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Physiological underpinnings associated with differences in pace of life and metabolic rate in north temperate and neotropical birds

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Abstract

Animal life-history traits fall within limited ecological space with animals that have high reproductive rates having short lives, a continuum referred to as a “slow-fast” life-history axis. Animals of the same body mass at the slow end of the life-history continuum are characterized by low annual reproductive output and low mortality rate, such as is found in many tropical birds, whereas at the fast end, rates of reproduction and mortality are high, as in temperate birds. These differences in life-history traits are thought to result from trade-offs between investment in reproduction or self-maintenance as mediated by the biotic and abiotic environment. Thus, tropical and temperate birds provide a unique system to examine physiological consequences of life-history trade-offs at opposing ends of the “pace of life” spectrum. We have explored the implications of these trade-offs at several levels of physiological organization including whole-animal, organ systems, and cells. Tropical birds tend to have higher survival, slower growth, lower rates of whole-animal basal metabolic rate and peak metabolic rate, and smaller metabolically active organs compared with temperate birds. At the cellular level, primary dermal fibroblasts from tropical birds tend to have lower cellular metabolic rates and appear to be more resistant to oxidative cell stress than those of temperate birds. However, at the subcellular level, lipid peroxidation rates, a measure of the ability of lipid molecules within the cell membranes to thwart the propagation of oxidative damage, appear not to be different between tropical and temperate species. Nevertheless, lipids in mitochondrial membranes of tropical birds tend to have increased concentrations of plasmalogens (phospholipids with antioxidant properties), and decreased concentrations of cardiolipin (a complex phospholipid in the electron transport chain) compared with temperate birds.

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References

  • Anderson KJ, Jetz W (2005) The broad-scale ecology of energy expenditure of endotherms. Ecol Lett 8:310–318

    Google Scholar 

  • Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Quart Rev Biol 72:149–177

    Google Scholar 

  • Austin SH, Robinson TR, Robinson WD, Ricklefs RE (2011) Potential biases in estimating the rate parameter of sigmoid growth functions. Methods Ecol Evol 2:43–51

    Google Scholar 

  • Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120:483–495

    CAS  PubMed  Google Scholar 

  • Barja G, Cadenas S, Rojas C, Perez-Campo R, Lopez-Torres M (1994) Low mitochondrial free radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high aerobic metabolic rate in birds. Free Radic Res 21:317–327

    CAS  PubMed  Google Scholar 

  • Bartholomew GA (1972) Body temperature and energy metabolism. In: Gordon M (ed) Animal physiology: principles and adaptations. MacMillan, New York, pp 63–72

    Google Scholar 

  • Bennett AF (1991) The evolution of activity capacity. J Exp Biol 160:1–23

    CAS  PubMed  Google Scholar 

  • Bennett PM, Harvey PH (1987) Active and resting metabolism in birds: allometry, phylogeny and ecology. J Zool Lond 213:327–363

    Google Scholar 

  • Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206:649–654

    CAS  PubMed  Google Scholar 

  • Blake JG, Loiselle BA (2008) Estimates of apparent survival rates for forest birds in eastern Ecuador. Biotropica 40:485–493

    Google Scholar 

  • Brand MD, Affourtit C, Esteves TC, Green K, Lambert AJ, Miwa S, Pakay JL et al (2004) Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Rad Biol Med 37:755–767

    CAS  PubMed  Google Scholar 

  • Braverman NE, Moser AB (2012) Functions of plasmalogen lipids in health and disease. Biochim Biophys Acta 1822:1442–1452

    CAS  PubMed  Google Scholar 

  • Brawn JD, Karr JR, Nichols JD, Robinson WD (1998) Demography of tropical forest birds in Panama: how do transients affect estimates of survival rates? In: Adams NJ, Slotow RH (eds) Proceedings 22nd International Ornithological Congress. BirdLife South Africa, Johannesburg, pp 297–305

  • Brawn JD, Karr JR, Nichols JD, Robinson WD (1999) Demography of forest birds in Panama: how do transients affect estimates of survival rates. In: Proceedings of the International Ornithological Congress vol. 22, pp 297–305

  • Brookes PS, Hulbert AJ, Brand MD (1997) The proton permeability of Liposomes made from mitochondrial inner membrane phospholipids: no effect of fatty acid composition. Bioch Biophys Acta/Biomemb 1330:157–164

    CAS  Google Scholar 

  • Brosche T, Platt D (1998) The biological significance of plasmalogens in defense against oxidative damage. Exp Gerontol 33:363–369

    CAS  PubMed  Google Scholar 

  • Brown MF, Gratton TP, Stuart J (2007) Metabolic rate does not scale with body mass in cultured mammalian cells. Am J Physiol Regul Integr Comp Physiol 292:R2115–R2121

    CAS  PubMed  Google Scholar 

  • Bryant DM (1997) Energy expenditure in wild birds. Proc Nutr Soc 56:1025–1039

    CAS  PubMed  Google Scholar 

  • Bryant DM, Hails CJ (1983) Energetics and growth patterns of three tropical bird species. Auk 400:425–439

    Google Scholar 

  • Brzek P, Bielawska K, Ksiazek A, Konarzewski M (2007) Anatomic and molecular correlates of divergent selection for basal metabolic rate in laboratory mice. Physiol Biochem Zool 80:491–499

    CAS  PubMed  Google Scholar 

  • Buttemer WA, Battam H, Hulbert AJ (2008) Fowl play and the price of petrel: long-living Procellariiformes have peroxidation-resistant membrane composition compared with short-living Galliformes. Biol Lett 4:351–354

    PubMed Central  PubMed  Google Scholar 

  • Calder WA (1984) Size, function, and life history. Harvard University Press, Cambridge

    Google Scholar 

  • Calhoon EA, Jimenez AG, Harper JM, Jurkowitz MS, and Williams JB (2014) Linkages between mitochondrial lipids and life-history in temperate and tropical birds. Physiol Biochem Zool 87. doi:10.1086/674696

  • Camfield AF, Pearson SF, Martin K (2010) Life history variation between high and low elevation subspecies of horned larks Eremophila spp. J Avian Biol 41:273–281

    Google Scholar 

  • Campisi J (2001) From cells to organisms: can we learn about aging from cells in culture? Exp geront 36:607–618

    CAS  Google Scholar 

  • Chapman LB (1955) Studies of a tree swallow colony (third paper). Bird-Banding 45–70

  • Chappell MA, Bech C, Buttemer WA (1999) The relationship of central and peripheral organ masses to aerobic performance variation in house sparrows. J Exp Biol 202:2269–2279

    PubMed  Google Scholar 

  • Chappell MA, Garland T, Robertson GF, Saltzman W (2007) Relationships among running performance, aerobic physiology and organ mass in male Mongolian gerbils. J Exp Biol 210:4179–4197

    PubMed  Google Scholar 

  • Charnov EL (1993) Life history invariants. Oxford University Press, Oxford

    Google Scholar 

  • Cheng YR, Martin TE (2012) Nest predation risk and growth strategies of passerine species: grow fast or develop traits to escape risk? Am Nat 180:285–295

    PubMed  Google Scholar 

  • Chicco AJ, Sparagna GC (2007) Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol 292:C33–C44

    CAS  PubMed  Google Scholar 

  • Cilimburg AB, Lindberg MS, Tewksbury JJ, Hejl SJ (2002) Effects of dispersal on survival probability of adult Yellow Warblers (Dendroica petechia). Auk 119:778–789

    Google Scholar 

  • Cohen AA, Mcgraw KJ, Wiersma P, Williams JB, Robinson WD, Robinson TD, Brown JD, Ricklefs RE (2008) Interspecific association between circulating antioxidant levels and life-history variation in birds. Am Nat 172:178–193

    PubMed  Google Scholar 

  • Constantini D, Verhulst S (2009) Does high antioxidant capacity indicate low oxidative stress? Funct Ecol 23:506–509

    Google Scholar 

  • Costantini D, Rowe M, Butler MW, McGraw KJ (2010) From molecules to living systems: historical and contemporary issues in oxidative stress and antioxidant ecology. Funct Ecol 24:950–959

    Google Scholar 

  • Couture P, Hulbert AJ (1995) Relationship between body mass, tissue metabolic rate, and sodium pump activity in mammalian liver and kidney. Am J Physiol 268:R641–R650

    CAS  PubMed  Google Scholar 

  • Cox WA, Martin TE (2009) Breeding biology of the three-striped warbler in Venezuela: a contrast between tropical and temperate parulids. Wilson J Ornithol 121:667–678

    Google Scholar 

  • Daan S, Masman D, Groenewold A (1990) Avian basal metabolic rates: their association with body composition and energy expenditure in nature. Am J Physiol 259:R333–R340

    CAS  PubMed  Google Scholar 

  • Daan S, Masman D, Strijkstra AM, Kenagy GJ (1991) Daily energy turnover during reproduction in birds and mammals: its relationship to basal metabolic rate. Acta XX Congr Int Ornithol 4:1976–1987

    Google Scholar 

  • Demetrius L (2006) The origin of allometric scaling laws in biology. J Theor Biol 243:455–467

    PubMed  Google Scholar 

  • Dietz MW, Ricklefs RE (1997) Growth rate and maturation of skeletal muscles over a size range of galliform birds. Physiol Biochem Zool 70:502–510

    CAS  Google Scholar 

  • Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116

    PubMed  Google Scholar 

  • Dohm M, Richardson C, Garland T (1994) Exercise physiology of wild and random-bred laboratory house mice and their reciprocal hybrids. Am J Physiol 36:R1098–R1108

    Google Scholar 

  • Dowling DK, Simmons LW (2009) Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc B Biol Sci 276:1737–1745

    CAS  Google Scholar 

  • Drilling NE, Thompson CF (1988) Natal and breeding dispersal in House Wrens (Troglodytes aedon). Auk 105:480–491

    Google Scholar 

  • Drummen GP, van Liebergen L, Op den Kamp JA, Post JA (2002) C11-BODIPY581/591, an oxidation-sensitive fluorescent lipid peroxidation probe:(micro) spectroscopic characterization and validation of methodology. Free Radical Biol Med 33:473–490

    CAS  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dufour E, Larsson NG (2004) Understanding aging, revealing order out of chaos. Biochim Biophys Acta 1658:122–132

    CAS  PubMed  Google Scholar 

  • Dumas J, Peyta L, Couet C, Servais S (2013) Implication of liver cardiolipins in mitochondrial energy metabolism disorder in cancer cachexia. Biochimie 95:27–32

    CAS  PubMed  Google Scholar 

  • Eli M (1992) Organ and tissue contribution to metabolic rate. In: Kinney JM, Tucker HN (eds) Energy metabolism: tissue determinants and cellular corollaries. Raven Press, New York, pp 61–79

    Google Scholar 

  • Else PL, Hulbert AJ (1985) An allometric comparison of the mitochondria of mammalian and reptilian tissues: the implications for the evolution of endothermy. J Comp Phyiol B 156:3–11

    CAS  Google Scholar 

  • Else PL, Wu BJ (1999) What role for membranes in determining the higher sodium pump molecular activity of mammals compared to ectotherms? J Comp Physiol B 169:296–302

    CAS  PubMed  Google Scholar 

  • Engelmann B, Brautigam C, Thiery J (1994) Plasmalogen phospholipids as potential protectors against lipid-peroxidation of low-density lipoproteins. Biochem Biophys Res Commun 204:1235–1242

    CAS  PubMed  Google Scholar 

  • Faaborg J, Arendt WJ (1995) Survival rates of Puerto Rican birds: are islands really that different? Auk 112:503–507

    Google Scholar 

  • Fankhauser DP (1971) Annual adult survival rates of blackbirds and starlings. Bird-Banding 42:36–42

    Google Scholar 

  • Felde R, Spiteller G (1995) Plasmalogen oxidation in human serum lipoproteins. Chem Phys Lipids 76:259–267

    CAS  PubMed  Google Scholar 

  • Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247

    CAS  PubMed  Google Scholar 

  • Fontaine JJ, Martel M, Markland HM, Niklison AM, Decker KL, Martin TE (2007) Testing ecological and behavioral correlates of nest predation. Oikos 116:1887–1894

    Google Scholar 

  • Francis CM, Terborgh JS and Fitzpatrick JW (1999) Survival rates of understory forest birds in Peru. In: Adams NJ, Slotow RH (eds) Proceedings 22nd International Ornithological Congress. BirdLife South Africa, Johannesburg, pp 326-335

  • Freed LA, Conant S, Fleischer RC (1987) Evolutionary ecology and radiation of Hawaiian passerine birds. Trends Ecol Evol 2:196–203

    CAS  PubMed  Google Scholar 

  • Fukagawa NK (1999) Aging: is oxidative stress a marker or is it causal? Proc Soc Exp Biol Med 222:293–298

    CAS  PubMed  Google Scholar 

  • Garrido G, Guzman M, Odriozola J (1996) Effects of physical training on fatty acid metabolism in liver and skeletal muscle of rats fed four different high- carbohydrate diets. J Nutr Biochem 7:348–355

    CAS  Google Scholar 

  • Ghalambor CK, Martine TE (2001) Fecundity-survival trade-offs and parental risk-taking in birds. Science 292:494–497

    CAS  PubMed  Google Scholar 

  • Gill SA, Haggerty TM (2012) A comparison of life history and parental care in temperate and tropical wrens. J Avian Biol 43:461–471

    Google Scholar 

  • Golden TR, Hinerfeld DA, Melov S (2002) Oxidative stress and aging: beyond correlation. Aging Cell 1:117–123

    CAS  PubMed  Google Scholar 

  • Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312

    CAS  PubMed  Google Scholar 

  • Hails CJ (1983) The metabolic rate of tropical birds. Condor 85:61–65

    Google Scholar 

  • Halliwell B, Gutteridge JM (1999) Free radicals in biology and medicine vol 135. Oxford university press, Oxford, p 729

    Google Scholar 

  • Hammond KA, Chappell MA, Cardullo RA, Lin R-S, Johnsen TS (2000) The mechanistic basis of aerobic performance variation in red junglefowl. J Exp Biol 203:2053–2064

    CAS  PubMed  Google Scholar 

  • Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Geront 11:298–300

    CAS  PubMed  Google Scholar 

  • Harman D (2001) Aging: overview. Ann N Y Acad Sci 928:1–21

    CAS  PubMed  Google Scholar 

  • Harper JM, Salmon AB, Leiser SF, Galecki AT, Miller RA (2007) Skin-derived fibroblasts from long-lived species are resistant to some, but not all, lethal stresses and to the mitochondrial inhibitor rotenone. Aging Cell 6:1–13

    CAS  PubMed Central  PubMed  Google Scholar 

  • Herrero A, Barja G (1997) Sites and mechanisms responsible for the low rate of free radical production of heart mitochondria in the long-lived pigeon. Mech Ageing Dev 98:95–111

    CAS  PubMed  Google Scholar 

  • Hilton B Jr, Miller MW (2003) Annual survival and recruitment in a ruby-throated hummingbird population, excluding the effect of transient individuals. Condor 105:54–62

    Google Scholar 

  • Huang H, Manton KG (2004) The role of oxidative damage in mitochondria during aging: a review. Front Biosci 9:1100–1111

    CAS  PubMed  Google Scholar 

  • Huang Z, Jiang J, Tyurin VA, Zhao Q, Mnuskin A, Ren J, Belikova NA, Feng W, Kurnikov IV, Kagan VE (2008) Cardiolipin deficiency leads to decreased cardiolipin peroxidation and increased resistance of cells to apoptosis. Free Radical Biol Med 44:1935–1944

    CAS  Google Scholar 

  • Hulbert AJ, Else PL (2005) Membranes and the setting of energy demand. J Exp Biol 208:1593–1599

    CAS  PubMed  Google Scholar 

  • Hulbert AJ (2010) Metabolism and longevity: is there a role for membrane fatty acids? Integr Comp Biol 50:808–817

    CAS  PubMed  Google Scholar 

  • Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87:1175–1213

    CAS  PubMed  Google Scholar 

  • Jang YC, Pérez VI, Song W, Lustgarten MS, Salmon AB, Mele J, Qi W (2009) Overexpression of Mn superoxide dismutase does not increase life span in mice. J Gerontol Ser A 64:1114–1125

    Google Scholar 

  • Jeon TI, Lim BO, Yu BP, Lim Y, Jeon EJ, Park DK (2001) Effect of dietary restriction on age-related increase of liver susceptibility to peroxidation in rats. Lipids 36:589–593

    CAS  PubMed  Google Scholar 

  • Jimenez AG, Dillaman R, Kinsey ST (2013a) Large fiber size in skeletal muscle is metabolically advantageous. Nat Commun 4:2150. doi:10.1038/ncomms3150

    PubMed Central  PubMed  Google Scholar 

  • Jimenez AG, Harper JM, Queenborough SA, Williams JB (2013b) Linkages between the life-history evolution of tropical and temperate birds and the resistance of their cells to oxidative and non-oxidative chemical injury. J Exp Biol 216:1373–1380

    CAS  PubMed  Google Scholar 

  • Jimenez AG, van Brocklyn J, Wortman M, Williams JB (2014a) Cellular metabolic rate is influenced by life-history traits in tropical and temperate birds. PLoS ONE 9:e87349. doi:10.1371/journal.pone.0087349

    PubMed Central  PubMed  Google Scholar 

  • Jimenez AG, Cooper-Mullin C, Anthony N, Williams JB (2014b) A comparison of cellular metabolic rate between isolated primary dermal fibroblasts and myoblast cells from fast-growing and slow-growing Coturnix quail. Comp Biochem Physiol A (in press)

  • Johnston JP, White SA, Peach WJ, Gregory RD (1997) Survival rates of tropical and temperate passerines: a Trinidadian perspective. Am Nat 150:771–789

    CAS  PubMed  Google Scholar 

  • Joshi AS, Zhou J, Gohil VM, Chen S, Greenberg ML (2009) Cellular functions of cardiolipin in yeast. Biochim Biophys Acta Mol Cell Res 1793:212–218

    CAS  Google Scholar 

  • Karr JR, Nichols JD, Klimkiewicz MK, Brawn JD (1990) Survival rates of birds of tropical and temperate forests: will the dogma survive? Am Nat 136:277–291

    Google Scholar 

  • Kersten M, Piersma T (1987) High levels of energy expenditure in shorebirds: metabolic adaptations to an energetically expensive way of life. Ardea 75:175–187

    Google Scholar 

  • Khairallah RJ, Kim J, O’Shea KM, O’Connell KA, Brown BH, Galvao T, Daneault C, des Rosiers C, Polster BM, Hoppel CL (2012) Improved mitochondrial function with diet-induced increase in either docosahexaenoic acid or arachidonic acid in membrane phospholipids. PLOS ONE 7:e34402

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kirkwood TB (1977) Evolution of ageing. Nature 270:301–304

    CAS  PubMed  Google Scholar 

  • Klaassen M, Drent R (1991) An analysis of hatchling resting metabolism: in search of ecological correlates that explain deviations from allometric relations. Condor 93:612–629

    Google Scholar 

  • Kleiber M (1975) The fire of life: an introduction to animal energetics. R.E. Krieger Pub. Co, Melbourne

    Google Scholar 

  • Koch LG, Britton SL (2008) Aerobic metabolism underlies complexity and capacity. J Physiol 586:83–95

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kowald A (2001) The mitochondrial theory of aging. Biol Signals Recept 10:162–175

    CAS  PubMed  Google Scholar 

  • Krebs HA (1950) Body size and tissue respiration. Biochim Biophys Acta 4:249–269

    CAS  PubMed  Google Scholar 

  • Lack D (1968) Bird migration and natural selection. Oikos 19:1–9

    Google Scholar 

  • Larsen S, Nielsen J, Hansen CN et al (2012) Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol 590:3349–3360

    CAS  PubMed Central  PubMed  Google Scholar 

  • Law R (1979) Optimal life histories under age-specific predation. Am Nat 114:399–417

    Google Scholar 

  • Leray C, Cazenave J, Gachet C (2002) Platelet phospholipids are differentially protected against oxidative degradation by plasmalogens. Lipids 37:285–290

    CAS  PubMed  Google Scholar 

  • Lessig J, Fuchs B (2009) Plasmalogens in biological systems: their role in oxidative processes in biological membranes, their contribution to pathological processes and aging and plasmalogen analysis. Curr Med Chem 16:2021–2041

    CAS  PubMed  Google Scholar 

  • Longo VD, Mitteldorf J, Skulachev VP (2005) Programmed and altruistic ageing. Nat Rev Genet 6:866–872

    CAS  PubMed  Google Scholar 

  • Lopez-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, de Cabo R (2006) Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci USA 103:1768–1773

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lopez-Torres M, Perez-Campo R, Cadenas S, Rojas C, Barja G (1993) A comparative study of free radicals in vertebrates-II. Non-enzymatic antioxidants and oxidative stress. Comp Biochem Physiol B Comp Biochem 105:757–763

    CAS  Google Scholar 

  • Maeba R, Ueta N (2003) Ethanolamine plasmalogens prevent the oxidation of cholesterol by reducing the oxidizability of cholesterol in phospholipid bilayers. J Lipid Res 44:164–171

    CAS  PubMed  Google Scholar 

  • Marsh R, Dawson W (1982) Substrate metabolism in seasonally acclimatized American goldfinches. Am J Physiol 242:R563–R569

    CAS  PubMed  Google Scholar 

  • Martin TE, Li P (1992) Life history traits of open-vs. cavity-nesting birds. Ecology 73:579–592

    Google Scholar 

  • Martin TE, Auer SK, Bassar RD, Niklison AM, Lloyd P (2007) Geographic variation in avian incubation periods and parental influences on embryonic temperature. Evolution 61:2558–2569

    PubMed  Google Scholar 

  • Martin TE, Lloyd P, Bosque C, Barton DC, Biancucci AL, Cheng YR, Ton R (2011) Growth rate variation among passerine species in tropical and temperate sites: an antagonistic interaction between parental food provisioning and nest predation risk. Evolution 65:1607–1622

    PubMed  Google Scholar 

  • McNab BK (1997) On the utility of uniformity in the definition of basal rate of metabolism. Physiol Zool 70:718–720

    CAS  PubMed  Google Scholar 

  • McNab BK (2008) An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol 151A:5–28

    CAS  Google Scholar 

  • McNab BK (2009) Ecological factors affect the level and scaling of avian BMR. Comp Biochem Physiol 152A:22–45

    CAS  Google Scholar 

  • Milby MM, Wright ME (1976) Survival of house sparrows and house finches in Kern County, California. Bird-Banding 47:119–122

    Google Scholar 

  • Mitchell T, Buffenstein R, Hulbert AJ (2007) Membrane phospholipid composition may contribute to exceptional longevity of the naked mole-rat (Heterocephalus glaber): a comparative study using shotgun lipidomics. Exp Geront 42:1053–1062

    CAS  Google Scholar 

  • Mitteldorf J, Pepper J (2009) Senescence as an adaptation to limit the spread of disease. J Theor Biol 260:186–195

    PubMed  Google Scholar 

  • Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92

    PubMed  Google Scholar 

  • Morandat S, Bortolato M, Anker G, Doutheau A, Lagarde M, Chauvet JP, Roux B (2003) Plasmalogens protect unsaturated lipids against UV-induced oxidation in monolayer. Biochim Biophys Acta Biomembr 1616:137–146

    CAS  Google Scholar 

  • Morrison P, Rosenmann M, Estes JA (1974) Metabolism and thermoregulation in the sea otter. Physiol Zool 47:218–229

    Google Scholar 

  • Moyes CD (2003) Controlling muscle mitochondrial content. J Exp Biol 206:4385–4391

    CAS  PubMed  Google Scholar 

  • Mueller P, Diamond J (2001) Metabolic rate and environmental productivity: well- provisioned animals evolved to run and idle fast. Proc Natl Acad Sci 98:12550–12554

    CAS  PubMed Central  PubMed  Google Scholar 

  • Munro D, Blier PU (2012) The extreme longevity of Artica islandica is associated with increased peroxidation resistance in mitochondrial membranes. Aging Cell 11:845–855

    CAS  PubMed  Google Scholar 

  • Murphy RC (2001) Free-radical-induced oxidation of arachidonoyl plasmalogen phospholipids: antioxidant mechanism and precursor pathway for bioactive eicosanoids. Chem Res Toxicol 14:463–472

    CAS  PubMed  Google Scholar 

  • Nealen P, Ricklefs R (2001) Early diversification of the avian brain: body relationship. J Zool 253:391–404

    Google Scholar 

  • Nespolo RF, Bacigalupe LD, Sabat P, Bozinovic F (2002) Interplay among energy metabolism, organ mass and digestive enzyme activity in the mouse-opossum Thylamys elegans: the role of thermal acclimation. J Exp Biol 205:2697–2703

    PubMed  Google Scholar 

  • Oniki Y, Ricklefs RE (1981) More growth rates of birds in the humid new world tropics. Ibis 123:349–354

    Google Scholar 

  • Oring LW, Lank DB, Maxson SJ (1983) Population studies of the polyandrous spotted sandpiper. Auk 100:272–285

    Google Scholar 

  • Pacheco MA, Beissinger SR, Bosque C (2010) Why grow slowly in a dangerous place? Postnatal growth, thermoregulation, and energetics of nestling green-rumped parrotlets (Forpus Passerinus). Auk 127:558–570

    Google Scholar 

  • Pape Møller A, Szép T (2002) Survival rate of adult barn swallows Hirundo rustica in relation to sexual selection and reproduction. Ecology 83:2220–2228

    Google Scholar 

  • Paradies G, Petrosillo G, Paradies V, Reiter RJ, Ruggiero FM (2010) Melatonin, cardiolipin and mitochondrial bioenergetics in health and disease. J Pineal Res 48:297–310

    CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    CAS  PubMed  Google Scholar 

  • Pearl R (1928) The rate of living. University Press, London

    Google Scholar 

  • Perez-Campo R, Lopez-Torres M, Rojas C, Cadenas S, Barja G (1994) Longevity and antioxidant enzymes, non-enzymatic antioxidants and oxidative stress in the vertebrate lung: a comparative study. J Comp Physiol B 163:682–689

    CAS  PubMed  Google Scholar 

  • Perez-Campo R, Lopez-Torres M, Cadenas S, Rojas C, Barja G (1998) The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approach. J Comp Physiol B 168:149–158

    CAS  PubMed  Google Scholar 

  • Petrosillo G, Matera M, Casanova G, Ruggiero FM, Paradies G (2008) Mitochondrial dysfunction in rat brain with aging Involvement of complex I, reactive oxygen species and cardiolipin. Neurochem Int 53:126–131

    CAS  PubMed  Google Scholar 

  • Piersma T (2002) Energetic bottlenecks and other design constraints in avian annual cycles. Integr Comp Biol 42:51–67

    PubMed  Google Scholar 

  • Piersma T, Bruinzeel L, Drent R, Kersten M, van der Meer J, Wiersma P (1996) Variability in basal metabolic rate of a long-distance migrant shorebird (red knot, Calidris canutus) reflects shifts in organ sizes. Physiol Zool 69:191–217

    Google Scholar 

  • Porter RK (2001) Allometry of mammalian cellular oxygen consumption. Cell Mol Life Sci 58:815–822

    CAS  PubMed  Google Scholar 

  • Pöyry S, Cramariuc O, Postila PA, Kaszuba K, Sarewicz M, Osyczka A, Vattulainen I, Róg T (2013) Atomistic simulations indicate cardiolipin to have an integral role in the structure of the cytochrome bc 1 complex. Biochim Biophys Acta 1827:769–778

    PubMed  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Remeŝ V, Martin TE (2002) Environmental influences on the evolution of growth and developmental rates in passerines. Evolution 56:2505–2518

    PubMed  Google Scholar 

  • Ricklefs RE (1968) Patterns of growth in birds. Ibis 110:419–451

    Google Scholar 

  • Ricklefs RE (1969a) Natural selection and the development of mortality rates in young birds. Nature 233:922–925

    Google Scholar 

  • Ricklefs RE (1969b) The nesting cycle of songbirds in tropical and temperate regions. Living Bird 8:165–175

    Google Scholar 

  • Ricklefs RE (1973) Patterns of growth in birds. II. Growth rate and mode of development. Ibis 115:177–201

    Google Scholar 

  • Ricklefs RE (1974) Energetics of reproduction in birds. pp 152–292

  • Ricklefs RE (1976) Growth rates of birds in the humid New World tropics. Ibis 118:179–207

    Google Scholar 

  • Ricklefs RE (1979) Patterns of growth in birds. V. A comparative study of development in the starling, common tern, and Japanese quail. Auk 96:10–30

    Google Scholar 

  • Ricklefs RE (1983) Avian postnatal development. Avian Biol 7:1–83

    Google Scholar 

  • Ricklefs RE (1997) Comparative demography of New World populations of thrushes (Turdus spp.). Ecol Monogr 67:23–43

    Google Scholar 

  • Ricklefs RE (2000) Density dependence, evolutionary optimization, and the diversification of avian life histories. Condor 103:9–22

    Google Scholar 

  • Ricklefs RE, Shea RE (2007) Estimating annual survival in sexually dimorphic species from proportions of first-year birds. Ecology 88:1408–1419

    PubMed  Google Scholar 

  • Ricklefs RE, Starck JM (1996) Applications of phylogenetically independent contrasts: a mixed progress report. Oikos 77:167–172

    Google Scholar 

  • Ricklefs RE, Webb T (1985) Water content, thermogenesis, and growth rate of skeletal muscles in the European Starling. Auk 102:369–376

    Google Scholar 

  • Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468

    Google Scholar 

  • Ricklefs RE, Shea RE, Choi IH (1994) Inverse relationship between functional maturity and exponential growth rate of avian skeletal muscle: a constraint on evolutionary response. Evolution 48:1080–1088

    Google Scholar 

  • Ricklefs RE, Tsunekage T, Shea RE (2011) Annual adult survival in several New World passerine birds based on age ratios in museum collections. J Ornithol 152:481. doi:10.1007/s10336-010-0614-9

    Google Scholar 

  • Ringsby TH, Sæther BE, Altwegg R, Solberg EJ (1999) Temporal and spatial variation in survival rates of a house sparrow, Passer domesticus, metapopulation. Oikos 85:419–425

    Google Scholar 

  • Robinson WD, Hau M, Klasing KC, Wikelski M, Brawn JD, Austin S, Tarwater CE, Ricklefs RE (2010) Diversification of life histories in New World birds. Auk 127:253–262

    Google Scholar 

  • Roff DA (1992) The evolution of life histories: theory and analysis. Springer, New York

    Google Scholar 

  • Rolfe D, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758

    CAS  PubMed  Google Scholar 

  • Rose M (1984) Genetic covariation in Drosophila life-history: untangling the data. Am Nat 123:565–569

    Google Scholar 

  • Rubner M (1908) Das Problem der Lebensdauer und seine Beziehungen zu Wachstum und Ernährung. R Oldenburg, Munich

    Google Scholar 

  • Russell EM, Yom-Tov Y, Geffen E (2004) Extended parental care and delayed dispersal: northern, tropical, and southern passerines compared. Behav Ecol 15:831–838

    Google Scholar 

  • Sæther BE (1989) Survival rates in relation to body weight in European birds. Ornis Scand 20:13–21

    Google Scholar 

  • Sæther BE, Bakke Ø (2000) Avian life history variation and contribution of demographic traits to the population growth rate. Ecology 81:642–653

    Google Scholar 

  • Salmon AB, Sadighi AA, Buffenstein R, Miller RA (2008) Fibroblasts from naked mole-rats are resistant to multiple forms of cell injury, but sensitive to peroxide, ultraviolet light and endoplasmic reticulum stress. J Gereontol 63A:232–241

    CAS  Google Scholar 

  • Samuels DC (2005) Life span is related to the free energy of mitochondrial DNA. Mech Ageing Dev 126:1123–1129

    CAS  PubMed  Google Scholar 

  • Sauer JR, Williams BK (1989) Generalized procedures for testing hypotheses about survival or recovery rates. J Wildl Manage 53:137–142

    Google Scholar 

  • Savidge IR, Davis DE (1974) Survival of some common passerines in a Pennsylvania woodlot. Bird-banding 45:152–155

    Google Scholar 

  • Schlame M, Ren M, Xu Y, Greenberg M, Haller I (2005) Molecular symmetry in mitochondrial cardiolipins. Chem Phys Lipids 138:38–49

    CAS  PubMed  Google Scholar 

  • Schleucher E, Withers PC (2002) Metabolic and thermal physiology of pigeons and doves. Physiol Biochem Zool 75:439–450

    PubMed  Google Scholar 

  • Scholander PF et al (1950) Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. Biol Bull 99:259–271

    CAS  PubMed  Google Scholar 

  • Seebacher F, Brand MD, Else PL, Guderley H, Hulbert AJ, Moyes CD (2010) Plasticity of oxidative metabolism in variable climates: molecular mechanisms. Physiol Biochem Zool 83:721–732

    CAS  PubMed  Google Scholar 

  • Selman C, Blount JD, Nussey DH, Speakman JR (2012) Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol Evol 27:570–577

    PubMed  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    CAS  PubMed  Google Scholar 

  • Siriwardena GM, Baillie SR, Wilson JD (1999) Temporal variation in the annual survival rates of six granivorous birds with contrasting population trends. Ibis 141:621–636

    Google Scholar 

  • Skutch AF (1985) Clutch size, nesting success, and predation on nests of neotropical birds, reviewed. Ornithol Monogr 36:575–594

    Google Scholar 

  • Snow DW, Lill A (1974) Longevity records for some neotropical land birds. Condor 76:262–267

    Google Scholar 

  • Sohal RS, Allen RG (1990) Oxidative stress as a causal factor in differentiation and aging: a unifying hypothesis. Exp Gerontol 25:499–522

    CAS  PubMed  Google Scholar 

  • Sohal RS, Orr WC (2012) The redox stress hypothesis of aging. Free Radical Biol Med 52:539–555

    CAS  Google Scholar 

  • Sorrell JM, Caplan AI (2004) Fibroblast heterogeneity: more than skin deep. J Cell Sci 117(5): 667–675

    CAS  PubMed  Google Scholar 

  • Speakman JR (2005) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730

    PubMed  Google Scholar 

  • Speakman JR (2008) The physiological costs of reproduction in small mammals. Philos Trans R Soc 27:375–398

    Google Scholar 

  • Speakman JR, Selman C (2011) The free radical damage theory: accumulating evidence against a simple link of oxidative stress to ageing and lifespan. BioEssays 33:255–259

    PubMed  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Styrsky JN (2003) Life-history evolution and population dynamics of a neotropical forest bird (Hylophylax naevioides). Thesis/Dissertation: Thesis (Ph. D.) University of Illinois at Urbana-Champaign

  • Suarez RK (1996) Upper limits to mass specific metabolic rates. Annu Rev Physiol 58:583–605

    CAS  PubMed  Google Scholar 

  • Surai PF (2002) Selenium in poultry nutrition I. Antioxidant properties, deficiency and toxicity. Worlds Poult Sci J Wyton 58:333–348

    Google Scholar 

  • Swanson DL, Liknes ET (2006) A comparative analysis of thermogenic capacity and cold tolerance in small birds. J Exp Biol 209:466–474

    PubMed  Google Scholar 

  • Tieleman BI, Williams JB, Buschur ME, Brown CR (2003) Phenotypic variation of larks along an aridity gradient: are desert birds more flexible? Ecology 84:1800–1815

    Google Scholar 

  • Tieleman BI, Dijkstra TH, Lasky JR, Mauck RA, Visser GH, Williams JB (2006) Physiological and behavioural correlates of life-history variation: a comparison between tropical and temperate zone House Wrens. Funct Ecol 20:491–499

    Google Scholar 

  • Tjorve KMC (2007) Does chick development relate to breeding latitude in waders and gulls? Bull Wader Study Group 112:12

    Google Scholar 

  • Valencak T, Ruf T (2007) Membrane fatty acids and maximum lifespan in mammals: a reassessment. Comp Biochem Physiol A 146:S55

    Google Scholar 

  • Van Voorhies WA (1992) Production of sperm reduces nematode lifespan. Nature 360:456–458

    CAS  PubMed  Google Scholar 

  • Vézina F, Williams TD (2005) Interaction between organ mass and citrate synthase activity as an indicator of tissue maximal oxidative capacity in breeding European starlings: implications for metabolic rate and organ mass relationships. Funct Ecol 19:119–128

    Google Scholar 

  • Vézina F, Jalvingh KM, Dekinga A, Piersma T (2006) Acclimation to different thermal conditions in a northerly wintering shorebird is driven by body mass-related changes in organ size. J Exp Biol 209:3141–3154

    PubMed  Google Scholar 

  • Vleck CM, Vleck D (1979) Metabolic rate in five tropical bird species. Condor 81:89–91

    Google Scholar 

  • Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang Z, O’Connor TP, Heshka S, Heymsfield SB (2001) The reconstruction of Kleiber’s law at the organ-tissue level. J Nutr 131:2967–2970

    CAS  PubMed  Google Scholar 

  • Watkins S, Carter L, German J (1998) Docosahexaenoic acid accumulates in cardiolipin and enhances HT-29 cell oxidant production. J Lipid Res 39:1583–1588

    CAS  PubMed  Google Scholar 

  • Weathers WW (1979) Climatic adaptation in avian standard metabolic rate. Oecologia 42:81–89

    Google Scholar 

  • Weber TP, Piersma T (1996) Basal metabolic rate and the mass of tissues differing in metabolic scope: migration-related covariation between individual knots Calidris canutus. J Avian Biol 27:215–224

    Google Scholar 

  • Weibel ER, Hoppeler H (2005) Exercise-induced maximal metabolic rate scales with muscle aerobic capacity. J Exp Biol 208:1635–1644

    PubMed  Google Scholar 

  • West GB, Savage VM, Gillooly J, Enquist B, Woodruff WH, Brown JH (2003) Why does metabolic rate scale with body size? Nature 421:713

    CAS  PubMed  Google Scholar 

  • Wharton WP (1935) Survival as indicated by returns to Summerville, South Carolina. Bird-Banding 6:125–130

    Google Scholar 

  • Wheatley DN (2007) Convergence of metabolic rate of cultured cells from animals of different sizes. Am J Physiol Regul Integr Comp Physiol 292:R2113–R2114

    CAS  PubMed  Google Scholar 

  • White CR, Seymour RS (2004) Does basal metabolic rate contain a useful signal? Mammalian BMR allometry and correlations with a selection of physiological, ecological, and life-history variables. Physiol Biochem Zool 77:929–941

    PubMed  Google Scholar 

  • Wiersma P, Muñoz-Garcia A, Walker A, Williams JB (2007a) Tropical birds have a slow pace of life. Proc Natl Acad Sci 104:9340–9345

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wiersma P, Selman C, Speakman JR, Verhulst S (2004) Birds sacrifice oxidative protection for reproduction. Proc Biol Sci 271(Suppl 5):S360–S363

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wiersma P, Chappell MA, Williams JB (2007b) Cold-and exercise-induced peak metabolic rates in tropical birds. Proc Natl Acad Sci 104:20866–20871

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wiersma P, Nowak B, Williams JB (2012) Small organ size contributes to the slow pace of life in tropical birds. J Exp Biol 215:1662–1669

    PubMed  Google Scholar 

  • Williams JB, Tieleman BI, Visser GH, Ricklefs RE (2007) Does growth rate determine the rate of metabolism in shorebird chicks living in the Arctic? Physiol Biochem Zool 80:500–513

    PubMed  Google Scholar 

  • Williams JB, Miller RA, Harper JM, Wiersma P (2010) Functional linkages for the pace of life, life-history, and environment in birds. Integr Comp Biol 50:855–868

    PubMed Central  PubMed  Google Scholar 

  • Wu BJ, Hulbert AJ, Storlien LH, Else PL (2004) Membrane lipids and sodium pumps of cattle and crocodiles: an experimental test of the membrane pacemaker theory of metabolism. Am J Physiol 287:R633–R641

    CAS  Google Scholar 

  • Zoeller RA, Morand OH, Raetz CRH (1988) A possible role for plasmalogens in protecting animal-cells against photosensitized killing. J Biol Chem 263:11590–11596

    CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Dr. Raineldo Urriola, and the Autoridad Nacional del Ambiente for permission to collect birds in Panama, and the Smithsonian Tropical Research Institute for hosting us. Dr. Jim Van Brocklyn’s help was indispensable in raising cells from Panamanian birds, and Dr. Jim Harper has been a tremendous source of knowledge for our lab while learning to do tissue culture. We greatly appreciate Dr. Matt Wortman’s constant hospitality in his lab and his generosity in letting us use his XF Analyzer. We would like to thank the Velleman lab at the Ohio State University Wooster campus and Cynthia Coy for her help in teaching us myoblast tissue culture methods. We also appreciate Paul Blischak’s help in creating our consensus trees. This study was funded by NSF IBN 0212587 (JBW), and a Smithsonian Tropical Research Institute post-doctoral fellowship (AGJ).

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  1. Department of Evolution, Ecology and Organismal Biology, Ohio State University, 318 W. 12th Ave., Columbus, OH, 43210, USA

    Ana Gabriela Jimenez, Clara Cooper-Mullin, Elisabeth A. Calhoon & Joseph B. Williams

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  1. Ana Gabriela Jimenez
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  2. Clara Cooper-Mullin
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  3. Elisabeth A. Calhoon
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  4. Joseph B. Williams
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Correspondence to Ana Gabriela Jimenez.

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Communicated by I. D. Hume.

Appendix

Appendix

Growth

We tested for phylogenetic signal in our comparisons of growth rate in tropical and temperate birds. We first sampled 1,000 trees from birdtree.org, and used BEAST TreeAnnotator v1.8.0 (Drummond et al. 2012) to identify three consensus trees, one for growth rates of all birds in the dataset, one for growth rates of Passerines, and one for growth rates of Non-Passerines. Phylogenetic-independent contrast was run in R version 3.0.2 (R Development Core Team 2013) using the package ape v2.6 (Paradis et al. 2004). There was a phylogenetic signal in growth rates of tropical and temperate species for all birds in the dataset (Bloomberg’s K = 1.47). When phylogenetically informed analysis was used, tropical birds had slower growth rates than temperate birds (PIC, F = 18.34, p < 0.001), consistent with the results from conventional analysis. There was no phylogenetic signal in growth rates of tropical and temperate species for Passeriformes (Bloomberg’s K = 0.4). For our colleagues that would insist that we include phylogeny in the analysis, growth rates of tropical passerines were significantly lower than temperate passerines when we used statistics that were phylogenetically informed (PIC, F = 3.9, p = 0.01), consistent with our results from conventional ANOVAs. There was no phylogenetic signal in growth rates of tropical and temperate species for Passeriformes (Bloomberg’s K = 0.8), and phylogenetically informed analysis did not change the results (PIC, F = 2.93, p = 0.06).

Survival

We tested for phylogenetic signal in our comparisons of survival rate in tropical and temperate birds. We first sampled 1,000 trees from birdtree.org, and used BEAST TreeAnnotator v1.8.0 (Drummond et al. 2012) to identify a consensus tree. Phylogenetic-independent contrast was run in R version 3.0.2 (R Development Core Team 2013) using the package ape v2.6 (Paradis et al. 2004). There was no phylogenetic signal in survival rates of tropical and temperate species (Bloomberg’s K = 0.2). When we ran phylogenetically informed analysis, survival rates of tropical species were significantly higher than temperate birds (PIC, F = 3.9, p = 0.01), consistent with our results from conventional analysis.

All consensus trees used in this study are available from cooper-mullin.1@buckeyemail.osu.edu.

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Jimenez, A.G., Cooper-Mullin, C., Calhoon, E.A. et al. Physiological underpinnings associated with differences in pace of life and metabolic rate in north temperate and neotropical birds. J Comp Physiol B 184, 545–561 (2014). https://doi.org/10.1007/s00360-014-0825-0

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