The evolutionary consequences of oxygenic photosynthesis: a body size perspective


The high concentration of molecular oxygen in Earth’s atmosphere is arguably the most conspicuous and geologically important signature of life. Earth’s early atmosphere lacked oxygen; accumulation began after the evolution of oxygenic photosynthesis in cyanobacteria around 3.0–2.5 billion years ago (Gya). Concentrations of oxygen have since varied, first reaching near-modern values ~600 million years ago (Mya). These fluctuations have been hypothesized to constrain many biological patterns, among them the evolution of body size. Here, we review the state of knowledge relating oxygen availability to body size. Laboratory studies increasingly illuminate the mechanisms by which organisms can adapt physiologically to the variation in oxygen availability, but the extent to which these findings can be extrapolated to evolutionary timescales remains poorly understood. Experiments confirm that animal size is limited by experimental hypoxia, but show that plant vegetative growth is enhanced due to reduced photorespiration at lower O2:CO2. Field studies of size distributions across extant higher taxa and individual species in the modern provide qualitative support for a correlation between animal and protist size and oxygen availability, but few allow prediction of maximum or mean size from oxygen concentrations in unstudied regions. There is qualitative support for a link between oxygen availability and body size from the fossil record of protists and animals, but there have been few quantitative analyses confirming or refuting this impression. As oxygen transport limits the thickness or volume-to-surface area ratio—rather than mass or volume—predictions of maximum possible size cannot be constructed simply from metabolic rate and oxygen availability. Thus, it remains difficult to confirm that the largest representatives of fossil or living taxa are limited by oxygen transport rather than other factors. Despite the challenges of integrating findings from experiments on model organisms, comparative observations across living species, and fossil specimens spanning millions to billions of years, numerous tractable avenues of research could greatly improve quantitative constraints on the role of oxygen in the macroevolutionary history of organismal size.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4



Present atmospheric level (of oxygen)


Millions of years ago


Billions of years ago


  1. Acquisti C, Kleffe J, Collins S (2007) Oxygen content of transmembrane proteins over macroevolutionary time scales. Nature 445:47–52

  2. Albani AE, Bengtson S, Canfield DE, Bekker A, Macchiarelli R, Mazurier A, Hammarlund EU, Boulvais P, Dupuy J-J, Fontaine C, Fürsich FT, Gauthier-Lafaye F, Janvier P, Javaux E, Ossa FO, Pierson-Wickmann A-C, Riboulleau A, Sardini P, Vachard D, Whitehouse M, Meunier A (2010) Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago. Nature 466:100–104

  3. Alexander RM (1971) Size and shape. Edward Arnold, London

  4. Allwood AC, Walter MR, Kamber BS, Marshall CP, Burch IW (2006) Stromatolite reef from the Early Archaean era of Australia. Nature 441:714–718

  5. Andrews RM (2002) Low oxygen: a constraint on the evolution of viviparity in reptiles. Physiol Biochem Zool 75:145–154

  6. Barghoorn ES, Tyler SA (1963) Fossil organisms from Precambrian sediments. Ann N Y Acad Sci 108:451–452

  7. Barghoorn ES, Tyler SA (1965) Microorganisms from Gunflint Chert—these structurally preserved Precambrian fossils from Ontario are most ancient organisms known. Science 147:563–575

  8. Barras CG, Twitchett RJ (2007) Response of the marine infauna to Triassic-Jurassic environmental change: ichnological data from southern England. Palaeogeogr Palaeoclimatol Palaeoecol 244:223–241

  9. Belcher CM, McElwain JC (2008) Limits for combustion in low O2 redefine paleoatmospheric predictions for the Mesozoic. Science 321:1197–1200

  10. Bergman NM, Lenton TM, Watson AJ (2004) COPSE: a new model of biogeochemical cycling over Phanerozoic time. Am J Sci 304:397–437

  11. Berkner LV, Marshall LC (1965) History of major atmospheric components. Proc Natl Acad Sci USA 53:1215–1226

  12. Berner RA (2004) The Phanerozoic carbon cycle: CO2 and O2. Oxford University Press, New York

  13. Berner RA (2006) GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2. Geochim Cosmochim Acta 70:5653–5664

  14. Berner RA, Canfield DE (1989) A new model for atmospheric oxygen over Phanerozoic time. Am J Sci 289:333–361

  15. Berner RA, Beerling DJ, Dudley R, Robinson JM, Wildman RA (2003) Phanerozoic atmospheric oxygen. Annu Rev Earth Planet Sci 31:105–134

  16. Berner RA, VandenBrooks JM, Ward PD (2007) Oxygen and evolution. Science 316:557–558

  17. Björkman O, Hiesey WM, Nobs MA, Nicholson F, Hart RW (1968) Effect of oxygen concentration in higher plants. Carnegie Inst Wash Year B 66:228–232

  18. Björkman O, Gauhl E, Hiesey WM, Nicholson F, Nobs MA (1969) Growth of Mimulus, Marchantia, and Zea under different oxygen and carbon dioxide levels. Carnegie Inst Wash Year B 67:477–478

  19. Blankenship RE, Sadekar S, Raymond J (2007) The evolutionary transition from anoxygenic to oxygenic photosynthesis. In: Falkowski PG, Knoll AH (eds) Evolution of primary producers in the sea. Academic Press, Amsterdam, pp 21–35

  20. Bonner JT (1965) Size and cycle. Princeton University Press, Princeton, NJ

  21. Bonner JT (1988) The evolution of complexity by means of natural selection. Princeton University Press, Princeton, NJ

  22. Bonner JT (2006) Why size matters: from bacteria to blue whales. Princeton University Press, Princeton, NJ

  23. Braddy SJ, Poschmann M, Tetlie OE (2008) Giant claw reveals the largest ever arthropod. Biol Lett 4:106–109

  24. Brocks JJ, Logan GA, Buick R, Summons RE (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285:1033–1036

  25. Brown JH (1995) Macroecology. University of Chicago Press, Chicago

  26. Brown JH, Marquet PA, Taper ML (1993) Evolution of body-size—consequences of an energetic definition of fitness. Am Nat 142:573–584

  27. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

  28. Brown JH, West GB, Enquist BJ (2005) Yes, West, Brown and Enquist’s model of allometric scaling is both mathematically correct and biologically relevant. Funct Ecol 19:735–738

  29. Brusca RC, Brusca GJ (2003) Invertebrates. Sinauer Associates, Sunderland, MA

  30. Busk M, Overgaard J, Hicks JW, Bennett AF, Wang T (2000) Effects of feeding on arterial blood gases in the American alligator Alligator mississippiensis. J Exp Biol 203:3117–3124

  31. Butterfield NJ (2000) Bangiomorpha pubescens n. gen., n.sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26:386–404

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

  33. Canfield DE (2005) The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu Rev Earth Planet Sci 33:1–36

  34. Canfield DE, Poulton SW, Narbonne GM (2007) Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315:92–95

  35. Carpenter FM (1960) Studies on Carboniferous insects. 1. The Protodonata. Psyche 67:98–110

  36. Catling DC, Glein CR, Zahnle KJ, McKay CP (2005) Why O2 is required by complex life on habitable planets and the concept of planetary “oxygenation time”. Astrobiology 5:415–438

  37. Chan T, Burggren W (2005) Hypoxic incubation creates differential morphological effects during specific developmental critical windows in the embryo of the chicken (Gallus gallus). Respir Physiol Neurobiol 145:251–263

  38. Chapelle G, Peck LS (1999) Polar gigantism dictated by oxygen availability. Nature 399:114–115

  39. Chapelle G, Peck LS (2004) Amphipod crustacean size spectra: new insights in the relationship between size and oxygen. Oikos 106:167–175

  40. Cloud PE (1965) Significance of the Gunflint (Precambrian) microflora. Science 148:27–35

  41. Cloud PE (1968) Pre-metazoan evolution and the origins of the Metazoa. In: Drake ET (ed) Evolution and environment. Yale University Press, New Haven, pp 1–72

  42. Cloud PE (1972) A working model of the primitive Earth. Am J Sci 272:537–548

  43. Crossley DA II, Altimiras J (2005) Cardiovascular development in embryos of the American alligator Alligator mississippiensis: effects of chronic and acute hypoxia. J Exp Biol 208:31–39

  44. Cunningham EL, Brody JS, Jain BP (1974) Lung growth induced by hypoxia. J Appl Physiol 37:362–366

  45. Dabrowski K, Lee K-J, Guz L, Verlhac V, Gabaudan J (2004) Effects of dietary ascorbic acid on oxygen stress (hypoxia or hyperoxia), growth and tissue vitamin concentrations in juvenile rainbow trout (Oncorhynchus mykiss). Aquaculture 233:383–392

  46. Darveau CA, Suarez RK, Andrews RD, Hochachka PW (2002) Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 417:166–170

  47. DeLong JP, Okie JG, Moses ME, Sibly RM, Brown JH (2010) Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life. Proc Natl Acad Sci USA 107. doi: 10.1073/iti2510107

  48. Dodds PS, Rothman DH, Weitz JS (2001) Re-examination of the “3/4-law” of metabolism. J Theor Biol 209:9–27

  49. Dudley R (1998) Atmospheric oxygen, giant Paleozoic insects and the evolution of aerial locomotor performance. J Exp Biol 201:1043–1050

  50. Dutta A, Popel AS (1995) A theoretical analysis of intracellular oxygen diffusion. J Theor Biol 176:433–445

  51. Dzialowski EM, von Plettenberg D, Elmonoufy NA, Burggren WW (2002) Chronic hypoxia alters the physiological and morphological trajectories of developing chicken embryos. Comp Biochem Physiol A 131:713–724

  52. Else PL, Hulbert AJ (1981) Comparison of the “mammal machine” and the “reptile machine”: energy production. Am J Physiol 240:3–9

  53. Falkowski PG, Katz ME, Milligan AJ, Fennel K, Cramer BS, Aubry MP, Berner RA, Novacek MJ, Zapol WM (2005) The rise of oxygen over the past 205 million years and the evolution of large placental mammals. Science 309:2202–2204

  54. Fan C, Iacobas DA, Zhou D, Chen Q, Lai JK, Gavrialov O, Haddad GG (2005) Gene expression and phenotypic characterization of mouse heart after chronic constant or intermittent hypoxia. Physiol Genomics 22:292–307

  55. Fehling J, Stoecker D, Baldauf SL (2007) Photosynthesis and the eukaryote tree of life. In: Falkowski PG, Knoll AH (eds) Evolution of primary producers in the sea. Academic Press, Amsterdam, pp 75–107

  56. Fike DA, Grotzinger JP, Pratt LM, Summons RE (2006) Oxidation of the Ediacaran ocean. Nature 444:744–747

  57. Finkel ZV, Katz ME, Wright JD, Schofield OME, Falkowski PG (2005) Climatically driven macroevolutionary patterns in the size of marine diatoms of the Cenozoic. Proc Natl Acad Sci USA 102:8927–8932

  58. Finkel ZV, Sebbo J, Feist-Burkhardt S, Irwin AJ, Katz ME, Schofield OEM, Young JR, Falkowski PG (2007) A universal driver of macroevolutionary change in the size of marine phytoplankton over the Cenozoic. Proc Natl Acad Sci USA 104:20416–20420

  59. Foss A, Vollen T, Øiestad V (2003) Growth and oxygen consumption in normal and O2 supersaturated water, and interactive effects of O2 saturation and ammonia on growth in spotted wolffish (Anarhichas minor Olafsen). Aquaculture 224:105–116

  60. Fraiser ML, Bottjer DJ (2004) The non-actualistic Early Triassic gastropod fauna: a case study of the Lower Triassic Sinbad Limestone member. Palaios 19:259–275

  61. Fralick P, Davis DW, Kissin SA (2002) The age of the Gunflint Formation, Ontario, Canada: single zircon U–Pb age determinations from reworked volcanic ash. Can J Earth Sci 39:1085–1091

  62. Frappell PB, Mortola JP (1994) Hamsters vs. rats: metabolic and ventilatory response to development in chronic hypoxia. J Appl Physiol 77:2748–2752

  63. 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

  64. Frei R, Gaucher C, Poulton SW, Canfield DE (2009) Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes. Nature 461:250–253

  65. Frisancho AR, Baker PT (1970) Altitude and growth: a study of the patterns of physical growth of a high altitude Peruvian Quechua population. Am J Phys Anthropol 32:279–292

  66. Gilbert DL (1960) Speculation on the relationship between organic and atmospheric evolution. Perspect Biol Med 4:58–71

  67. Gilbert DL (1996) Evolutionary aspects of atmospheric oxygen and organisms. In: Fregly MJ, Blatteis CM (eds) Environmental physiology. Oxford University Press, New York, pp 1059–1094

  68. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001a) Effects of size and temperature on metabolic rate. Science 293:2248–2251

  69. Gillooly JF, Charnov EL, West GB, Savage VM, Brown JH (2001b) Effects of size and temperature on developmental time. Nature 417:70–73

  70. Giussani DA, Salinas CE, Villena M, Blanco CE (2007) The role of oxygen in prenatal growth: studies in the chicken embryo. J Physiol 585:911–917

  71. Gooday AJ, Bernhard JM, Levin LA, Suhr SB (2000) Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas. Deep-Sea Res II 47:25–54

  72. Gould SJ (1988) Trends as changes in variance—a new slant on progress and directionality in evolution. J Paleontol 62:319–329

  73. Gould SJ (1996) Full house: the spread of excellence from Plato to Darwin. Harmony Books, New York

  74. Graham JB, Aguilar NM, Dudley R, Gans C (1995) Implications of the late Paleozoic oxygen pulse for physiology and evolution. Nature 375:117–120

  75. Graham MH, Kinlan BP, Druehl LD, Garske LE, Banks S (2007) Deep-water kelp refugia as potential hotspots of tropical marine diversity and productivity. Proc Natl Acad Sci USA 104:16576–16580

  76. Greenberg S, Ar A (1996) Effects of chronic hypoxia, normoxia and hyperoxia on larval development in the beetle Tenebrio molitor. J Insect Physiol 42:991–996

  77. Greenlee KJ, Harrison JF (2004) Development of respiratory function in the American locust Schistocerca americana I. Across-instar effects. J Exp Biol 207:497–508

  78. Greenlee KJ, Harrison JF (2005) Respiratory changes throughout ontogeny in the tobacco hornworm caterpillar, Manduca sexta. J Exp Biol 208:1385–1392

  79. Greenlee KJ, Nebeker C, Harrison JF (2007) Body size-independent safety margins for gas exchange across grasshopper species. J Exp Biol 210:1288–1296

  80. Guo SS, Tang YK, Gao F, Ai WD, Qin LF (2008) Effects of low pressure and hypoxia on growth and development of wheat. Acta Astronaut 63:1081–1085

  81. Hallam A, Wignall PB (1997) Mass extinctions and their aftermaths. Oxford University Press, New York

  82. Hallock P (1985) Why are larger Foraminifera large? Paleobiology 11:195–208

  83. Harrison JF (2010) Atmospheric oxygen level and the evolution of insect body size. Proc R Soc Lond B 277:1937–1946

  84. Harrison J, Frazier MR, Henry JR, Kaiser A, Klok CJ, Rascón B (2006) Responses of terrestrial insects to hypoxia or hyperoxia. Respir Physiol Neurobiol 154:4–17

  85. He C, Davies FT, Lacey RE (2007) Separating the effects of hypobaria and hypoxia on lettuce: growth and gas exchange. Physiol Plant 131:226–240

  86. He W-H, Twitchett RJ, Zhang Y, Shi GR, Feng Q-L, Yu J-X, Wu S-B, Peng X-F (2010) Controls on body size during the Late Permian mass extinction event. Geobiology. doi: 10.1111/j.1472-4669.2010.00248.x

  87. Henry JR, Harrison JF (2004) Plastic and evolved responses of larval tracheae and mass to varying atmospheric oxygen content in Drosophila melanogaster. J Exp Biol 207:3559–3567

  88. Herman J, Ingermann R (1996) Effects of hypoxia and hyperoxia on oxygen-transfer properties of the blood of a viviparous snake. J Exp Biol 199:2061–2070

  89. Holland HD (2006) The oxygenation of the atmosphere and oceans. Philos Trans R Soc Lond B 361:903–915

  90. Holland HD (2009) Why the atmosphere became oxygenated: a proposal. Geochim Cosmochim Acta 73:5241–5255

  91. Hsia CCW, Carbayo JJP, Yan X, Bellotto DJ (2005) Enhanced alveolar growth and remodeling in Guinea pigs raised at high altitude. Respir Physiol Neurobiol 147:105–115

  92. Huey RB, Ward PD (2005) Hypoxia, global warming, and terrestrial Late Permian extinctions. Science 308:398–401

  93. Jacobsen D, Rostgaard S, Vásconez JJ (2003) Are macroinvertebrates in high altitude streams affected by oxygen deficiency? Freshw Biol 48:2025–2032

  94. Javaux EJ, Marshall CP, Bekker A (2010) Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits. Nature 463:934–938

  95. Jin J (2001) Evolution and extinction of the North American Hiscobeccus brachiopod Fauna during the Late Ordovician. Can J Earth Sci 38:143–151

  96. Johnson MD, Volker J, Moeller HV, Laws E, Breslauer KJ, Falkowski PG (2009) Universal constant for heat production in protists. Proc Natl Acad Sci USA 106:6696–6699

  97. Julian CG, Vargas E, Armaza JF, Wilson MJ, Niermeyer S, Moore LG (2007) High-altitude ancestry protects against hypoxia-associated reductions in fetal growth. Arch Dis Child 92:F372–F377

  98. Kaiho K (1998) Global climatic forcing of deep-sea benthic foraminiferal test size during the past 120 m.y. Geology 26:491–494

  99. Kaiser A, Klok CJ, Socha JJ, Lee W-K, Quinlan MC, Harrison JF (2007) Increase in tracheal investment with beetle size supports hypothesis of oxygen limitation on insect gigantism. Proc Natl Acad Sci USA 104:13198–13203

  100. Kam Y-C (1993) Physiological effects of hypoxia on metabolism and growth of turtle embryos. Respir Physiol 92:127–138

  101. Kirkton SD, Niska JA, Harrison JE (2005) Ontogenetic effects on aerobic and anaerobic metabolism during jumping in the American locust, Schistocerca americana. J Exp Biol 208:3003–3012

  102. Kleiber M (1932) Body size and metabolism. Hilgardia 6:315–351

  103. Klok CJ, Harrison JF (2009) Atmospheric hypoxia limits selection for large body size in insects. PLoS One 4:e3876

  104. Klok CJ, Hubb AJ, Harrison JF (2009) Single and multigenerational responses of body mass to atmospheric oxygen concentrations in Drosophila melanogaster: evidence for roles of plasticity and evolution. J Evol Biol 22:2496–2504

  105. Klok CJ, Kaiser A, Lighton JRB, Harrison JF (2010) Critical oxygen partial pressures and maximal tracheal conductances for Drosophila melanogaster reared for multiple generations in hypoxia or hyperoxia. J Insect Physiol 56:461–469

  106. Knoll AH (1992) The early evolution of eukaryotes—a geological perspective. Science 256:622–627

  107. Knoll AH (2003) The geological consequences of evolution. Geobiology 1:3–14

  108. Knoll AH, Carroll SB (1999) Early animal evolution: emerging views from comparative biology and geology. Science 284:2129–2137

  109. Knoll AH, Holland HD (1995) Oxygen and Proterozoic evolution: an update. In: Commission on Geosciences EaR (ed) Effects of past global change on life. National Academy Press, Washington, DC, pp 21–33

  110. Knoll AH, Bambach RK, Payne JL, Pruss S, Fischer WW (2007) Paleophysiology and end-Permian mass extinction. Earth Planet Sci Lett 256:295–313

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

  112. Kozlowski J, Konarzewski M (2005) West, Brown and Enquist’s model of allometric scaling again: the same questions remain. Funct Ecol 19:739–743

  113. Kukalová-Peck J (1985) Ephemeroid wing venation based upon new gigantic Carboniferous mayflies and basic morphology, phylogeny, and metamorphosis of pterygote insects (Insecta, Ephemerida). Can J Zool 63:933–955

  114. Kumar S (1995) Megafossils from the Mesoproterozoic Rohtas Formation (the Vindhyan Supergroup), Katni area, central India. Precambr Res 72:171–184

  115. Kump LR (2008) The rise of atmospheric oxygen. Nature 451:277–278

  116. Kump LR, Barley ME (2007) Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago. Nature 448:1033–1036

  117. Labandiera CC (2005) The fossil record of insect extinction: new approaches and future directions. Am Entomol 51:14–29

  118. Lane N (2002) Oxygen: the molecule that made the world. Oxford University Press, Oxford

  119. Lenton TM (2003) The coupled evolution of life and atmospheric oxygen. In: Lister A, Rothschild LJ (eds) Evolution on planet earth: impact of the physical environment. Academic Press, San Diego, pp 33–51

  120. Levin LA (2003) Oxygen minimum zone benthos: adaptation and community response to hypoxia. Oceanogr Mar Biol Annu Rev 41:1–45

  121. Levin LA, Plaia GR, Huggett CL (1994) The influence of natural organic enhancement on life histories and community structure of bathyal polychaetes. In: Young CM, Eckelbarger KJ (eds) Reproduction, larval biology, and recruitment of the deep-sea benthos. Columbia University Press, Columbia, SC, pp 261–283

  122. Lighton JRB (2007) Respiratory biology: they would be giants. Curr Biol 17:R969–R971

  123. Loudon C (1988) Development of Tenebrio molitor in low oxygen levels. J Insect Physiol 34:97–103

  124. Lyons TW, Reinhard CT (2009) Early Earth: oxygen for heavy-metal fans. Nature 461:179–181

  125. Makarieva AM, Gorshkov VG, Li B-L (2003) A note on metabolic rate dependence on body size in plants and animals. J Theor Biol 221:301–307

  126. Makarieva AM, Gorshkov VG, Li B-L, Chown SL, Reich PB, Gavrilov VM (2008) Mean mass-specific metabolic rates are strikingly similar across life’s major domains: evidence for life’s metabolic optimum. Proc Natl Acad Sci USA 105:16994–16999

  127. Marshall CR (2006) Explaining the Cambrian “explosion” of animals. Annu Rev Earth Planet Sci 34:355–384

  128. McAlester AL (1970) Animal extinctions, oxygen consumption, and atmospheric history. J Paleontol 44:405–409

  129. McClain CR, Barry J (2010) Habitat heterogeneity, biotic disturbance, and resource availability work in concert to regulate biodiversity in deep submarine canyons. Ecology 91:964–976

  130. McClain CR, Rex M (2001) The relationship between dissolved oxygen concentration and maximum size in deep-sea turrid gastropods: an application of quantile regression. Mar Biol 139:681–685

  131. McClain CR, Rex MA, Jabbour R (2005) Deconstructing bathymetric patterns of body size in deep-sea gastropods. Mar Ecol Prog Ser 297:181–187

  132. McClain CR, Boyer A, Rosenberg G (2006) The island rule and the evolution of body size in the deep sea. J Biogeogr 33:1578–1584

  133. McMinn A, Pankowski A, Delfatti T (2005) Effect of hyperoxia on the growth and photosynthesis of polar sea microalgae. J Phycol 41:732–741

  134. McShea DW (1994) Mechanisms of large-scale evolutionary trends. Evolution 48:1747–1763

  135. Metcalfe J, McCutcheon IE, Francisco DL, Metzenberg AB, Welch JE (1981) Oxygen availability and growth of the chick embryo. Respir Physiol 46:81–88

  136. Mills NE, Barnhart MC (1999) Effects of hypoxia on embryonic development in two Ambystoma and two Rana species. Physiol Biochem Zool 72:179–188

  137. Mojzsis SJ, Arrhenius G, McKeegan KD, Harrison TM, Nutman AP, Friend CRL (1996) Evidence for life on Earth before 3, 800 million years ago. Nature 384:55–59

  138. Mori S, Yamaji K, Ishida A, Prokushkin SG, Masyagina OV, Hagihara A, Rafiqul Hoque ATM, Suwa R, Osawa A, Nishizono T, Ueda T, Kinjo M, Miyagi T, Kajimoto T, Koike T, Matsuura Y, Toma T, Zyryanova OA, Abaimov AP, Awaya Y, Araki MG, Kawasaki T, Chiba Y, Umari M (2010) Mixed-power scaling of whole-plant respiration from seedlings to giant trees. Proc Natl Acad Sci USA 107:1447–1451

  139. Mortola JP, Xu L, Lauzon A-M (1990) Body growth, lung and heart weight, and DNA content in newborn rats exposed to different levels of chronic hypoxia. Can J Physiol Pharmacol 68:1590–1594

  140. Mortola JP, Frappell PB, Aguero L, Armstrong K (2000) Birth weight and altitude: a study in Peruvian communities. J Pediatr 136:324–329

  141. Musgrave ME, Strain BR (1988) Response of two wheat cultivars to CO2 enrichment under subambient oxygen conditions. Plant Physiol 87:346–350

  142. Nelson SJ (1959) Arctic Ordovician fauna: an equatorial assemblage? J Alta Soc Petrol Geol 7:45–47

  143. Newell ND (1949) Phyletic size increase, an important trend illustrated by fossil invertebrates. Evolution 3:103–124

  144. Niklas KJ (2007) Maximum plant height and the factors that limit it. Tree Physiol 27:433–440

  145. Norris RD (1989) Cnidarian taphonomy and affinities of the Ediacara biota. Lethaia 22:381–393

  146. Nursall JR (1959) Oxygen as a prerequisite to the origin of the Metazoa. Nature 183:1170–1172

  147. Okajima R (2008) The controlling factors limiting maximum body size of insects. Lethaia 41:423–430

  148. Owerkowicz T, Elsey RM, Hicks JW (2009) Atmospheric oxygen level affects growth trajectory, cardiopulmonary allometry and metabolic rate in the American alligator (Alligator mississippiensis). J Exp Biol 212:1237–1247

  149. Payne JL (2005) Evolutionary dynamics of gastropod size across the end-Permian extinction and through the Triassic recovery interval. Paleobiology 31:269–290

  150. Payne JL, Boyer AG, Brown JH, Finnegan S, Kowalewski M, Krause RA, Lyons SK, McClain CR, McShea DW, Novack-Gottshall PM, Smith FA, Stempien JA, Wang SC (2009) Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity. Proc Natl Acad Sci USA 106:24–27

  151. Peck LS, Chapelle G (2003) Reduced oxygen at high altitude limits maximum size. Proc R Soc Lond B 270:S166–S167

  152. Peck LS, Maddrell SHP (2005) Limitation of size by hypoxia in the fruit fly Drosophila melanogaster. J Exp Zool 303A:968–975

  153. Perez-Cruz LL, Machain-Castillo ML (1990) Benthic foraminifera of the oxygen minimum zone, continental shelf of the Gulf of Tehuantepec, Mexico. J Foramin Res 20:312–325

  154. Peters RH (1983) The ecological implications of body size. Cambridge University Press, New York

  155. Phleger FB, Soutar A (1973) Production of benthic foraminifera in three east Pacific oxygen minima. Micropaleontology 19:110–115

  156. Pruder GD, Bolton ET (1980) Differences between cell division and carbon fixation rates associated with light intensity and oxygen concentration: implications in the cultivation of an estuarine diatom. Mar Biol 59:1–6

  157. Quebedeaux B, Hardy RWF (1973) Oxygen as a new factor controlling reproductive growth. Nature 243:477–479

  158. Quebedeaux B, Hardy RWF (1975) Reproductive growth and dry matter production of Glycine max (L.) Merr. in response to oxygen concentration. Plant Physiol 55:102–107

  159. Raff RA, Raff EC (1970) Respiratory mechanisms and the metazoan fossil record. Nature 228:1003–1005

  160. Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR (2008) Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455:1101–1104

  161. Raup DM, Sepkoski JJ (1982) Mass extinctions in the marine fossil record. Science 215:1501–1503

  162. Raven JA (1991) Plant responses to high O2 concentrations: relevance to previous high O2 episodes. Palaeogeogr Palaeoclimatol Palaeoecol 97:19–38

  163. Raven JA, Johnston AM, Parsons R, Kübler J (1994) The influence of natural and experimental high O2 concentrations on O2-evolving phototrophs. Biol Rev 69:61–94

  164. Retallack GJ, Smith RMH, Ward PD (2003) Vertebrate extinction across the Permian-Triassic boundary in Karoo Basin, South Africa. Geol Soc Am Bull 115:1133–1152

  165. Rex MA, Etter RJ, Morris JS, Crouse J, McClain CR, Johnson NA, Stuart CT, Thies R, Avery R (2006) Global bathymetric patterns of standing stock and body size in the deep-sea benthos. Mar Ecol Prog Ser 317:1–8

  166. Rhoads DC, Morse JW (1971) Evolutionary and ecologic significance of oxygen-deficient marine basins. Lethaia 4:413–428

  167. Rohr DM, Blodgett RB, Furnish WMF (1992) Maclurina manitobensis (Whiteaves) (Ordovician Gastropoda): the largest known Paleozoic gastropod. J Paleontol 66:880–884

  168. Rolfe WDI, Ingham JK (1967) Limb structure, affinity and diet of the Carboniferous “centipede” Arthropleura. Scot J Geol 3:118–124

  169. Rosing MT (1999) C-13-depleted carbon microparticles in >3700-Ma sea-floor sedimentary rocks from west Greenland. Science 283:674–676

  170. Rudkin DM, Young GA, Elias RJ, Dobrzanski EP (2003) The world’s biggest trilobite—Isotelus rex new species from the Upper Ordovician of northern Manitoba, Canada. J Paleontol 77:99–112

  171. Runnegar B (1982) Oxygen requirements, biology and phylogenetic significance of the late Precambrian worm Dickinsonia, and the evolution of the burrowing habit. Alcheringa 6:223–239

  172. Rutten MG (1966) Geologic data on atmospheric history. Palaeogeogr Palaeoclimatol Palaeoecol 2:47–57

  173. Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth. Bioscience 47:235–242

  174. Samuelsson J, Butterfield NJ (2001) Neoproterozoic fossils from the Franklin Mountains, northwestern Canada: stratigraphic and palaeobiological implications. Precambr Res 107:235–251

  175. Savage VM, Gillooly JF, Woodruff WH, West GB, Allen AP, Enquist BJ, Brown JH (2004) The predominance of quarter-power scaling in biology. Funct Ecol 18:257–282

  176. Schidlowski M, Appel PWU, Eichmann R, Junge CE (1979) Carbon isotope geochemistry of the 3.7 × 109-yr-old Isua sediments, West Greenland—implications for the Archaean carbon and oxygen cycles. Geochim Cosmochim Acta 43:189–199

  177. Schlanger SO, Jenkyns HC (1976) Cretaceous oceanic anoxic events: causes and consequences. Geol Mijnb 55:179–184

  178. Schmidt DN, Thierstein HR, Bollmann J, Schiebel R (2004) Abiotic forcing of plankton evolution in the Cenozoic. Science 303:207–210

  179. Schmidt-Nielsen K (1984) Scaling, why is animal size so important. Cambridge University Press, New York

  180. Schneider DA, Bickford ME, Cannon WF, Schulz KJ, Hamilton MA (2002) Age of volcanic rocks and syndepositional iron formations, Marquette Range Supergroup: implications for the tectonic setting of Paleoproterozoic iron formations of the Lake Superior region. Can J Earth Sci 39:999–1012

  181. Schopf JW (1993) Microfossils of the Early Archean Apex Chert—new evidence of the antiquity of life. Science 260:640–646

  182. Schopf JW, Klein C (1992) The Proterozoic biosphere: a multidisciplinary study. Cambridge University Press, New York

  183. Schopf JW, Packer BM (1987) Early Archean (3.3-billion to 3.5-billion-year-old) microfossils from Warrawoona Group, Australia. Science 237:70–73

  184. Scott C, Lyons TW, Bekker A, Shen Y, Poulton SW, Chu X, Anbar AD (2008) Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452:456–459

  185. Sebens KP (2002) Energetic constraints, size gradients, and size limits in benthic marine invertebrates. Integr Comp Biol 42:853–861

  186. Sessions AL, Doughty DM, Welander PV, Summons RE, Newman DK (2009) The continuing puzzle of the Great Oxidation Event. Curr Biol 19:R567–R574

  187. Shear WA, Kukalová-Peck J (1990) The ecology of Paleozoic terrestrial arthropods: the fossil evidence. Can J Zool 68:1807–1834

  188. Smith DM, Cook A (2001) Beetle bias: how sedimentary environment influences patterns of coleopteran diversity in the fossil record. Geological Society of America Annual Meeting Abstracts with Program 33:267

  189. Socha JJ, Lee W-K, Harrison JF, Waters JS, Fezzaa K, Westneat MW (2008) Correlated patterns of tracheal compression and convective gas exchange in a carabid beetle. J Exp Biol 211:3409–3420

  190. Stahl WR (1967) Scaling of respiratory variables in mammals. J Appl Physiol 22:453–460

  191. Stanley SM (1973) An explanation for Cope’s rule. Evolution 27:1–26

  192. Stephen JW, Dulynn H, Tobias W (1995) Responses to chronic hypoxia in embryonic alligators. J Exp Zool 273:44–50

  193. Stock MK, Francisco DL, Metcalfe J (1983) Organ growth in chick embryos incubated in 40% or 70% oxygen. Respir Physiol 52:1–11

  194. Sundt-Hansen L, Sundström LF, Einum S, Hindar K, Fleming IA, Devlin RH (2007) Genetically enhanced growth causes increased mortality in hypoxic environments. Biol Lett 3:165–168

  195. Tappan H (1974) Molecular oxygen and evolution. In: Hayaishi O (ed) Molecular oxygen in biology. Elsevier, Amsterdam, pp 81–135

  196. Teichert C, Kummel B (1960) Size of endoceroid cephalolopods. Breviora 128:1–7

  197. Thannickal VJ (2009) Oxygen in the evolution of complex life and the price we pay. Am J Respir Cell Mol Biol 40:507–510

  198. Tice MM, Lowe DR (2004) Photosynthetic microbial mats in the 3, 416-Myr-old ocean. Nature 431:549–552

  199. Tintu AN, le Noble FAC, Rouwet EV (2007) Hypoxia disturbs fetal hemodynamics and growth. Endothelium 14:353–360

  200. Torzillo G, Bernardini P, Masojídek J (1998) On-line monitoring of chlorophyll fluorescence to assess the extent of photoinhibition of photosynthesis induced by high oxygen concentration and low temperature and its effect on the productivity of outdoor cultures of Spirulina plantensis (Cyanobacteria). J Phycol 34:504–510

  201. Twitchett RJ (2007) The Lilliput effect in the aftermath of the end-Permian extinction event. Palaeogeogr Palaeoclimatol Palaeoecol 252:132–144

  202. Twitchett RJ, Barras CG (2004) Trace fossils in the aftermath of mass extinction events. Geol Soc Lond 228:397–418

  203. Tyler SA, Barghoorn ES (1954) Occurrence of structurally preserved plants in pre-cambrian rocks of the Canadian Shield. Science 119:606–608

  204. Wangensteen OD, Rahn H, Burton RR, Smith AH (1974) Respiratory gas exchange of high altitude adapted chick embryos. Respir Physiol 21:61–70

  205. West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126

  206. Westneat MW, Betz O, Blob RW, Fezzaa K, Cooper WJ, Lee W-K (2003) Tracheal respiration in insects visualized with synchrotron X-ray imaging. Science 299:558–560

  207. Whyte MA (2005) Palaeoecology: a gigantic fossil arthropod trackway. Nature 438:576–577

  208. Wignall PB, Hallam A (1992) Anoxia as a cause of the Permian Triassic mass extinction: facies evidence from northern Italy and the western United-States. Palaeogeogr Palaeoclimatol Palaeoecol 93:21–46

  209. Wignall PB, Twitchett RJ (1996) Oceanic anoxia and the end Permian mass extinction. Science 272:1155–1158

  210. Williams JB, Swift K (1988) Oxygen consumption and growth of Northern Bobwhite embryos under normoxic and hyperoxic conditions. The Condor 90:187–192

  211. Woods HA, Moran AL, Arango CP, Mullen L, Shields C (2009) Oxygen hypothesis of polar gigantism not supported by performance of Antarctic pycnogonids in hypoxia. Proc R Soc Lond B 276:1069–1075

  212. Xiao S, Dong L (2006) On the morphological and ecological history of Proterozoic macroalgae. In: Xiao S, Kaufman AJ (eds) Neoproterozoic geobiology and paleobiology. Springer, Dordrecht, pp 57–90

  213. Zamudio S, Postigo L, Illsley NP, Rodriguez C, Heredia G, Brimacombe M, Echalar L, Torricos T, Tellez W, Moldonado I, Balanza E, Alvarez T, Ameller J, Vargas E (2007) Maternal oxygen delivery is not related to altitude- and ancestry-associated differences in human fetal growth. J Physiol 582:883–895

Download references


This review is a product of the working group on body size evolution (principal investigators JLP, JAS, and MK) funded by the National Evolutionary Synthesis Center (NESCent), National Science Foundation Grant EF-0423641. P. Falkowski, P. Harnik, J. Skotheim, and N. Sleep provided comments that greatly improved the manuscript. We thank G.X. Rothdrake for correcting the body size estimate of the Ordovician cephalopod.

Author information

Correspondence to Jonathan L. Payne.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Payne, J.L., McClain, C.R., Boyer, A.G. et al. The evolutionary consequences of oxygenic photosynthesis: a body size perspective. Photosynth Res 107, 37–57 (2011) doi:10.1007/s11120-010-9593-1

Download citation


  • Body size
  • Oxygen
  • Evolution
  • Precambrian
  • Maximum size
  • Optimum size