Original Research

You have full text access to this OnlineOpen article

Differential physiological responses to environmental change promote woody shrub expansion

  1. Mary Heskel1,*,
  2. Heather Greaves2,
  3. Ari Kornfeld3,4,
  4. Laura Gough5,
  5. Owen K. Atkin6,
  6. Matthew H. Turnbull4,
  7. Gaius Shaver7,
  8. Kevin L. Griffin1,8

Article first published online: 13 MAR 2013

DOI: 10.1002/ece3.525

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Issue

Ecology and Evolution

Ecology and Evolution

Volume 3, Issue 5, pages 1149–1162, May 2013

Additional Information

How to Cite

Ecology and Evolution 2013; 3(5):1149–1162.

Author Information

  1. 1

    Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, New York USA

  2. 2

    Department of Forest Ecosystems and Society, Oregon State University, Corvallis, Oregon, USA

  3. 3

    Department of Global Ecology, Carnegie Institution for Science, Stanford, California, USA

  4. 4

    School of Biological Sciences, University of Canterbury, Christchurch, New Zealand

  5. 5

    Department of Biology, University of Texas-Arlington, Arlington, Texas, USA

  6. 6

    Research School of Biology, The Australian National University, Canberra, ACT, Australia

  7. 7

    Ecosystems Center, Marine Biological Laboratory, Woods Hole, Massachusetts, USA

  8. 8

    Department of Earth and Environmental Sciences, Lamont-Doherty Earth Observatory, Columbia University, Palisades, New York USA, USA

* Correspondence
Mary Heskel, Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, NY 10027. Tel: (267) 259-7549; Fax: +1-845-365-8150; E-mail: mah2207@columbia.edu

Publication History

  1. Issue published online: 10 MAY 2013
  2. Article first published online: 13 MAR 2013
  3. Manuscript Accepted: 14 FEB 2013
  4. Manuscript Revised: 13 FEB 2013
  5. Manuscript Received: 30 JAN 2013

Funded by

  • National Science Foundation. Grant Number: #0732664
  • Australian Research Council. Grant Number: DP0986823
  • Marsden Fund of the Royal Society of New Zealand

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (623K)

References

  • Atkin, O. K., and M. J. Tjoelker. 2003. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci. 8:343–351.
  • Atkin, O. K., M. Westbeek, M. L. Cambridge, H. Lambers, and T. L. Pons. 1997. Leaf respiration in light and darkness: a comparison of slow- and fast-growing Poa species. Plant Physiol. 113:961–965.
  • Atkin, O. K., I. Scheurwater, and T. L. Pons. 2006. High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric. Glob. Change Biol. 12:500–515.
    Direct Link:
  • Ayub, G., R. A. Smith, D. T. Tissue, and O. K. Atkin. 2011. Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature. New Phytol. 190:1003–1018.
    Direct Link:
  • Biasi, C., H. Meyer, O. Rusalimova, R. Hammerle, C. Kaiser, C. Baranyi, et al. 2008. Initial effects of experimental warming on carbon exchange rates, plant growth and microbial dynamics of a lichen-rich dwarf shrub tundra in Siberia. Plant Soil 307:191–205.
  • Bigger, M. C., and W. C. Oechel. 1982. Nutrient effect on maximum photosynthesis in arctic plants. Holarct. Ecol. 5:158–163.
  • Blok, D., G. Schaepman-Strub, H. Bartholomeus, M. M. P. D. Heijmans, T. C. Maximov, and F. Berendse. 2011. The response of Arctic vegetation to the summer climate: relation between shrub cover, NDVI, surface albedo and temperature. Environ. Res. Lett. 6:35502.
  • Boelman, N., M. Stieglitz, K. L. Griffin, and G. R. Shaver. 2005. Inter-annual variability of NDVI in response to long-term warming and fertilization in wet sedge and tussock tundra. Oecologia 143:588–597.
  • Bret-Harte, M. S., G. R. Shaver, J. P. Zoerner, J. F. Johnstone, J. L. Wagner, A. S. Chavez, et al. 2001. Developmental plasticity allows Betula nana to dominate tundra subjected to an altered environment. Ecology 82:18–32.
  • Bret-Harte, M. S., G. R. Shaver, and F. S. Chapin III. 2002. Primary and secondary stem growth in arctic shrubs: implications for community response to environmental change. J. Ecol. 90:251–267.
    Direct Link:
  • Brooks, A., and G. Farquhar. 1985. Effect of temperature on the CO2-O2 specificity of ribulose-1, 5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165:397–406.
  • Budde, R. J., and D. D. Randall. 1990. Pea leaf mitochondrial pyruvate dehydrogenase complex is inactivated in vivo in a light-dependent manner. Proc. Natl. Acad. Sci. USA 87:673–676.
  • von Caemmerer, S., and G. D. Farquhar. 1981. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387.
  • Chapin, F. S., III, and G. R. Shaver. 1985. Individualistic growth-response of tundra plant species to environmental manipulations in the field. Ecology 66:564–576.
  • Chapin, F. S., III, and G. R. Shaver. 1996. Physiological and growth responses of Arctic plants to a field experiment simulating climatic change. Ecology 77:822–840.
  • Chapin, F. S., III, G. R. Shaver, A. E. Giblin, K. J. Nadelhoffer, and J. A. Laundre. 1995. Responses of Arctic tundra to experimental and observed changes in climate. Ecology 76:694–711.
  • Chapin, F. S. III, M. Sturm, M. C. Serreze, J. P. McFadden, J. R. Key, A. H. Lloyd, et al. 2005. Role of land-surface changes in Arctic summer warming. Science 310:657–660.
  • Clemmensen, K. E., A. Michelsen, S. Jonasson, and G. R. Shaver. 2006. Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytol. 171:391–404.
    Direct Link:
  • Collatz, G. J. 1977. Influence of certain environmental factors on photosynthesis and photorespiration Simmondsia chinensis. Planta 134:127–132.
  • Deslippe, J. R., and S. W. Simard. 2011. Below-ground carbon transfer among Betula nana may increase with warming in Arctic tundra. New Phytol. 162:689–698.
    Direct Link:
  • Deslippe, J. R., M. Hartmann, W. W. Mohn, and S. W. Simard. 2011. Long-term experimental manipulation of climate alters the ectomycorrhizal community of Betula nana in Arctic tundra. Glob. Change Biol. 17:1625–1636.
    Direct Link:
  • Elmendorf, S. C., G. H. R. Henry, R. D. Hollister, R.G. Bjork, A. D. Bjorkman, T. V. Callaghan, et al. 2012. Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecol. Lett. 15:164–175.
    Direct Link:
  • Fetcher, N. 1985. Effects of removal of neighboring species on growth, nutrients, and microclimate of Eriophorum vaginatum. Arct. Alp. Res. 17:7–17.
  • Gorham, E. 1991. Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol. Appl. 1:182–195.
  • Gough, L., and S. E. Hobbie. 2003. Responses of moist non-acidic arctic tundra to altered environment: productivity, biomass, and species richness. Oikos 103:204–216.
    Direct Link:
  • Gough, L., J. C. Moore, G. R. Shaver, R. T. Simpson, and D. R. Johnson. 2012. Above- and belowground responses of arctic tundra ecosystems to altered soil nutrients and mammalian herbivory. Ecology 93:1683–1694.
  • Griffin, K. L., and M. H. Turnbull. 2013 Light saturate RuBP oxygenation by Rubisco is a robust predictor of light inhibition of respiration in Triticum aestivum L. Plant Biol. In press.
    Direct Link:
  • Heskel, M. H., O. R. Anderson, O. K. Atkin, M. H. Turnbull, and K. L. Griffin. 2012. Leaf- and cell-level carbon cycling responses to a nitrogen and phosphorus gradient in two Arctic tundra species. Am. J. Bot. 99:1702–1714.
  • Hicks-Pries, C. E., E. A. G. Schuur, and K. G. Crummer. 2013. Thawing permafrost increases old soil and autotrophic respiration in tundra: partitioning ecosystem respiration using δ13C and Δ14C. Glob. Change Biol. 19:649–661.
    Direct Link:
  • Hobbie, S. E., and F. S. Chapin III. 1998. The response of tundra plant biomass, aboveground production, nitrogen, and CO2 flux to experimental warming. Ecology 79:1526–1544.
  • Hoefnagel, M. H. N., O. K. Atkin, and J. T. Wiskich. 1998. Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim. Biophys. Acta 1366:235–255.
  • Huemmrich, K. F., G. Kinoshita, J. A. Gamon, S. Houston, H. Kwon, and W. C. Oechel. 2010. Tundra carbon balance under varying temperature and moisture regimes. J. Geophys. Res., 115, G00I02.
    Direct Link:
  • Hurry, V., A. Igamberdiev, O. Keerberg, T. Pärnik, O. Atkin, J. Zaragoza-Castells, et al. 2005 Respiration in photosynthetic cells: gas exchange components, interactions with photorespiration and the operation of mitochondria in the light. Pp. 43–61 in H. Lambers and M. Ribas-Carbo, eds. Plant respiration. Springer, the Netherlands.
  • Kirschbaum, M. U. F., and G. D. Farquhar. 1987. Investigation of the CO2 dependence of quantum yield and respiration in Eucalyptus pauciflora. Plant Physiol. 83:1023–1036.
  • Kok, B. 1948. A critical consideration of the quantum yield of Chlorella-photosynthesis. Enzymologia 13:1–56.
  • Lambers, H., F. S. Chapin III, and T. Pons. 2008. Plant physiological ecology. Springer Science, New York, NY.
  • Leegood, R. C., and G. E. Edwards. 2004 Carbon metabolism and photorespiration: temperature dependence in relation to other environmental factors. Pp. 191–221 in N. R. Baker, ed. Photosynthesis and the environment. Springer, the Netherlands.
  • Leegood, R. C., P. J. Lea, M. D. Adcock, and R. E. Hausler. 1995. The regulation and control of photorespiration. J. Exp. Bot. 46:1397–1414.
  • Liston, G. E., J. P. Mcfadden, M. Sturm, and R. A. Pielke. 2002. Modelled changes in arctic tundra snow, energy and moisture fluxes due to increased shrubs. Glob. Change Biol. 8:17–32.
    Direct Link:
  • Mack, M. C., E. A. G. Schuur, M. S. Bret-Harte, G. R. Shaver, and F. S. Chapin III. 2004. Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431:440–443.
  • Mitchell, K. A., P. V. Bolstad, and J. M. Vose. 1999. Interspecific and environmentally induced variation in foliar dark respiration among eighteen southeastern deciduous tree species. Tree Physiol. 19:861–870.
  • Oberbauer, S. F., C. E. Tweedie, J. M. Welker, J. T. Fahnestock, G. H. R. Henry, P. J. Webber, et al. 2007. Tundra CO2 fluxes in response to experimental warming across latitudinal and moisture gradients. Ecol. Monogr. 77:221–238.
  • Oechel, W., S. Hastings, G. Vourlitis, and M. Jenkins. 1993. Recent change of Arctic tundra ecosystems from a net carbon dioxide sink to a source. Nature 361:520–523.
  • Onoda, Y., K. Hikosaka, and T. Hirose. 2004. Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Funct. Ecol. 18:419–425.
    Direct Link:
  • Pärnik, T., H. Ivanova, and O. Keerberg. 2007. Photorespiratory and respiratory decarboxylations in leaves of C3 plants under different CO2 concentrations and irradiances. Plant Cell Environ. 30:1535–1544.
    Direct Link:
  • Ping, C., G. Michaelson, and M. Jorgenson. 2008. High stocks of soil organic carbon in the North American Arctic region. Nat. Geosci. 1:615–619.
  • Pomeroy, J. W., D. S. Bewley, R. L. H. Essery, N. R. Hedstrom, T. Link, R. J. Granger, et al. 2006. Shrub tundra snowmelt. Hydrol. Process. 20:923–941.
    Direct Link:
  • Post, E., M. C. Forchhammer, M. S. Bret-Harte, T. V. Callaghan, T. R. Christensen, B. Elberling, et al. 2009. Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358.
  • Schimel, J. P., C. Bilbrough, and J. M. Welker. 2004. Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities. Soil Biol. Biochem. 36:217–227.
  • Shapiro, J. B., K. L. Griffin, J. D. Lewis, and D. T. Tissue. 2004. Response of Xanthium strumarium leaf respiration in the light to elevated CO2 concentration, nitrogen availability and temperature. New Phytol. 162:377–386.
    Direct Link:
  • Sharp, R. E., M. A. Matthews, and J. S. Boyer. 1984. Kok effect and the quantum yield of photosynthesis: light partially inhibits dark respiration. Plant Physiol. 75:95.
  • Shaver, G. R., and F. S. Chapin III. 1986. Effect of fertilizer on production and biomass of tussock tundra, Alaska, U.S.A. Arct. Alp. Res. 18:261–268.
  • Shaver, G. R., W. D. Billings, F. S. Chapin III, A. E. Giblin, K. J. Nadelhoffer, W. C. Oechel, et al. 1992. Global change and the carbon balance of arctic ecosystems. Bioscience 42:433–441.
  • Shaver, G. R., M. S. Bret-Harte, M. H. Jones, J. Johnstone, L. Gough, J. Laundre, et al. 2001. Species composition interacts with fertilizer to control long-term change in tundra productivity. Ecology 82:3163–3181.
  • Shaver, G. R., J. A. Laundre, M. S. Bret-Harte, F. S. Chapin III, A. E. Giblin, L. Gough, et al. 2013. Terrestrial ecosystems at Toolik Lake, Alaska. In press in J. E. Hobbie and G. W. Kling, eds. A changing arctic: ecological consequences for tundra, streams, and lakes. Oxford Univ. Press, Oxford, New York.
  • Street, L. E., G. R. Shaver, M. Williams, and M. T. Van Wijk. 2007. What is the relationship between changes in canopy leaf area and changes in photosynthetic CO2 flux in arctic ecosystems? J. Ecol. 95:139–150.
    Direct Link:
  • Sturm, M., C. Racine, and K. Tape. 2001. Climate change: increasing shrub abundance in the Arctic. Nature 411:546–547.
  • Sturm, M., T. Douglas, C. Racine, and G. E. Liston. 2005a. Changing snow and shrub conditions affect albedo with global implications. J. Geophys. Res. 110:G01004.
    Direct Link:
  • Sturm, M., J. Schimel, G. Michaelson, J. Welker, S. F. Oberbauer, G. E. Liston, et al. 2005b. Winter biological processes could help convert Arctic tundra to shrubland. Bioscience 55:17–26.
  • Sullivan, P., M. Sommerkorn, H. Rueth, K. Nadelhoffer, G. R. Shaver, and J. M. Welker. 2007. Climate and species affect fine root production with long-term fertilization in acidic tussock tundra near Toolik Lake, Alaska. Oecologia 153:643–652.
  • Takashima, T., K. Hikosaka, and T. Hirose. 2004. Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ. 27:1047–1054.
    Direct Link:
  • Tape, K., M. Sturm, and C. Racine. 2006. The evidence for shrub expansion in Northern Alaska and the Pan-Arctic. Glob. Change Biol. 12:686–702.
    Direct Link:
  • Tarnocai, C., J. G. Canadell, G. Schuur Ea, P. Kuhry, G. Mazhitova, and S. Zimov. 2009 Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochem. Cycles 23:GB2023.
    Direct Link:
  • Tcherkez, G., G. Cornic, R. Bligny, E. Gout, and J. Ghashghaie. 2005. In vivo respiratory metabolism of illuminated leaves. Plant Physiol. 138:1596–1606.
  • Tcherkez, G., R. Bligny, E. Gout, A. Mahe, M. Hodges, and G. Cornic. 2008. Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions. Proc. Natl. Acad. Sci. USA 105:797–802.
  • Templer, P. H., and A. B. Reinmann. 2011. Multi-factor global change experiments: what have we learned about terrestrial carbon storage and exchange? New Phytol. 192:797–800.
    Direct Link:
  • Tessier, J. T., and D. J. Raynal. 2003. Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. J. Appl. Ecol. 40:523–534.
    Direct Link:
  • Turnbull, M. H., D. Whitehead, D. T. Tissue, W. S. F. Schuster, K. J. Brown, and K. L. Griffin. 2003. Scaling foliar respiration in two contrasting forest canopies. Funct. Ecol. 17:101–114.
    Direct Link:
  • Van Wijk, M. T., and M. Williams. 2003. Interannual variability of plant phenology in tussock tundra: modelling interactions of plant productivity, plant phenology, snowmelt and soil thaw. Glob. Change Biol. 9:743–758.
    Direct Link:
  • Van Wijk, M. T., M. Williams, and G. R. Shaver. 2005. Tight coupling between leaf area index and foliage N content in arctic plant communities. Oecologia 142:421–427.
  • Walker, M. D., C. H. Wahren, R. D. Hollister, G. H. R. Henry, L. E. Alhquist, J. M. Alatalo, et al. 2006. Plant community responses to experimental warming across the tundra biome. Proc. Natl. Acad. Sci. USA 103:1342.
  • Wang, X., J. D. Lewis, D. T. Tissue, J. R. Seemann, and K. L. Griffin. 2001. Effects of elevated atmospheric CO2 concentration on leaf dark respiration of Xanthium strumarium in light and in darkness. Proc. Natl. Acad. Sci. USA 98:2479–2484.
  • Wein, R. W., and L. C. Bliss. 1974. Primary Production in Arctic Cottongrass Tussock Tundra Communities. Arct. Alp. Res. 6:261–274.
  • Weintraub, M. N., and J. P. Schimel. 2005. Nitrogen cycling and the spread of shrubs control changes in the carbon balance of Arctic tundra ecosystems. Bioscience 55:408–415.
  • Welker, J. M., J. T. Fahnestock, G. H. R. Henry, K. W. O'Dea, and R. A. Chimner. 2004. CO2 exchange in three Canadian High Arctic ecosystems: response to long-term experimental warming. Glob. Change Biol. 10:1981–1995.
    Direct Link:
  • Williams, M., and E. B. Rastetter. 1999. Vegetation characteristics and primary productivity along an arctic transect: implications for scaling-up. J. Ecol. 87:885–898.
    Direct Link:
  • Wookey, P. A., R. Aerts, R. D. Bardgett, F. Baptist, K. A. Brathen, J. H. C. Cornelissen, et al. 2009. Ecosystem feedbacks and cascade processes: understanding their role in the responses of Arctic and alpine ecosystems to environmental change. Glob. Change Biol. 15:1153–1172.
    Direct Link:
View Full Article with Supporting Information (HTML) Get PDF (623K)