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Contrasting seasonal patterns of carbon gain in evergreen and deciduous trees of ancient polar forests

Published online by Cambridge University Press:  08 April 2016

Dana L. Royer
Affiliation:
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom. E-mail: c.p.osborne@sheffield.ac.uk, E-mail: d.j.beerling@sheffield.ac.uk
Colin P. Osborne
Affiliation:
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom. E-mail: c.p.osborne@sheffield.ac.uk, E-mail: d.j.beerling@sheffield.ac.uk
David J. Beerling*
Affiliation:
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom. E-mail: c.p.osborne@sheffield.ac.uk, E-mail: d.j.beerling@sheffield.ac.uk
*
Corresponding author

Abstract

Polar deciduous forests were an important biome during much of the Mesozoic and Paleogene, occupying upwards of 40% of the total land surface. Little is known about their physiological ecology, however, because these types of forests do not exist for study today. Furthermore, the role of high atmospheric CO2 levels in modulating the physiological response of ancient polar forests is poorly known. Here we report detailed measurements of whole-tree net carbon uptake over a full annual cycle for five tree species whose close ancestors were components of Cretaceous and Paleogene polar forests. Measurements were made on both evergreen and deciduous species after two years growth in a simulated Mesozoic polar (69°N) environment at either ambient (400 ppmv) or elevated (800 ppmv) levels of CO2. The deciduous species exhibited a significant pulse in carbon uptake during the late summer and early autumn (August to mid-October) that enabled them to achieve annual carbon budgets similar to those of evergreen trees, despite incurring higher carbon losses through annual leaf shedding. Area-based photosynthetic rates dropped progressively in all species during the polar summer (June to mid-July), resulting in decreases in whole-tree carbon uptake late in the polar summer. The high-CO2-grown trees were more strongly affected by this polar summer depression than the low-CO2-grown trees. Our results indicate that, from a carbon balance perspective, deciduous taxa have no clear advantage over evergreens. Moreover, the seasonal patterns reported here suggest that at latitudes poleward of 69°, evergreens will be even more strongly favored. The consideration of factors not directly related to carbon budgeting is probably therefore required to fully understand the adaptive significance of the deciduous leaf habit in ancient polar forests.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Askin, R. A., and Spicer, R. A. 1995. The Late Cretaceous and Cenozoic history of vegetation and climate at northern and southern high latitudes: a comparison. Pp. 156173in Effects of past global change on life. Studies in Geophysics Series, National Research Council. National Academy Press, Washington, D.C.Google Scholar
Axelrod, D. I. 1966. Origin of deciduous and evergreen habits in temperate forests. Evolution 20:115.Google Scholar
Beerling, D. J., and Osborne, C. P. 2002. Physiological ecology of Mesozoic polar forests in a high CO2 environment. Annals of Botany 89:329339.Google Scholar
Beerling, D. J., and Royer, D. L. 2002. Fossil plants as indicators of the Phanerozoic global carbon cycle. Annual Review of Earth and Planetary Sciences 30:527556.Google Scholar
Beerling, D. J., and Woodward, F. I. 2001. Vegetation and the terrestrial carbon cycle: modelling the first 400 million years. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Beerling, D. J., Woodward, F. I., Lomas, M. R., Wills, M. A., Quick, W. P., and Valdes, P. J. 1998. The influence of Carboniferous palaeoatmospheres on plant function: an experimental and modelling assessment. Philosophical Transactions of the Royal Society of London B 353:131140.Google Scholar
Berner, R. A., and Kothavala, Z. 2001. GEOCARB III: a revised model of atmospheric CO2 over Phanerozoic time. American Journal of Science 301:182204.Google Scholar
Chabot, B. F., and Hicks, D. F. 1982. The ecology of leaf life spans. Annual Review of Ecology and Systematics 13:229259.Google Scholar
Chaney, R. W. 1947. Tertiary centers and migration routes. Ecological Monographs 17:139148.Google Scholar
Chaney, R. W. 1951. A revision of the fossil Sequoia and Taxodium in western North America based on the recent discovery of Metasequoia. American Philosophical Society Transactions 40:171263.Google Scholar
Creber, G. T., and Chaloner, W. G. 1985. Tree growth in the Mesozoic and Early Tertiary and the reconstruction of palaeoclimates. Palaeogeography, Palaeoclimatology, Palaeoecology 52:3560.Google Scholar
Damesin, C. 2003. Respiration and photosynthesis characteristics of current-year stems of Fagus sylvatica: from the seasonal pattern to an annual balance. New Phytologist 158:465475.Google Scholar
Dutton, A. L., Lohmann, K. C., and Zinsmeister, W. J. 2002. Stable isotope and minor element proxies for Eocene climate of Seymour Island, Antarctica. Paleoceanography 17(2), 1016, doi: 10.1029/2000PA000593.Google Scholar
Eissenstat, D. M., Graham, J. H., Syvertsen, J. P., and Drouillard, D. L. 1993. Carbon economy of sour orange in relation to mycorhiza colonization and phosphorus status. Annals of Botany 71:110.Google Scholar
Ekart, D. D., Cerling, T. E., Montañez, I. P., and Tabor, N. J. 1999. A 400 million year carbon isotope record of pedogenic carbonate: implications for paleoatmospheric carbon dioxide. American Journal of Science 299:805827.Google Scholar
Ellsworth, D. S. 2000. Seasonal CO2 assimilation and stomatal limitations in a Pinus taeda canopy. Tree Physiology 20:435445.Google Scholar
Estes, R., and Hutchison, J. 1980. Eocene lower vertebrates from Ellesmere Island, Canadian Arctic Archipelago. Palaeogeography, Palaeoclimatology, Palaeoecology 30:325347.CrossRefGoogle Scholar
Falcon-Lang, H. J., and Cantrill, D. J. 2001. Leaf phenology of some mid-Cretaceous polar forests, Alexander Island, Antarctica. Geological Magazine 138:3952.Google Scholar
Frakes, L. A., Francis, J. E., and Syktus, J. I. 1992. Climate modes of the Phanerozoic: the history of the earth's climate over the past 600 million years. Cambridge University Press, Cambridge.Google Scholar
Francis, J. E., and Poole, I. 2002. Cretaceous and Tertiary climates of Antarctica: evidence from fossil wood. Palaeogeography, Palaeoclimatology, Palaeoecology 182:4764.Google Scholar
Givnish, T. J. 2002. Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fennica 36:703743.Google Scholar
Griffis, T. J., Black, T. A., Morgenstern, K., Barr, A. G., Nesic, Z., Drewitt, G. B., Gaumont-Guay, D., and McCaughey, J. H. 2003. Ecophysiological controls on the carbon balances of three southern boreal forests. Agricultural and Forest Meteorology 117:5371.Google Scholar
Hari, P., and Mäkelä, A. 2003. Annual pattern of photosynthesis in Scots pine in the boreal zone. Tree Physiology 23:145155.Google Scholar
Herman, A. B., and Spicer, R. A. 1996. Palaeobotanical evidence for a warm Cretaceous Arctic Ocean. Nature 380:330333.Google Scholar
Hickey, L. J. 1984. Eternal summer at 80 degrees north. Discovery 17(1):1723.Google Scholar
Hill, R. S. 1991. Tertiary Nothofagus (Fagaceae) macrofossils from Tasmania and Antarctica and their bearing on the evolution of the genus. Linnean Society Botanical Journal 105:73112.Google Scholar
Huber, B. T., Norris, R. D., and MacLeod, K. G. 2002. Deep-sea paleotemperature record of extreme warmth during the Cretaceous. Geology 30:123126.Google Scholar
Jagels, R., Visscher, G. E., Lucas, J., and Goodell, B. 2003. Palaeo-adaptive properties of the xylem of Metasequoia: mechanical/hydraulic compromises. Annals of Botany 92:7988.Google Scholar
Jahren, A. H., and Sternberg, L. S. L. 2003. Humidity estimate for the middle Eocene Arctic rain forest. Geology 31:463466.2.0.CO;2>CrossRefGoogle Scholar
Jefferson, T. H. 1982. Fossil forests from the Lower Cretaceous of Alexander Island, Antarctica. Palaeontology 25:681708.Google Scholar
Lloyd, J., Shibistova, O., Zolotoukhine, D., Kolle, O., Arneth, A., Wirth, C., Styles, J. M., Tchebakova, N. M., and Schulze, E. D. 2002. Seasonal and annual variations in the photosynthetic productivity and carbon balance of a central Siberian pine forest. Tellus B 54:590610.Google Scholar
Milliken, G. A., and Johnson, D. E. 1992. Analysis of messy data, Vol. I. Designed experiments. Van Nostrand Reinhold, New York.Google Scholar
Osborne, C. P., and Beerling, D. J. 2003. The penalty of a long, hot summer. Photosynthetic acclimation to high CO2 and continuous light in “living fossil” conifers. Plant Physiology 133:803812.Google Scholar
Read, J., and Francis, J. 1992. Responses of some Southern Hemisphere tree species to a prolonged dark period and their implications for high-latitude Cretaceous and Tertiary floras. Palaeogeography, Palaeoclimatology, Palaeoecology 99:271290.Google Scholar
Royer, D. L., Hickey, L. J., and Wing, S. L. 2003a. Ecological conservatism in the “living fossil” Ginkgo. Paleobiology 29:84104.Google Scholar
Royer, D. L., Osborne, C. P., and Beerling, D. J. 2003b. Carbon loss by deciduous trees in a CO2-rich ancient polar environment. Nature 424:6062.Google Scholar
Rustad, L. E., Campbell, J. L., Marion, G. M., Norby, R. J., Mitchell, M. J., Hartley, A. E., Cornelissen, J. H. C., and Gurevitch, J. 2001. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543562.Google Scholar
Sokal, R. R., and Rohlf, F. J. 1995. Biometry, 3d ed.W. H. Freeman, New York.Google Scholar
Spicer, R. A., and Chapman, J. L. 1990. Climate change and the evolution of high-latitude terrestrial vegetation and flora. Trends in Ecology and Evolution 5:279284.Google Scholar
Starr, G., Oberbauer, S. F., and Pop, E. W. 2000. Effects of lengthened growing season and soil warming on the phenology and physiology of Polygonum bistorta. Global Change Biology 6:357369.Google Scholar
Stylinski, C. D., Gamon, J. A., and Oechel, W. C. 2002. Seasonal patterns of reflectance indices, carotenoid pigments and photosynthesis of evergreen chaparral species. Oecologia 131:366374.Google Scholar
Sun, B., Dilcher, D. L., Beerling, D. J., Zhang, C., Yan, D., and Kowalski, E. 2003. Variation in Ginkgo biloba L. leaf characters across a climatic gradient in China. Proceedings of the National Academy of Sciences USA 100:71417146.Google Scholar
Sweet, A. R., and Braman, D. R. 2001. Cretaceous-Tertiary palynofloral perturbations and extinctions within the Aquilapollenites phytogeographic province. Canadian Journal of Earth Science 38:249269.Google Scholar
Tarduno, J. A., Brinkman, D. B., Renne, P. R., Cottrell, R. D., Scher, H., and Castillo, P. 1998. Evidence for extreme climatic warmth from Late Cretaceous arctic vertebrates. Science 282:22412244.Google Scholar
Tieszen, L. L. 1975. CO2 exchange in the Alaskan arctic tundra: seasonal changes in the rate of photosynthesis of four species. Photosynthetica 9:376390.Google Scholar
Tralau, H. 1968. Evolutionary trends in the genus Ginkgo. Lethaia 1:63101.Google Scholar
Tripati, A., Zachos, J., Marincovich, L., and Bice, K. 2001. Late Paleocene Arctic coastal climate inferred from molluscan stable and radiogenic isotope ratios. Palaeogeography, Palaeoclimatology, Palaeoecology 170:101113.Google Scholar
Williams, C. J., Johnson, A. H., LePage, B. A., Vann, D. R., and Sweda, T. 2003. Reconstruction of Tertiary Metasequoia forests. II. Structure, biomass, and productivity of Eocene floodplain forests in the Canadian Arctic. Paleobiology 29:271292.Google Scholar
Wing, S. L., Harrington, G. J., Bowen, G. J., and Koch, P. L. 2003. Floral change during the Initial Eocene Thermal Maximum in the Powder River Basin, Wyoming. In Wing, S. L., Gingerich, P. D., and Thomas, E., eds. Causes and consequences of globally warm climates in the early Paleogene. Geological Society of America Special Paper 369:425440.Google Scholar
Wolfe, J. A. 1985. Distribution of major vegetational types during the Tertiary. Pp. 357375in Sundquist, E. T. and Broecker, W. S., eds. The carbon cycle and atmospheric CO2: natural variations, Archean to present. Geophysical Monograph Series No. 32. American Geophysical Union, Washington, D.C.Google Scholar
Wolfe, J. A. 1987. Late Cretaceous-Cenozoic history of deciduousness and the terminal Cretaceous event. Paleobiology 13:215226.Google Scholar
Woodward, F. I. 1987. Climate and plant distribution. Cambridge University Press, Cambridge.Google Scholar
Zachos, J., Pagani, M., Sloan, L., Thomas, E., and Billups, K. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686693.Google Scholar