, 2007). Some individuals presented sigmoid results and the Boltzmann sigmoidal regression model was used for the set of isotopic data as a function of time. \begin{equation} \delta^{13}C(t)\ =\ \delta^{13}C\left(f\right)+\frac{\delta^{13}C\left(i\right)-\ \delta^{13}C\left(f\right)}{{1+e}^{\frac{t-o}{\text{dx}}\text{\ \ }}}\nonumber \\ \end{equation}\begin{equation} \delta^{15}N(t)\ =\ \delta^{15}N\left(f\right)+\frac{\delta^{15}N\left(i\right)-\ \delta^{15}N\left(f\right)}{{1+e}^{\frac{t-o}{\text{dx}}\text{\ \ }}}\nonumber \\ \end{equation} where: δ 13 C (i), δ 15 N (i) = initial value of δ 13 C and δ 15 N; δ 13 C (f), δ 15 N (f) = final value of δ 13 C and δ 15 N; δ 13 C (t), δ 15 N (t) = final value of δ 13 C and δ 15 N at any time; χ0 = inflection point of the sigmoid, representing the half-life of carbon and nitrogen; dx = time constant (expressed in time unit); t = experimental time (expressed in days) (SILVA, et al 2007). The rate of isotopic turnover from 15 N to plasm at arouse was determined using the Bézier model applied to the set of isotopic data as a function of time and represented by the equation: y = A + Bt + Ct 2 +Dt 3 where: y = value of the final δ 15 N; A = initial δ 15 N control point (representing the previous diet), B = 15 N control point of the new diet; C = control point of the mixture of the 15 N new diet with the endogenous 15 N in the pre-dormancy phase; D = control point resulting from the endogenous 15 N entry of the seasonal dormancy process; t = experimental time (expressed in days). The discrimination factor was determined by the equation: Δ(p/s) = δ(p) - δ(s) where: Δ (p/s) = discrimination factor; δ (p) = isotopic ratio of the animal’s sample; δ (s) = isotopic ratio of the diet. The total length, body mass, δ 13 C and δ 15 N mean and the respective blood tissue were subjected to ANOVA analysis of variance and the Tukey’s means comparison test (P <0.05). In addition, comparisons were made with the δ 13 C t-Student Test of red cells and plasma in adults and juveniles. All statistical data were analyzed using Origin 2020- © software (OriginLab Corporation). Results The total length of tegus adult did not differ between the sampled periods (F = 0.01; df = 6; p = 0.999) (Table1; Figure1). The same occurred with the body mass over the sampling period (F = 0.50; df = 12; p = 0.907) (Table 2; Figure1). The total length of juvenile lizards did not show any statistical difference between the sampled periods (F = 0.93; df = 10; p = 0.500) (Table3; Figure2). However, the body mass did not vary significantly, however there was a change as expected during the experiment, this change occurred after 135 days (F = 3.73; df = 12; p <0.001) (Table 4; Figure 2). Initially, the type of diet administered throughout the life of the lizards was based on 92% chicken meat mixed with 8% rabbit meal. Chicken with δ 13 C of -15.52 ± 0.15 ‰ and rabbit feed δ 13 C of -25.77 ± 0.58 ‰ and for chicken δ 15 N of 3.72 ± 0.16 ‰ and rabbit feed of δ 15 N 2.98 ± 0.31 ‰. After 15 days from the ground zero of the experiment, a diet of chicken and soybean 1: 1 was administered with δ 13 C -23.01 ± 0.61 ‰ and δ 15 N 0.31 ± 0.27 ‰. The adults showed variation between the periods sampled in the isotopic compositions of carbon and nitrogen for the red blood cells. After 60 days, there was a significant difference in the values (δ 13 C: F = 15.71; df = 11; p values (Table 5,6). The δ 13 C in the adult red cells indicated two adjustment curves. Four individuals responded to the experiment promptly after starting and changing the diet, the fit curve for these data was the 1st order exponential model (Table 6; Figure 3). On the other hand, another four individuals took a long time to adapt to the new diet and for these data the best fit of the curve was the Boltzmann sigmoid model (Table 6; Figure 4). The significant change in nitrogen started at 75 days and remained similar until the end of the sampled period (δ 15 N: F = 4.64; df = 11; p <0.001) the ideal model for adjusting the curve of the eight lizard individuals was the 1st order exponential (Table 5,6; Figure 5). The same response to the experiment was found for the plasm carbon, showing the variation after 15 days, becoming depleted in that period and remaining so until the end of the sample (δ 13 C: F = 29.82; df = 11; p < 0.001) (Table 5,6; Figure 6). After 30 days, the plasm nitrogen isotopic composition changed, becoming lighter in relation to the initial isotopic value of the experiment, however, the seasonal dormancy arouses showed a value of δ 15 N similar to the initial value before changing the diet, configuring a 3rd order cubic curve (δ 15 N: F = 8.36; df = 11; p Tegus juveniles showed the same pattern of variation between the periods sampled in the isotopic compositions of carbon and nitrogen for red cells. The juveniles showed a difference after 75 days, there was a significant difference in the values (δ 13 C: F = 32.84; df = 11; p <0.05) of the red cells in relation to the initial isotopic values (Table 7,8). The red cell carbon of juveniles pointed to two adjustment curves like adults. Three individuals responded to the experiment promptly after starting and changing the diet, the fit curve for these data was the 1st order exponential model (Table 8; Figure 8). On the other hand, other five individuals of tegu were slow to adapt to the new diet and in this way, the curve adjustment was the Boltzmann sigmoid model (Table 8; Figure 9). The significant change in nitrogen started at 45 days and remained similar until the end of the sampled period (δ 15 N: F = 6.68; df = 11; p individuals was the exponential 1st order (Table 7,8; Figure 10). The plasm carbon showed the variation after 45 days and remained so until the end of the sample (δ 13 C: F = 16.17; df = 11; p <0.001) (Table7,8). Four juvenile individuals responded immediately after changing the diet using the 1st order exponential curve (Table 8; Figure 11). The other four individuals took a long time to adapt to the new diet and the model that best fitted the data was the sigmoid Boltzmann (Table 8; Figure 12). However, after 75 days, the plasma nitrogen isotopic composition changed, becoming lighter in relation to the initial isotopic value of the experiment, however, in the arouse of seasonal dormancy the value of δ 15 N was similar to the initial value before changing the diet configuring a 3rd order cubic curve (δ 15 N: F = 6.31; df = 11; p The isotopic carbon composition of the adult cells’ red cells in pre-dormancy was like arouse (t = -0.29; gl = 14; p = 0.774) (Table 9; Figure 13). However, plasma δ 13 C was different between the periods of pre-dormancy and arouse (t = -2.91; gl = 14; p = 0.01) (Table 9; Figure 13). On the other hand, the δ 13 C of juvenile red cell and plasm cells was similar in the pre-dormancy period and at arouse (t = 0.19; gl = 14; p = 0.854; t = 1.73; gl = 14; p = 0.105) respectively (Table 9; Figure 14; Figure 15). Discussion The 13 C turnover rate of Salvator merianae adults and juvenile red cells showed two models (exponential and boltzmann) with different half-lives, being 45 and 75 days and 57 and 78 days, respectively. However, for the 15 N turnover rate, both pointed only to the exponential model 41 and 22 days. Plasma for both adults and juveniles showed a 13 C turnover rate faster than red blood cells. However, adults exposed only the exponential model with the value of 23 days and juveniles exposed the exponential and boltzmann models 20 and 55 days, respectively. Like the literature, plasm points to a faster turnover rate than red cells (HOBSON & CLARK 1993). WARNE et al. (2010) worked with two species of lizards Sceloporus undulatus and Crotaphytus collaris adults. The smaller species (12g) Sceloporus undulatus reached the half-life of red cell carbon in 61 days and plasma in 25 days. The larger species (47g) Crotaphytus collaris showed a slower carbon half-life for red cells of 311 days and 44 days for plasma. The adult and juvenile Salvator merianae species in this experiment were expected to have a 13 C turnover rate of red cells and plasma that were slower than Sceloporus undulatus and Crotaphytus collaris due to their greater body mass, being 59 times for adults and 30 times for juveniles, however, the values were similar to Sceloporus undulatus and faster than that of Crotaphytus collaris lizards. The turnover rate of both 13 C and 15 N of animal tissues varies between taxa. The factors that can influence the turnover rates indicated by the literature are the body size, growth and turnover rate of the protein (MARTINEZ DEL RIO et al. 2009). A study by CARLETON & MARTINEZ DEL RIO (2005), showed that the fractional rate of isotopic incorporation (λ) in the blood of 8 bird species decreased in relation to the body mass size by approximately -¼. However, this model only applies to adult animals with minimal or no growth (MARTINEZ DEL RIO et al. 2009). Therefore, these variations can occur due to the combined effect of body size in mass with the growth rate (MARTINEZ DEL RIO et al. 2009). However, in the case of juvenile gray lizards in the experiment, the growth rate was minimal, and many of these individuals after arousing were already ready for reproduction and fit into sub-adults. In view of this, the growth rate may not have been the main influence on the values of individuals’ turnover rates. However, tegus lizards in the reproductive period show an increase in temperature of 5 to 6ºC above room temperature and remain constant similar to endotherms, and this increase in temperature is sustained by a 5-fold increase in the metabolic rate of these animals during this period (TATTERSALL et al. 2016) and demanding a ratio between faster protein synthesis and degradation (MARTINEZ DEL RIO et al. 2009). Probably the facultative endotherm that this species presents in the reproductive period can influence the turnover rate of 13 C of the red cells and plasm of these individuals, showing differences in relation to the carbon turnover rate of Crotaphytus collaris lizards and similarity to that of Sceloporus undulatus . The most obvious consequence of a long period of starvation during the seasonal dormancy period is the loss of body mass (MCCUE 2010). However, based on specific metabolic demand for mass, smaller individuals would have a higher specific metabolic rate and lose more mass than larger individuals (MCNAB 1999). A loss of body mass of 15% was previously reported in tegus young in course in the first dormancy period (SOUZA et al. 2004), indicating that there is an ontogenic effect on the loss of body mass. In this case, the tegus two-year-old showed a slight difference in mass loss. Juveniles pointed to a 7% loss of body mass as opposed to a 5% loss of adults. Adults showed an enrichment of 0.23 ‰ δ 15 N for red cells and 0.25 ‰ for δ 15 N for plasm. The nitrogen isotopic composition of juveniles during the arousing period showed a depletion of -0.17 ‰ for red cells, showing that the new diet had not stabilized and an enrichment of 0.72 ‰ for plasm. The δ 15 N of the plasma for adults and juveniles on arousing was like the initial value (before changing the diet). Analyzing figures 7 (adults) and 13 (juveniles), the same pattern and safety point for plasma collection are observed at 105 days. At this point the plasm is reflecting the recent diet, after that period a mixture of endogenous 15 N with 15 N of the diet begins to occur. This phase corresponds to the moment when the foraging for this species starts to reduce and they start to gain body mass to enter the seasonal dormancy process. At 237 days, the point occurs when the tegu lizards cease their food and enter the process of seasonal dormancy with a reduced metabolic rate. Even in the face of this scenario, endogenous 15 N continues to be mobilized and can be seen on waking at 345 days when the isotopic value of plasm nitrogen is like the starting point before changing the diet. (CHEREL et al. 2005) in king penguins found an enrichment in δ 15 N of red cells of 0.24 ‰ and in plasma of 0.70 ‰ after prolonged fasting. The value for the red cells was similar to that presented by the tegus adult and of the plasma similar to the tegus juvenile of the experiment and in agreement, with the results in geese found by (HOBSON et al. 1993). Furthermore, these results agree with (CHEREL et al. 2000) who suggests that although prolonged fasting is marked by a reduction in protein synthesis and protein degradation, it is still sufficient to induce δ 15 N enrichment in the long-term tissues through the consumption of hepatic glycogen and endogenous amino acids. Accordingly, SOUZA et al. (2004) and HADDAD (2007), found that the concentration of β-hydroxybutyrate was twice as high during the dormancy period as compared to the activity period showing that a large part of the lipids is mobilized in order to produce ketone bodies to supply the tissues like brain and heart. In the same study, the authors pointed out that the maintenance of glucose-dependent tissues was complemented by gluconeogenesis, with the amino acids of muscle proteins destined for the production of ketone bodies, seen by the increase in pyruvate and ketone bodies in the bloodstream (SOUZA et al. 2004; HADDAD 2007). The same was found by CHEREL et al 2005, during the extended 25-day adult king penguin fast presented high levels of β-hydroxybutyrate and low concentrations of circulating uric acid. All these data support the isotopic data in suggesting the entry of endogenous amino acids sufficient to enrich plasm δ 15 N in the wake of seasonal dormancy. CHEREL et al. 2005 pointed out in his work with king penguin chicks an impoverishment of δ 13 C in plasm, suggesting the use of lipids in energy production during food deprivation. However, with the tegus adult of this work a significant enrichment of 0.38 ‰ do was found in the δ 13 C of the plasm between the periods of pre-dormancy and arousing. According to GAYE - SIESSEGGER et al. 2004, argues that the decrease in δ 13 C values occurs due to the use of lipid reserves to supply energy during fasting or starvation. These lizards during the seasonal dormancy process show a 60-90% reduction in their basal metabolic rate (SANDERS et al. 2015), and in view of that, lipids may have been used in energy production to supply prolonged fasting, however, not enough for the method used in the experiment to have detected this consumption. On the other hand, the 13 C that generated the enrichment may have originated from the mobilization of endogenous amino acids in energy production. Therefore, it seems to be advantageous for Salvator merianae to use the minimum of the lipid reserve in the production of energy in the face of an exceptionally low metabolic rate. Preserving in this way, the remaining lipids for allocation in the reproduction that occurs right after the period in which they arouse, even because when they emerge from their dens, they resume their food and, in this way, they can repair the organism. Tegus adult presented two δ 13 C of red cells according to their Exponential and Boltzmann curves, being 1.54 ‰ and 2.45 ‰ respectively. The same occurred with the δ 13 C of juvenile red cells pointing to the values 0.82 ‰ and 1.82 ‰. However, the δ 15 N values of the adult and juvenile red cells was related to only one Exponential fit curve and the values were 3.71 ‰ and 2.73 ‰. However, the δ 13 C of the adult plasm was 2.58 ‰ and the juveniles exposed two δ 13 C of the plasm, the values being 2.33 ‰ for the Exponential adjustment and 2.16 ‰ for the Boltzmann adjustment. On the other hand, δ 15 N was not calculated because its adjustment curve is a Bézier curve. In the remainder, no pattern was found in the discrimination factor values for both carbon and nitrogen in the literary taxa. The variability in the carbon and nitrogen discrimination factor in taxa has been reported previously and may vary by δ 13 C ‰ (-0.4 - 7.9 ‰) and δ 15 N ‰ (-0.1 - 4 ‰) (CAUT et al. 2009). Therefore, this variability occurs because the isotopic discrimination factor from the diet to the tissue may be linked to the biological processes associated with chemical and physical discrimination. And not with age, quality and proportion of diet, omnivore, herbivore and carnivore, tissue types, growth, temperature and protein turnover rates (CAUT et al. 2008; VANDERKLIFT & PONSARD 2003; WARNE et al. 2010). To PhD. Augusto Shinya Abe for the collaboration of his fundamental knowledge and the provision of animals for the experimental development. Literature Cited Abe A.S. 1983. Observations on dormancy in tegu lizards – Tupinambis teguixim (Reptilia, Teiidae). 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J Exp Biol 207:307-318. Stenvinkel P. et al. 2013. Metabolic changes in summer active and anuria hibernation free-ranging brown bears ( Ursus arctos ) . PloS one 8(9): e72934. Doi: https://doi.org/10.1371/journal.pone.0072934. Tattersall G.J., C.A.C. Leite, C.E. Sanders, V. Cadena, D.V. Andrade, A.S. Abe and W.K. Milson. 2016. Seasonal reproductive endothermy in tegu lizards. Sci Adv 2: e1500951. Tieszen L.L., T.W. Boutton, K.G. Tesdahl and N.A. Slade. 1983. Fractionation and turnover of stable carbono isotopes in animal tissues: Implications for δ¹³C analyses of diet. Oecologia 57: 32-37. Vanderklift M.A. and S. Ponsard. 2003. Sources of variation in consumer-diet δ 15 N enrichment: a meta-analysis. Oecologia 136: 169-182. Warne R.W., C.A. Gilman, B.O. Wolf. 2010. Tissue – incorporation rates in lizard: implications for ecological studies using stable isotopes in terrestrial ectotherms. Physiol Biochem Zool 83(4):608-617. Table 1. Mean values and standard deviation total length of adults (n = 8) Salvator merianae during the annual seasonal cycle. Total length (cm) Days N Mean SD PD1 8 117.38 8.47 0 8 117.13 9.88 45 8 117.25 8.63 105 8 117.63 9.26 195 8 116.63 9.24 PD2 8 117.38 8.37 A 8 117.38 8.81 1 PD1 – Pre-dormancy (April 2016) 2 PD2 = 225 days – Pre-dormancy (April 2017) 3 A = 345 days – Arouse (end of August - beginning of September 2017) Table 2. Mean values and standard deviation body mass of adults (n = 8) Salvator merianae during the annual seasonal cycle. Body mass (g) Days N Mean SD PD1 8 2781.00 764.97 0 8 2620.63 715.86 15 8 2689.63 692.37 30 8 2582,13 637.49 45 8 2453.63 672.99 60 8 2331.00 667.94 75 8 2554.50 770.32 105 8 2950.25 697.41 135 8 2853.63 827.05 165 8 2905.25 814.05 195 8 2867.88 801.44 PD2 8 2826.88 789.88 A 8 2677.50 783.49 1 PD1 – Pre-dormancy (April 2016) 2 PD2 = 225 days – Pre-dormancy (April 2017) 3 A = 345 days – Arouse (end of August - beginning of September 2017) Table 3. Mean values and standard deviation of the total length of juveniles of Salvator merianae (n = 8) during the annual seasonal cycle. Total length (cm) Days N Mean SD PD1 8 82.11 7.80 0 8 84.67 7.90 30 8 83.44 12.01 45 8 84.56 10.19 75 8 85.56 9.02 105 8 86.78 10.48 135 8 89,78 9.99 165 8 90,78 10,12 195 8 89,88 10,80 PD2 8 90,67 10,23 A 8 90.00 10.27 1 PD1 – Pre-dormancy (April 2016) 2 PD2 = 225 days – Pre-dormancy (April 2017) 3 A = 345 days – Arouse (end of August - beginning of September 2017) Table 4. Mean values and standard deviation of the body mass of juveniles of Salvator merianae (n = 8) during the annual seasonal cycle. Body mass (g) Days N Mean SD PD1 8 949.44ª 322.67 0 8 822.89ª 297.90 15 8 827.33ª 290.19 30 8 834.56 a 310.85 45 8 833.22ª 299.28 60 8 807.11ª 294.08 75 8 1016.67ª 376.54 105 8 1138.33ª 372.60 135 8 1337.44 b 417.27 165 8 1311.11 b 449.34 195 8 1389.56 b 486.43 PD2 8 1410.78 b 481.76 A 8 1311.44 b 479.37 1 PD1 – Pre-dormancy (April 2016) 2 PD2 = 225 days – Pre-dormancy (April 2017) 3 A = 345 days – Arouse (end of August - beginning of September 2017) 4 Line values accompanied by the same letter, do not differ by Fisher test (p <0.05). Table 5. Mean values and standard deviation of carbon and nitrogen of adults red cells and plasm (n = 8) of Salvator merianae during the annual seasonal cycle. Days N Mean SD Days N Mean SD 0 8 -18.20 a 0.54 0 8 4.98 a 0.43 15 8 -19.14 a 0.62 15 8 4.64 a 0.55 30 8 -19.19 a 0.49 30 8 4.42 a 0.48 45 8 -19.12 a 0.68 45 8 4.36 a 0.36 60 8 -19.55 b 0.63 60 8 4.48 a 0.53 75 8 -20.06 b 0.96 75 8 4.09 b 0.58 105 8 -21.13 b 0.86 105 8 4.00 b 0.74 135 8 -20.99 b 1.11 135 8 3.78 b 0.56 165 8 -21.23 b 0.92 165 8 3.82 b 0.54 195 8 -21.31 b 0.78 195 8 3.87 b 0.47 PD2 8 -21.13 b 0.77 PD2 8 3.79 b 0.55 A 8 -21.01 b 0.78 A 8 4.02 b 0.44 Plasm δ 13 C Plasm δ 15 N Days N Mean SD Days N Mean SD 0 8 -17.81 a 0.44 0 8 5.92 a 0.41 15 8 -19.05 b 0.91 15 8 5.35 a 0.48 30 8 -19.21 b 0.61 30 8 5.16 b 0.56 45 8 -19.21 b 0.68 45 8 5.07 b 0.69 60 8 -19.66 b 0.77 60 8 5.17 b 0.72 75 8 -20.65 b 0.42 75 8 4.55 b 0.36 105 8 -20.91 b 0.76 105 8 4.37 b 0.17 135 8 -21.10 b 0.31 135 8 4.45 b 0.30 165 8 -21.07 b 0.35 165 8 4.61 b 0.24 195 8 -20.93 b 0.28 195 8 4.80 b 0.24 PD2 8 -20.81 b 0.24 PD2 8 4.96 b 0.20 A 8 -20.43 b 0.28 A 8 5.21 a 0.35 1 PD2 = 225 days – Pre-dormancy (April 2017) 2 A = 345 days – Arousal (end of August - beginning of September 2017) 3 Values in the line accompanied by the same letter do not differ by Tukey test (p <0.05) Table 6. Equation of turnover rates, calculated values of half-lives (days), 99% of carbon and nitrogen substituted (days) and isotopic discrimination factor (‰) between the tissue and diet of carbon and nitrogen of red cells and plasma of Salvator merianae adults. Exponencial model Red cells and plasm δ 13 C(t) = -22.02348 +4.02535 e -0.01524t δ 13 C (t) = -20.973323+ 3.34391 e -0.03054t δ 15 N(t) = 3.41972 + 1.04822e – 0.01696 Boltzmann sigmoidal model Red cells \(13C(t)=\ -21.77521+\frac{19.10738}{{1+e\text{\ \ }}^{\frac{t-75.43659}{18.89837}\text{\ \ }}}\) —— Bézier model Plasm ——- δ 15 N(t) = 5.85171 + [-0.03686t + 2.37048E-4t 2 + (-3.96799E-7t 3 )] Red cells δ 13 C Exponencial model (n=4) Red cells δ 13 C Boltzmann model (n=4) Red cells δ 15 N Exponencial model (n=8) Plasm δ 13 C Exponencial model (n=8) Plasm δ 15 N Bézier model (n=8) Half-life (days) 45 75 41 23 —— Red cells δ 13 C Exponencial model Red cells δ 13 C Boltzmann model Red cells δ 15 N Exponencial model Plasm δ 13 C Exponencial model Plasm δ 15 N Bézier model 99% of carbon and nitrogen substituted (days) 315 525 286 159 —— Red cells δ 13 C Exponencial model Red cells δ 13 C Boltzmann model Red cells δ 15 N Exponencial model Plasm δ 13 C Exponencial model Plasm ⊗ 15 N Bézier model Isotopic discrimination factor (‰) 1.54 2.45 3.71 2.58 —— * Δ = δ tissue – δ diet Table 7. Mean values and standard deviation of carbon and nitrogen of juveniles red cells and plasm (n = 8) of Salvator merianae during the annual seasonal cycle. Days N Mean SD Days N Mean SD 0 8 -18.61 a 0.18 0 8 4.09 a 0.22 15 8 -18.85 a 0.29 15 8 3.84 a 0.14 30 8 -18.97 a 0.39 30 8 3.81 a 0.26 45 8 -19.25 a 0.75 45 8 3.68 b 0.34 60 8 -19.31 a 0.83 60 8 3.87 b 0.41 75 8 -20.02 b 0.89 75 8 3.50 b 0.47 105 8 -20.05 b 0.68 105 8 3.44 b 0.33 135 8 -20.95 b 0.57 135 8 3.22 b 0.29 165 8 -21.28 b 0.45 165 8 3.36 b 0.24 195 8 -21.45 b 0.37 195 8 3.33 b 0.21 PD2 8 -21.49 b 0.42 PD2 8 3.59 b 0.21 A 8 0.46 A 8 3.42 b 0.20 Plasm δ 13 C Plasm δ 15 N Days N Mean SD Days N Mean SD 0 8 -17.66 a 0.18 0 8 5.46 a 0.25 15 8 -18.31 a 0.69 15 8 4.92 a 0.44 30 8 -18.78 a 1.11 30 8 4.73 a 0.80 45 8 -19.26 b 1.12 45 8 4.49 a 0.62 60 8 -19.20 b 1.45 60 8 4.77 a 0.78 75 8 -20.51 b 1.29 75 8 4.17 b 0.79 105 8 -20.80 b 0.57 105 8 4.05 b 0.18 135 8 -20.77 b 0.42 135 8 4.00 b 0.22 165 8 -20.77 b 0.49 165 8 4.33 b 0.30 195 8 -20.90 b 0.40 195 8 4.27 b 0.29 PD2 8 -20.84 b 0.35 PD2 8 4.67 a 0.15 A 8 -20.54 b 0.33 A 8 4.99 a 0.24 1 PD2 = 225 days – Pre-dormancy (April 2017) 2 A = 345 days – Arousal (end of August - beginning of September 2017) 3 Values in the line accompanied by the same letter do not differ by Tukey test (p <0.05) Table 8. Equation of turnover rates, calculated values of half-lives (days), 99% of carbon and nitrogen substituted (days) and isotopic discrimination factor (‰) between the tissue and diet of carbon and nitrogen of red cells and plasma of Salvator merianae juveniles. Exponencial model Red cells Plasm δ 13 C(t) = -22.1933 + 3.92537 e -0.01219t δ 13 C (t) = -20.67936+ 3.17972 e -0.03441t δ 15 N(t) = 3.41972 + 1.04822e – 0.01696 —— Boltzmann sigmoidal model Red cells Plasm \[13C(t)=\ -21.36865+\frac{18.54835}{{1+e\text{\ \ }}^{\frac{t-77.87546}{19.11738}\text{\ \ }}}\] \[13C(t)=\ -20,84593+\frac{17.57317}{{1+e\text{\ \ }}^{\frac{t-55.31362}{14.40905}\text{\ \ }}}\] —— —— Bézier model Plasm ——- δ 15 N(t) = 5.46451 + [-0.02313t + 1.16952-4t 2 + (-1.58863E-7t 3 )] Red cells δ 13 C Exponencial model (n=3) Red cells δ 13 C Boltzmann model (n=5) Red Cells δ 15 N Exponencial model (n=8) Plasm δ 13 C Exponencial model (n=4) Plasm δ 13 C Boltzmann model (n=4) Plasm δ 15 N Bézier model (n=8) Half-life days 57 78 22 20 55 —— Red cells δ 13 C Exponencial model (n=3) Red cells δ 13 C Boltzmann model (n=5) Red Cells δ 15 N Exponencial model (n=8) Plasm δ 13 C Exponencial model (n=4) Plasm δ 13 C Boltzmann model (n=4) Plasm δ 15 N Bézier model (n=8) 99% of carbon and nitrogen substituted (days) 398 546 140 151 385 —— Red cells δ 13 C Exponencial model (n=3) Red cells δ 13 C Boltzmann model (n=5) Red Cells δ 15 N Exponencial model (n=8) Plasm δ 13 C Exponencial model (n=4) Plasm δ 13 C Boltzmann model (n=4) Plasm δ 15 N Bézier model (n=8) Isotopic discrimination factor (‰) 0.82 1.82 2.73 2.33 2.16 ——- * Δ = δ tissue – δ diet Table 9. Mean and standard deviation of δ 13 C ‰ from red cells and plasm from adults and juveniles. PD -21.13 ± 0.77 -20.80 ± 0.24 -21.49 ± 0.42 -20.84 ± 0.35 A -21.01 ± 0.78 -20.43 ± 0.28 -21.53 ± 0.46 -20.54 ± 0.33 1 PD = 225 days – Pre-dormancy (April 2017) 2 A = 345 days – Arousal (end of August - beginning of September 2017) Figure Captions Figure 1. Mean values and standard deviation of body mass and total length of Salvator merianae adults during the anual seasonal cycle. Figure 2. Mean values and standard deviation of body mass and total length of Salvator merianae juveniles during the anual seasonal cycle. Figure 3. Turnover rate curve of 13 C with the exponential model of the red cells of adult individuals (n = 4) of Salvator merianae. Figure 4. Turnover rate curve of 13 C with the Boltzmann sigmoidal model of the red cells of adult individuals (n = 4) from Salvator merianae. Figure 5. Turnover rate curve of ¹⁵N with the exponential model of the red cells of adult individuals (n = 8) of Salvator merianae. Figure 6. Turnover rate curve of 13 C with the exponential model of the plasm of adult individuals (n = 8) of Salvator merianae. Figure 7. (A)Turnover rate curve of ¹⁵N with the Bézier model of the plasm of adult individuals (n = 8) of Salvator merianae ; (B) Bézier curve with the activity, pre-dormancy and arousing phases. Figure 8. Turnover rate curve of 13 C with the exponential model of the red cells of juveniles individuals (n = 3) of Salvator merianae. Figure 9. Turnover rate curve of 13 C with the Boltzmann sigmoidal model of the red cells of juveniles individuals (n = 5) from Salvator merianae. Figure 10. Turnover rate curve of ¹⁵N with the exponential model of the red cells of juveniles individuals (n = 8) of Salvator merianae. Figure 11. Turnover rate curve of ¹³C with the exponential model of the plasm of juveniles individuals (n = 4) of Salvator merianae. Figure 12. Turnover rate curve of 13 C with the Boltzmann sigmoidal model of the plasm of juveniles individuals (n = 4) from Salvator merianae. Figure 13. (A) Turnover rate curve of ¹⁵N with the Bézier model of the plasm of juveniles individuals (n = 8) of Salvator merianae ; (B) Bézier curve with the activity, pre-dormancy and arousing phases. Figure 14. Box - plot of comparisons of stable carbon isotopes in red cells and plasma of adult individuals (N = 8) of Salvator merianae . The data is shown as boxes; The lower and upper ends of the box indicate the 25% and 75% percentiles; The central line is the median; Whiskers indicate the full range of the data; Black dots indicate individual data points. PD - Pre-dormancy and A – arousing. Figure 15. Box - plot of comparisons of stable carbon isotopes in red cells and plasma of juveniles individuals (N = 8) of Salvator merianae . The data is shown as boxes; The lower and upper ends of the box indicate the 25% and 75% percentiles; The central line is the median; Whiskers indicate the full range of the data; Black dots indicate individual data points. PD - Pre-dormancy and A – arousing. Figure 1. Figure 2. Figure 3. Figure 4. Figure 5. Figure 6. Figure 7. Figure 8. Figure 9. Figure 10. Figure 11. Figure 12. Figure 13. Figure 14. Figure 15. Information & Authors Information Version history V1 Version 1 05 June 2025 Copyright This work is licensed under a Non Exclusive No Reuse License. Keywords dormancy facultative endothermy isotopic discrimination factors lizards metabolic adaptation Authors Affiliations Luciana M. Beloto Universidade de Sao Paulo Centro de Energia Nuclear na Agricultura View all articles by this author Marina Sartori Universidade Estadual de Campinas Faculdade de Ciencias Medicas View all articles by this author Thiago S. Marques Universidade de Sorocaba View all articles by this author Augusto Shinya Abe Universidade Estadual Paulista Julio de Mesquita Filho - Campus de Rio Claro View all articles by this author Barbara Protocevich 0009-0007-7350-4831 [email protected] Universidade de Sorocaba View all articles by this author Ronnie Von M. Ferreira Universidade de Sorocaba View all articles by this author Marcelo Moreira 0000-0001-6769-5570 Universidade de Sao Paulo Centro de Energia Nuclear na Agricultura View all articles by this author P Camargo Universidade de Sao Paulo Centro de Energia Nuclear na Agricultura View all articles by this author Metrics & Citations Metrics Article Usage 195 views 123 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Luciana M. Beloto, Marina Sartori, Thiago S. Marques, et al. Effect of seasonal dormancy on turnover rate and isotopic discrimination factor in Salvator merianae (Tegu lizard). Authorea . 05 June 2025. DOI: https://doi.org/10.22541/au.174911956.64150159/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download. 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