Skip to main content
SpringerLink
Log in

Are winter-active species vulnerable to climate warming? A case study with the wintergreen terrestrial orchid, Tipularia discolor

  • Global change ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

In the eastern United States, winter temperature has been increasing nearly twice as fast as summer temperature, but studies of warming effects on plants have focused on species that are photosynthetically active in summer. The terrestrial orchid Tipularia discolor is leafless in summer and acquires C primarily in winter. The optimum temperature for photosynthesis in T. discolor is higher than the maximum temperature throughout most of its growing season, and therefore growth can be expected to increase with warming. Contrary to this hypothesis, experimental warming negatively affected reproductive fitness (number of flowering stalks, flowers, fruits) and growth (change in leaf area from 2010 to 2012) in T. discolor. Temperature in June–July was critical for flowering, and mean July temperature greater than 29 °C (i.e., 2.5 °C above ambient) eliminated reproduction. Warming of 1.2 °C delayed flowering by an average of 10 days and fruiting by an average of 5 days. Warming of 4.4 °C reduced relative growth rates by about 60 %, which may have been partially caused by the direct effects of temperature on photosynthesis and respiration. Warming indirectly increased vapor pressure deficit (VPD) by 0.2–0.5 kPa, and leaf-to-air VPD over 1.3 kPa restricted stomatal conductance of T. discolor to 10–40 % of maximum conductance. These results highlight the need to account for changes in VPD when estimating temperature responses of plant species under future warming scenarios. Increasing temperature in the future will likely be an important limiting factor to the distribution of T. discolor, especially along the southern edge of its range.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adams MS (1970) Adaptations of Aplectrum hyemale to environment: effects of preconditioning temperature on net photosynthesis. Bull Torrey Bot Club 97:219–224

    Article  Google Scholar 

  • Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M, Diemer M, Gugerli F, Henry GHR, Jones MH, Hollister RD, Jonsdottir IS, Laine K, Levesque E, Marion GM, Molau U, Molgaard P, Nordenhall U, Raszhivin V, Robinson CH, Starr G, Stenstrom A, Stenstrom M, Totland O, Turner PL, Walker LJ, Webber PJ, Welker JM, Wookey PA (1999) Responses of tundra plants to experimental warming: meta-analysis of the international tundra experiment. Ecol Monogr 69:491–511

    Google Scholar 

  • Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351

    Article  CAS  PubMed  Google Scholar 

  • Atkin OK, Holly C, Ball MC (2000) Acclimation of snow gum (Eucalyptus pauciflora) leaf respiration to seasonal and diurnal variations in temperature: the importance of changes in the capacity and temperature sensitivity of respiration. Plant Cell Environ 23:15–26

    Article  Google Scholar 

  • Atkin OK, Scheurwater I, Pons TL (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

    Article  Google Scholar 

  • Badri MA, Minchin PEH, Lapointe L (2007) Effects of temperature on the growth of spring ephemerals: crocus vernus. Physiol Plant 130:67–76

    Article  CAS  Google Scholar 

  • Bernatchez A, Lapointe L (2012) Cooler temperatures favour growth of wild leek (Allium tricoccum), a deciduous forest spring ephemeral. Botany 90:1125–1132

    Article  CAS  Google Scholar 

  • Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol Plant Mol Biol 31:491–543

    Article  Google Scholar 

  • Blanchard MG, Runkle ES (2006) Temperature during the day, but not during the night, controls flowering of Phalaenopsis orchids. J Exp Bot 57:4043–4049

    Article  CAS  PubMed  Google Scholar 

  • Boyles RP, Raman S (2003) Analysis of climate trends in North Carolina (1949-1998). Environ Int 29:263–275

    Article  PubMed  Google Scholar 

  • Bradley NL, Leopold AC, Ross J, Huffaker W (1999) Phenological changes reflect climate change in Wisconsin. Proc Natl Acad Sci USA 96:9701–9704

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brown PM (1997) Wild orchids of the Northeastern United States. Cornell University Press, Ithaca

    Google Scholar 

  • Callahan P, Chapin JB (1960) Morphology of the reproductive systems and mating in two representative members of the family Noctuidae, Pseudaletia unipuncta and Peridroma margaritosa, with comparison to Heliothis zea. Ann Entomol Soc Am 53:763–782

    Google Scholar 

  • Coile NC, Garland MA (2003) Notes on Florida’s endangered and threatened plants, botany contribution no 38, 4th edn. Florida Department of Agriculture and Consumer Services, Division of Plant Industry, Gainesville

  • Day ME (2000) Influence of temperature and leaf-to-air vapor pressure deficit on net photosynthesis and stomatal conductance in red spruce (Picea rubens). Tree Physiol 20:57–63

    Article  PubMed  Google Scholar 

  • De Frenne P, Brunet J, Shevtsova A, Kolb A, Graae BJ, Chabrerie O, Cousins SA, Decocq G, De Schrijver A, Diekmann M, Gruwez R, Heinken T, Hermy M, Nilsson C, Stanton S, Tack W, Willaert J, Verheyen K (2011) Temperature effects on forest herbs assessed by warming and transplant experiments along a latitudinal gradient. Glob Change Biol 17:3240–3253

    Article  Google Scholar 

  • Dorji T, Totland Ã, Moe SR, Hopping KA, Pan J, Klein JA (2013) Plant functional traits mediate reproductive phenology and success in response to experimental warming and snow addition in Tibet. Glob Change Biol 19:459–472

    Article  Google Scholar 

  • Dormann CF, Woodin SJ (2002) Climate change in the Arctic: using plant functional types in a meta-analysis of field experiments. Funct Ecol 16:4–17

    Article  Google Scholar 

  • Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73:69–86

    Article  Google Scholar 

  • Duursma RA, Payton P, Bange MP, Broughton KJ, Smith RA, Medlyn BE, Tissue DT (2013) Near-optimal response of instantaneous transpiration efficiency to vapour pressure deficit, temperature and CO2 in cotton (Gossypium hirsutum L.). Agric For Meteorol 168:168–176

    Article  Google Scholar 

  • Ehleringer JR (1991) 13C/12C fractionation and its utility in terrestrial plant studies. In: Coleman D, Fry B (eds) Carbon isotope techniques. Chapman and Hall, New York, pp 187–200

    Chapter  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  PubMed  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537

    Article  CAS  Google Scholar 

  • Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Díaz-Espejo A, Berry JA, Cifre J, Galmes J, Kaidenhoff R, Medrano H, Ribas-Carbo M (2007) Analysis of leakage in IRGA’s leaf chambers of open gas exchange systems: quantification and its effects in photosynthesis parameterization. J Exp Bot 58:1533–1543

    Article  CAS  PubMed  Google Scholar 

  • Frye CT (1993) Population genetics and ecology of the clonal orchid Tipularia discolor (Pursh) Nutt. (Orchidaceae). Master’s thesis, Wake Forest University, Winston-Salem

  • Gandin A, Gutjahr S, Dizengremel P, Lapointe L (2011) Source-sink imbalance increases with growth temperature in the spring geophyte Erythronium americanum. J Exp Bot 62:3467–3479

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guppy JC (1969) Some effects of temperature on immature stages of armyworm, Pseudaletia unipuncta (Lepidoptera–Noctuidae), under controlled conditions. Can Entomol 101:1320–1327

    Article  Google Scholar 

  • Hegland SJ, Nielsen A, Lazaro A, Bjerknes AL, Totland O (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett 12:184–195

    Article  PubMed  Google Scholar 

  • Hoffmann WA, Poorter H (2002) Avoiding bias in calculations of relative growth rate. Ann Bot 90:37–42

    Article  PubMed  Google Scholar 

  • Hollister RD, Webber PJ, Bay C (2005) Plant response to temperature in northern Alaska: implications for predicting vegetation change. Ecology 86:1562–1570

    Article  Google Scholar 

  • Karl TR, Melillo JM, Peterson TC (2009) Global climate change impacts in the United States. US Global change research program. Cambridge University Press, New York

    Google Scholar 

  • Kattge J, Knorr W (2007) Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. Plant Cell Environ 30:1176–1190

    Article  CAS  PubMed  Google Scholar 

  • Klady RA, Henry GHR, Lemay V (2011) Changes in high arctic tundra plant reproduction in response to long-term experimental warming. Glob Change Biol 17:1611–1624

    Article  Google Scholar 

  • Lapointe L (2001) How phenology influences physiology in deciduous forest spring ephemerals. Physiol Plant 113:151–157

    Article  CAS  PubMed  Google Scholar 

  • Lapointe L, Lerat S (2006) Annual growth of the spring ephemeral Erythronium americanum as a function of temperature and mycorrhizal status. Can J Bot 84:39–48

    Article  CAS  Google Scholar 

  • Lawrimore JH, Menne MJ, Gleason BE, Williams CN, Wuertz DB, Vose RS, Rennie J (2011) An overview of the global historical climatology network monthly mean temperature data set, version 3. J Geophys Res Atmos 116

  • Liu H, Feng CL, Luo YB, Chen BS, Wang ZS, Gu HY (2010) Potential challenges of climate change to orchid conservation in a wild orchid hotspot in southwestern China. Bot Rev 76:174–192

    Article  Google Scholar 

  • Lynch IP (2006) The Duke Forest at 75: a resource for all seasons. Office of the Duke Forest, Durham

    Google Scholar 

  • Marchin RM (2013) Using a physiological approach to improve predictions of climate change effects on temperate forests. PhD dissertation, Department of Plant Biology, North Carolina State University

  • McLaughlin RE (1962) Effect of temperature upon larval mortality of armyworm, Pseudaletia unipuncta (Haworth). J Insect Pathol 4:279

    Google Scholar 

  • Menzel A, Sparks TH, Estrella N, Roy DB (2006) Altered geographic and temporal variability in phenology in response to climate change. Glob Ecol Biogeogr 15:498–504

    Article  Google Scholar 

  • Molnar AV, Tokolyi J, Vegvari Z, Sramko G, Sulyok J, Barta Z (2012) Pollination mode predicts phenological response to climate change in terrestrial orchids: a case study from central Europe. J Ecol 100:1141–1152

    Article  Google Scholar 

  • Monteith JL (1995) A reinterpretation of stomatal responses to humidity. Plant Cell Environ 18:357–364

    Article  Google Scholar 

  • Newton LA, Runkle ES (2009) High-temperature inhibition of flowering of Phalaenopsis and Doritaenopsis orchids. Hortic Sci 44:1271–1276

    Google Scholar 

  • NOAA (2012) State of the climate: national overview for February 2012, vol. 2013. NOAA National Climatic Data Center

  • Oishi AC, Oren R, Stoy PC (2008) Estimating components of forest evapotranspiration: a footprint approach for scaling sap flux measurements. Agric For Meteorol 148:1719–1732

    Article  Google Scholar 

  • Oren R, Sperry JS, Katul GG, Pataki DE, Ewers BE, Phillips N, Schafer KVR (1999) Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant Cell Environ 22:1515–1526

    Article  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  CAS  PubMed  Google Scholar 

  • Pelini SL, Bowles FP, Ellison AM, Gotelli NJ, Sanders NJ, Dunn RR (2011) Heating up the forest: open-top chamber warming manipulation of arthropod communities at Harvard and Duke Forests. Methods Ecol Evol 2:534–540

    Article  Google Scholar 

  • Pfeifer M, Wiegand K, Heinrich W, Jetschke G (2006) Long-term demographic fluctuations in an orchid species driven by weather: implications for conservation planning. J Appl Ecol 43:313–324

    Article  Google Scholar 

  • Posé D, Verhage L, Ott F, Yant L, Mathieu J, Angenent GC, Immink RGH, Schmid M (2013) Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature 503:414–417

    Article  PubMed  Google Scholar 

  • Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214

    Article  Google Scholar 

  • Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562

    Article  Google Scholar 

  • Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Sherry RA, Zhou XH, Gu SL, Arnone JA, Schimel DS, Verburg PS, Wallace LL, Luo YQ (2007) Divergence of reproductive phenology under climate warming. Proc Natl Acad Sci USA 104:198–202

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Skillman JB (1994) Environmental effects on photosynthesis and photoinhibition in evergreen perennials native to a seasonal habitat. PhD dissertation, Duke University, Durham

  • Smith NG, Dukes JS (2013) Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO2. Glob Change Biol 19:45–63

    Article  Google Scholar 

  • Smith JL, Hunter KL, Hunter RB (2002) Genetic variation in the terrestrial orchid Tipularia discolor. Southeast Nat 1:17–26

    Article  Google Scholar 

  • Snow AA, Whigham DF (1989) Costs of flower and fruit production in Tipularia discolor (Orchidaceae). Ecology 70:1286–1293

    Article  Google Scholar 

  • Sparks TH, Jeffree EP, Jeffree CE (2000) An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK. Int J Biometeorol 44:82–87

    Article  CAS  PubMed  Google Scholar 

  • Swarts ND, Dixon KW (2009) Terrestrial orchid conservation in the age of extinction. Ann Bot 104:543–556

    Article  PubMed Central  PubMed  Google Scholar 

  • Tissue DT, Skillman JB, McDonald EP, Strain BR (1995) Photosynthesis and carbon allocation in Tipularia discolor (Orchidaceae), a wintergreen understory herb. Am J Bot 82:1249–1256

    Article  Google Scholar 

  • Totland Ø, Alatalo JM (2002) Effects of temperature and date of snowmelt on growth, reproduction, and flowering phenology in the arctic/alpine herb, Ranunculus glacialis. Oecologia 133:168–175

    Article  Google Scholar 

  • Trenberth KE, Fasullo J, Smith L (2005) Trends and variability in column-integrated atmospheric water vapor. Clim Dyn 24:741–758

    Article  Google Scholar 

  • Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol 30:669–688

    Article  PubMed  Google Scholar 

  • Way DA, Sage RF (2008) Elevated growth temperatures reduce the carbon gain of black spruce [Picea mariana (Mill.) B.S.P.]. Glob Change Biol 14:624–636

    Article  Google Scholar 

  • Went FW (1953) The effect of temperature on plant growth. Annu Rev Plant Physiol Plant Mol Biol 4:347–362

    Article  Google Scholar 

  • Whigham DF (1984) Biomass and nutrient allocation of Tipularia discolor (Orchidaceae). Oikos 42:303–313

    Article  CAS  Google Scholar 

  • Whigham DF, McWethy M (1980) Studies on the pollination ecology of Tipularia discolor (Orchidaceae). Am J Bot 67:550–555

    Article  Google Scholar 

  • Will RE, Wilson SM, Zou CB, Hennessey TC (2013) Increased vapor pressure deficit due to higher temperature leads to greater transpiration and faster mortality during drought for tree seedlings common to the forest-grassland ecotone. New Phytol 200:366–374

    Article  PubMed  Google Scholar 

  • Wu ZT, Dijkstra P, Koch GW, Penuelas J, Hungate BA (2011) Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Glob Change Biol 17:927–942

    Article  Google Scholar 

  • Yamasaki T, Yamakawa T, Yamane Y, Koike H, Satoh K, Katoh S (2002) Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in winter wheat. Plant Physiol 128:1087–1097

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119:101–117

    Article  CAS  PubMed  Google Scholar 

  • Yu HY, Luedeling E, Xu JC (2010) Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. Proc Natl Acad Sci USA 107:22151–22156

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zimmerman JK (1990) Role of pseudobulbs in growth and flowering of Catasetum viridiflavum (Orchidaceae). Am J Bot 77:533–542

    Article  Google Scholar 

  • Zimmerman JK, Whigham DF (1992) Ecological functions of carbohydrates stored in corms of Tipularia discolor (Orchidaceae). Funct Ecol 6:575–581

    Article  Google Scholar 

Download references

Acknowledgments

We thank Mark Boudreau and Lauren Nichols for maintaining the experimental site and Jesse Nippert for processing the C isotope data. The Hoffmann lab group, three anonymous reviewers, and Joy Ward provided helpful comments on the manuscript. The experimental warming site is funded by a US DOE PER award (DE-FG02-08ER64510) to R. R. Dunn, A. M. Ellison, N. J. Gotelli, and N. J. Sanders. This study was funded by the National Institute of Climate Change Research (NICCR-DE-FC02-06ER64156), and this publication was developed under STAR Fellowship Assistance Agreement no. F09A10379 awarded by the US Environmental Protection Agency (EPA). It has not been formally reviewed by EPA. The views expressed in this publication are solely those of R. M. Marchin, and EPA does not endorse any products or commercial services mentioned in this publication.

Author information

Authors and Affiliations

  1. Centre for Carbon, Water and Food, University of Sydney, Camden, NSW, 2570, Australia

    Renée M. Marchin

  2. Department of Plant Biology, North Carolina State University, Raleigh, NC, 27695-7612, USA

    Renée M. Marchin & William A. Hoffmann

  3. Department of Biological Sciences and Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC, 27695-7617, USA

    Robert R. Dunn

Authors
  1. Renée M. Marchin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert R. Dunn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William A. Hoffmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Renée M. Marchin.

Additional information

Communicated by Joy K. Ward.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 452 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Marchin, R.M., Dunn, R.R. & Hoffmann, W.A. Are winter-active species vulnerable to climate warming? A case study with the wintergreen terrestrial orchid, Tipularia discolor . Oecologia 176, 1161–1172 (2014). https://doi.org/10.1007/s00442-014-3074-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-3074-8

Keywords

Search

Navigation