Abstract
Body maintenance costs are often considered a proxy for performance in fitness traits. Maintenance energy requirements are measured as minimal metabolic rate of inactive, postabsorptive individuals in the laboratory. For mountain-dwelling species, translocation to the laboratory often means that they are also moved to another elevation. Due to physiological adaptations to local oxygen pressure, rapid elevational change can alter metabolic rate and translocation may result in erroneous estimates of body maintenance costs. In this study, we measured resting metabolic rate (RMR) of three populations of the Mesquite lizard (Sceloporus grammicus, Wiegmann 1828) at their native elevations (i.e., 2600, 3200 and 4100 m). Our results showed that at native elevations, mass specific RMR of lizards from the high elevation population (4100 m) did not differ from the RMR of the other populations (i.e., 2600 and 3200 m), whereas the lizards from the low elevation (2600 m) had lower RMR than those from the intermediate population. These results differ from a previous study in which the RMR of lizards from the same populations were reported to increase with native elevation when translocated and measured at an intermediate elevation. Hence, our results show that translocation in elevation can affect metabolic measures. We caution researchers that changes in elevation may preclude accurate measures of RMR in some animals and may therefore incorrectly predict performance of fitness-related traits.
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References
Angilletta MJ Jr (2001) Variation in metabolic rate between populations of a geographically widespread lizard. Physiol Biochem Zool 74:11–21. https://doi.org/10.1086/319312
Barrios-Montiel R (2018) Implicaciones ecofisiológicas del gradiente altitudinal en Sceloporus grammicus. Master thesis, Universidad Autónoma de Tlaxcala
Bastiaans E, Morinaga G, Castañeda Gaytán JG, Marshall JC, Sinervo B (2013) Male aggression varies with throat color in 2 distinct populations of the mesquite lizard. Behav Ecol 24:968–981. https://doi.org/10.1093/beheco/art010
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Berg W, Theisinger O, Dausmann KH (2017) Acclimatization patterns in tropical reptiles: uncoupling temperature and energetics. Sci Nat 104:91. https://doi.org/10.1007/s00114-017-1506-0
Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659. https://doi.org/10.1016/j.tree.2010.08.003
Bodensteiner BL, Gangloff EJ, Kouyoumdjian L, Muñoz MM, Aubret F (2021) Thermal-metabolic phenotypes of the lizard Podarcis muralis differ across elevation, but converge in high-elevation hypoxia. J Exp Biol 224:jeb243660. https://doi.org/10.1242/jeb.243660
Burton T, Killen SS, Armstrong JD, Metcalfe NB (2011) What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc R Soc B 278:3465–3473. https://doi.org/10.1098/rspb.2011.1778
Callier V, Nijhout HF (2011) Control of body size by oxygen supply reveals size-dependent and size-independent mechanisms of molting and metamorphosis. Proc Natl Acad Sci USA 108:14664–14669. https://doi.org/10.1073/pnas.1106556108
Chabot D, Dutil JD (1999) Reduced growth of Atlantic cod in non-lethal hypoxic conditions. Fish Biol 55:472–491. https://doi.org/10.1111/j.1095-8649.1999.tb00693.x
Díaz de la Vega-Pérez AH, Barrios-Montiel R, Jiménez-Arcos VH, Bautista A, Bastiaans E (2019) High-mountain altitudinal gradient influences thermal ecology of the Mesquite lizard Sceloporus grammicus. Can J Zool 97:659–668. https://doi.org/10.1139/cjz-2018-0263
Domínguez-Godoy MA, Hudson R, Pérez-Mendoza HA, Ancona S, Díaz de la Vega-Pérez AH (2020a) Living on the edge: lower thermal quality but greater survival probability at a high altitude mountain for the mesquite lizard (Sceloporus grammicus). J Therm Biol 94:102757. https://doi.org/10.1016/j.jtherbio.2020.102757
Domínguez-Godoy MA, Gómez-Campos JE, Hudson R, Díaz de la Vega-Pérez AH (2020b) Lower predation with increasing altitude in the mesquite lizard Sceloporus grammicus. West N Am Naturalist 80:441–451. https://doi.org/10.3398/064.080.0401
Domínguez-Godoy MA, Hudson R, Montoya B, Bastiaans E, Díaz de la Vega-Pérez AH (2022) Too cool to fight: Is ambient temperature associated with male aggressive behavior in the mesquite lizard? J Zool. https://doi.org/10.1111/jzo.12979
Dzal YA, Jenkin SEM, Lague SL, Reichert MN, York JM, Pamenter ME (2015) Oxygen in demand: how oxygen has shaped vertebrate physiology. Comp Biochem Phys A 186:4–26. https://doi.org/10.1016/j.cbpa.2014.10.029
Espinoza RE, Wiens JJ, Tracy CR (2004) Recurrent evolution of herbivory in small, cold-climate lizards: breaking the ecophysiological rules of reptilian herbivory. Proc Natl Acad Sci 101:16819–16824. https://doi.org/10.1073/pnas.0401226101
Frazier MR, Woods HA, Harrison JF (2001) Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster. Physiol Biochem Zool 74:641–650. https://doi.org/10.1086/322172
Friesen CR, Powers DR, Mason RT (2017) Using whole-group metabolic rate and behaviour to assess the energetics of courtship in red-sider garter snakes. Anim Behav 130:177–185. https://doi.org/10.1016/j.anbehav.2017.06.020
Gangloff EJ, Telemeco RS (2018) High temperature, oxygen, and performance: Insights from reptiles and amphibians. Integr Comp Biol 58:9–24. https://doi.org/10.1093/icb/icy005
Gangloff EJ, Sorlin M, Cordero GA, Souchet J, Aubret F (2019) Lizards at the peak: physiological plasticity does not maintain performance in lizards transplanted to high altitude. Physiol Biochem Zool 92:189–200. https://doi.org/10.1086/701793
González-Morales JC, Quintana E, Díaz-Albiter H, Guevara-Fiore P, Fajardo V (2015) Is the erythrocyte size a strategy to avoid hypoxia in Wiegmann’s torquate lizards (Sceloporus torquatus) field evidence? Can J Zool 93:377–382. https://doi.org/10.1139/cjz-2014-0265
González-Morales JC, Beamonte-Barrientos R, Bastiaans E, Guevara-Fiore P, Quintana E, Fajardo V (2017) A mountain or a plateau? Hematological traits very nonlinearly with altitude in a highland lizard. Physiol Biochem Zool 90:638–645. https://doi.org/10.1086/694833
Hammond KA, Roth J, Janes DN, Dohm MR (1999) Morphological and physiological responses to altitude in deer mice Peromyscus maniculatus. Physiol Biochem Zool 75:613–622. https://doi.org/10.1086/316697
He J, Minghui X, Tang X, Yue F, Wang N, Yang S, Chen Q (2013) The different mechanisms of hypoxic acclimatization and adaptation in lizard Phrynocephalus vlangalii living on Qinghai-Tibet Plateau. J Exp Zool 319A:117–123. https://doi.org/10.1002/jez.1776
Horiuchi M, Fukuoka Y, Handa Y, Abe D, Pontzer H (2017) Measuring the energy of ventilation and circulation during human walking using induced hypoxia. Sci Rep 7:4938. https://doi.org/10.1038/s41598-017-05068-8
Horne CR, Hirst AG, Atkinson D (2017) Insect temperature–body size trends common to laboratory, latitudinal and seasonal gradients are not found across altitudes. Funct Ecol 32:948–957. https://doi.org/10.1111/1365-2435.13031
Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends Ecol Evol 4:131–135. https://doi.org/10.1016/0169-5347(89)90211-5
Hughes JL, Fitzpatrick LC, Ferguson W, Beitinger TL (1982) Oxygen consumption and temperature acclimation in the northern prairie swift Sceloporus undulatus garmani from Kansas. Comp Biochem Physiol A 71:611–613. https://doi.org/10.1016/0300-9629(82)90211-0
Ivy CM, Scott GR (2017) Control of breathing and ventilatory acclimation to hypoxia in deer mice native to high altitudes. Acta Physiol 221:266–282. https://doi.org/10.1111/apha.12912
Jiménez-Cruz E, Ramírez-Bautista A, Marshall JC, Lizana-Avia M, Nieto-Montes de Oca A (2005) Reproductive cycle of Sceloporus grammicus (Squamata: Phrynosomatidae) from Teotihuacán, México. Southwest Nat 50:178–187. https://doi.org/10.1894/0038-4909(2005)050[0178:RCOSGS]2.0.CO;2
Jin Y, Liu N, Li J (2007) Elevational variation in body size of Phrynocephalus vlangalii in the North Qinghai-Xizang (Tibetan) Plateau. Belg J Zool 137:197–202
Killen SS, Glazier DS, Rezende EL, Clark TD, Atkinson D, Willener AST, Halsey LG (2016) Ecological influences and morphological correlates of resting and maximal metabolic rates across teleost fish species. Am Nat 187:592–606. https://doi.org/10.1086/685893
Kouyoumdjian L, Gangloff EJ, Souchet J, Cordero GA, Dupoué A, Aubret F (2019) Transplanting gravid lizards to high elevation alters maternal and embryonic oxygen physiology, but not reproductive success or hatchling phenotype. J Exp Biol 222:jeb206839. https://doi.org/10.1242/jeb.206839
Kozłowski J, Konarzeweski M, Czarnoleski M (2020) Coevolution of body size and metabolic rate in vertebrates: a life-history perspective. Biol Rev 95:1393–1417. https://doi.org/10.1111/brv.12615
Krogh A (1916) The respiratory exchange of animals and man. Longmans, Green & Co, London
Lardies MA, Catalán TP, Bozinovic F (2004) Metabolism and life-history correlates in a lowland and highland population of a terrestrial isopod. Can J Zool 82:677–687. https://doi.org/10.1139/z04-033
Lemos-Espinal JA, Ballinger RE (1995) Ecology of growth of the high altitude lizard Sceloporus grammicus on the eastern slope of Iztaccihuatl volcano, Puebla, México. Trans Nebraska Acad Sci 22:77–85
Lemos-Espinal JA, Ballinger RE, Smith GR (1998) Comparative demography of the high-altitude lizard, Sceloporus grammicus (Phrynosomatidae), on the Iztaccihuatl Volcano, Puebla, México. Great Basin Nat 58:375–379. https://doi.org/10.1139/z95-258
Lenth R (2018) Emmeans: estimated marginal means, aka least-squares means. R package version 1.4.2. https://doi.org/10.1080/00031305.1980.10483031
Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University Press, Oxford
Lind CM, Agugliaro J, Farrell TM (2020) The metabolic response to an immune challenge in a viviparous snake, Sistrutus muliarius. J Exp Biol 223:jeb225185. https://doi.org/10.1242/jeb.225185
Lui M, Mahalingam S, Patel P, Connaty AD, Ivy CM, Cheviron ZA, Storz JF, McClelland GB, Scott GR (2015) High-altitude ancestry and hypoxia acclimation have distinct effects on exercise capacity and muscle phenotype in deer mice. Am J Physiol Reg Intgr Comp Physiol 308:R779–R791. https://doi.org/10.1152/ajpregu.00362.2014
Massot M, Clobert J, Montes-Polini L, Haussy C, Cubo J, Meylan S (2011) An integrative study of ageing in a wild population of common lizards. Funct Ecol 25:848–858. https://doi.org/10.1111/j.1365-2435.2011.01837.x
Mathot KJ, Dingemanse NJ, Nakagawa S (2019) The covariance between metabolic rate and behaviour varies across behaviours and thermal types: meta-analytic insights. Bio Rev 94:1056–1074. https://doi.org/10.1111/brv.12491
McArley TJ, Hickley AJR, Herbert NA (2018) Hyperoxia increases maximum oxygen consumption and aerobic scope of intertidal fish facing acutely high temperatures. J Exp Biol 221:jeb189993. https://doi.org/10.1111/jbi.12365
McArley TJ, Sandblom E, Herbert NA (2021) Fish and hyperoxia—from cardiorespiratory and biochemical adjustments to aquaculture and ecophysiology implications. Fish Fish 22:324–355. https://doi.org/10.1111/faf.12522
Montoya-Ciriaco N, Gómez-Acata S, Muñoz-Arenas LC, Dendooven L, Estrada-Torres A, Díaz de la Vega-Pérez AH, Navarro-Noya YE (2020) Dietary effects on gut microbiota of the mesquite lizard Sceloporus grammicus (Wiegmann, 1828) across different altitudes. Microbiome 8:6. https://doi.org/10.1186/s40168-020-0783-6
Müller J, Bässler C, Essbauer S, Schex S, Müller DWH, Opgenoorth L, Brandl R (2014) Relative heart size in two rodent species increases with elevation: reviving Hesse’s rule. J Biogeogr 41:2211–2220. https://doi.org/10.1111/jbi.12365
Norin T, Malte H, Clark TD (2016) Differential plasticity of metabolic rate phenotypes in a tropical fish facing environmental change. Funct Ecol 30:369–378. https://doi.org/10.1111/1365-2435.12503
Patterson JW (1984) Thermal acclimation in two subspecies of the tropical lizard Mabuya striata. Physiol Zool 57:301–306. https://doi.org/10.1086/physzool.57.3.30163718
Peacock AJ (1998) Oxygen at high altitude. BMJ-Brit Med J 317:1063–1066. https://doi.org/10.1136/bmj.317.7165.1063
Plasman M, Bautista A, McCue MD, Díaz de la Vega-Pérez AH (2020) Resting metabolic rates increase with elevation in a mountain-dwelling lizard. Integr Zool 15:363–374. https://doi.org/10.1111/1749-4877.12434
Polymeropoulos ET, Elliott NG, Frappell PB (2019) Acute but not chronic hyperoxia increases metabolic rate without altering the cardiorespiratory response in Atlantic salmon alevins. Aquaculture 502:189–195. https://doi.org/10.1016/j.aquaculture.2018.12.041
Porteus C, Hedrick MS, Hicks JW, Wang T, Milsom WK (2011) Time domains of the hypoxic ventilatory response in ectothermic vertebrates. J Comp Physiol B 181:311–333. https://doi.org/10.1007/s00360-011-0554-6
Pörtner HO, Van Dijk PLM, Hardewig I, Sommer A (2000) Levels of metabolic cold adaptation: Trade-offs in Eurythermal and Stenothermal ecotherms. In: Davison W, Howard-Williams C, Broady P (eds) Antarctic ecosystems: models for wider ecological understanding. Caxton Press, Christchurch, pp 109–122
Powell FL, Milsom WK, Mitchell GS (1998) Time domains of the hypoxic ventilatory response. Resp Physiol 112:123–134. https://doi.org/10.1002/cphy.c150026
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org
Ramirez JM, Folkow LP, Blix AS (2007) Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Annu Rev Physiol 69:113–143. https://doi.org/10.1146/annurev.physiol.69.031905.163111
Rao KP, Bullock TH (1954) Q10 as a function of size and habitat temperature in poikilotherms. Am Nat 88:33–44. https://doi.org/10.1086/281806
Riemer K, Anderson-Teixeira KJ, Smith FA, Harris DJ, Morgan Ernest SK (2018) Body size shifts influence effects of increasing temperatures on ectotherm metabolism. Global Ecol Biogeogr 27:958–967. https://doi.org/10.1111/geb.12757
Ríos-Rodas L, Rodríguez-Romero FDJ, Velázquez-Rodríguez AS, Hernández-Franyutti AA (2013) Morfometría geométrica del corazón de Hyla plicata a través de un gradiente altitudinal en el eje Neovolcánico Mexicano. Int J Morphol 31:905–910. https://doi.org/10.4067/S0717-95022013000300021
Roe JH, Hopkins WA, Talent LG (2005) Effect of body mass, feeding, and circadian cycles on metabolism in the lizard Sceloporus occidentalis. J Herp 39:595–603. https://doi.org/10.1670/75-05A.1
Rubalcaba JG, Verberk WCEP, Hendriks AJ, Saris B, Woods HA (2020) Oxygen limitation may affect the temperature and size dependence of metabolic metabolism in aquatic ectotherms. Proc Natl Acad Sci USA 117:31963–31968. https://doi.org/10.1073/pnas.2003292117
Schaefer J, Walters A (2010) Metabolic cold adaptation and developmental plasticity in metabolic rates among species in the Fundulus notatus species complex. Funct Ecol 24:1087–1094. https://doi.org/10.1111/j.1365-2435.2010.01726.x
Sears MW (2005) Resting metabolic expenditure as a potential source of variation in growth rates of the sagebrush lizard. Comp Biochem Physiol A 140:171–177. https://doi.org/10.1016/j.cbpb.2004.12.003
Shik JZ, Arnan X, Sanchez Oms C, Cerdá X, Boulay R (2018) Evidence for locally adaptive metabolic rates among ant populations along an elevational gradient. J Anim Ecol 88:1240–1249. https://doi.org/10.1111/1365-2656.13007
Sites JW, Archie JW, Cole CJ, Flores-Villela O (1992) A review of phylogenetic hypotheses for lizards of the genus Sceloporus (Phrynosomatidae): implications for ecological and evolutionary studies. Bull Am Mus Nat Hist 213:1–110
Snyder GK, Weathers WW (1977) Activity and oxygen consumption during hypoxic exposure in high altitude and lowland Sceloporine lizards. J Comp Physiol 117:291–301. https://doi.org/10.1007/BF00691555
Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15. https://doi.org/10.1016/j.marenvres.2012.04.003
Storz JF, Scott GR (2019) Life ascending: mechanism and process in physiological adaptation to high-altitude hypoxia. Annu Rev Ecol Evol Syst 50:503–526. https://doi.org/10.1146/annurev-ecolsys-110218-025014
Storz JF, Scott GR, Cheviron ZA (2010) Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. J Exp Biol 213:4125–4136. https://doi.org/10.1242/jeb.048181
Tan S, Li P, Yao Z, Liu G, Yue B, Fu J, Chen J (2021) Metabolic cold adaptation in the Asiatic toad: intraspecific comparison along an altitudinal gradient. J Comp Physiol B 191:765–776. https://doi.org/10.1007/s00360-021-01381-x
Theisinger O, Berg W, Dausmann KH (2017) Compensation of thermal constraints along a natural environmental gradient in a Malagasy iguanid lizard (Oplurus quadrimaculatus). J Therm Biol 68:21–26. https://doi.org/10.1016/j.jtherbio.2017.01.005
Tsuji JS (1988) Seasonal profiles of standard metabolic rate of lizards Sceloporus occidentalis in relation to latitude. Physiol Zool 61:230–240. https://doi.org/10.1086/physzool.61.3.30161236
Wiegmann AFA (1828) Beyträge zur Amphibienkunde. Isis Von Oken 21:364–383
Williams CM, Szejner-Sigal A, Morgan TJ, Edison AS (2016) Adaptation to low temperature exposure increases metabolic rates independently of growth rates. Integr Comp Biol 56:62–72. https://doi.org/10.1093/icb/icw009
Žagar A, Carretero MA, Marguč D, Simčič T, Vrezec A (2018) A metabolic syndrome in terrestrial ectotherms with different elevational and distribution patterns. Ecography 41:1728–1739. https://doi.org/10.1111/ecog.03411
Zhang SY, Pamenter ME (2019) Ventilatory, metabolic, and thermoregulatory responses of Damaraland mole rats to acute and chronic hypoxia. J Comp Physiol B 189:319–334. https://doi.org/10.1007/s00360-019-01206-y
Zuur AF, Leno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgements
Funding for this study was provided by postdoctoral grant from Consejo Nacional de Ciencia y Tecnologia (MP) and the Catedras CONACyT program (ADP, 883). We thank the Secretaría de Medio Ambiente y Recursos Naturales for providing the collecting permits (SGPA/DGVS/007736/18). We thank Comisión Nacional de Áreas Naturales Protegidas for the facilities in the Protection Area of Flora and Fauna Nevado de Toluca and La Malinche National Park. We thank I. López for providing facilities in Apizaco. We also thank M. Martínez-Gómez for her valuable help with logistics and use of the field station at La Malinche facilities to conduct this research and V. H. Reynoso for lending equipment. We thank M. D. McCue for his valuable comments to an early version of the manuscript. Finally, we thank M. Domínguez-Godoy, R. Barrios-Montiel, R. López-Vivanco and E. Gómez-Campos for help in the field.
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Consejo Nacional de Ciencia y Tecnologia, a postdoctoral grant to MP and Catedras-CONACyT program to ADP (number: 883).
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Plasman, M., Bautista, A. & Díaz de la Vega-Pérez, A.H. Avoiding the effects of translocation on the estimates of the metabolic rates across an elevational gradient. J Comp Physiol B 192, 659–668 (2022). https://doi.org/10.1007/s00360-022-01448-3
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DOI: https://doi.org/10.1007/s00360-022-01448-3