Seasonality of foliar respiration in two dominant plant species from the Arctic tundra: Response to long-term warming and short-term temperature variability

Functional Plant Biology

Volumn 41, Issue 3, 2014, Pages 287-300

  Heskel, Mary A ^a,b   Bitterman, Danielle ^a   Atkin, Owen K ^b   Turnbull, Matthew H ^c   Griffin, Kevin L ^a,d  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c UNIVERSITY OF CANTERBURY   (New Zealand)

^d Department of Earth and Environmental Sciences   (United States)

Author keywords

Betula nana; Eriophorum vaginatum; Kok effect; photosynthesis; seasonality.

Indexed keywords

EID: 84893910737     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP13137     Document Type: Article

References (68)

1. Armstrong AF, Logan DC, Atkin OK (2006a) On the developmental dependence of leaf respiration: responses to short and long-term changes in growth temperature. American Journal of Botany 93, 1633-1639. doi:10.3732/ajb.93.11. 1633
2. Armstrong AF, Logan DC, Tobin AK, O'Toole P, Atkin OK (2006b) Heterogeneity of plant mitochondrial responses underpinning respiratory acclimation to the cold in Arabidopsis thaliana leaves. Plant, Cell & Environment 29, 940-949. doi:10.1111/j.1365-3040.2005. 01475.x
3. Armstrong AF, Badger MR, Day DA, Barthet MM, Smith P, Millar AH, Whelan J, Atkin OK (2008) Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration. Plant, Cell & Environment 31, 1156-1169. doi:10.1111/j.1365-3040.2008.01830.x
4. Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343-351. doi:10.1016/S1360-1385(03)00136-5
5. 10; values and acclimation. In 'Plant respiration'. (Eds H. Lambers & M. Ribas-Carbo), pp. 95-135. (Springer: Dordrecht, The Netherlands)
6. Atkin OK, Scheurwater I, Pons TL (2006) High thermal acclimation potential of both photosynthesis and respirationin two lowlandPlantago species in contrast to an alpine congeneric. Global Change Biology 12, 500-515. doi:10.1111/j.1365-2486.2006.01114.x
7. 2 and growth temperature.New Phytologist 190, 1003-1018. doi:10.1111/j.1469-8137.2011.03673.x
8. Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 31, 491-543. doi:10.1146/annurev.pp.31. 060180.002423
9. Bret-Harte MS, Shaver GR, Zoerner JP, Johnstone JF, Wagner JL, Chavez AS, Gunkelman RF IV, Lippert SC, Laundre JA (2001) Developmental plasticity allows Betula nana to dominate tundra subjected to an altered environment. Ecology 82, 18-32.
10. Bret-Harte MS, Shaver GR, Chapin FS III (2002) Primary and secondary stem growth in Arctic shrubs: implications for community response to environmental change. Journal of Ecology 90, 251-267. doi:10.1046/j.1365-2745.2001.00657.x
11. 3 species based on stoichiometric flux balance. Plant, Cell & Environment 34, 89-112. doi:10.1111/j.1365-3040.2010.02228.x
12. Budde RJ, Randall DD (1990) Pea leaf mitochondrial pyruvate dehydrogenase complex is inactivated in vivo in a light-dependent manner. Proceedings of the National Academy of Sciences of the United States of America 87, 673-676. doi:10.1073/pnas.87.2.673
13. Cahoon SMP, Sullivan PF, Shaver GR, Welker JM, Post E (2012) Interactions among shrub cover and the soil microclimate may determine future Arctic carbon budgets. Ecology Letters 15, 1415-1422. doi:10.1111/j.1461-0248.2012.01865.x
14. Chapin FS, Shaver GR (1996) Physiological and growth responses of Arctic plants to a field experiment simulating climatic change. Ecology 77, 822-840. doi:10.2307/2265504
15. Chapin FS, Shaver GR, Giblin AE, Nadelhoffer KJ, Laundre JA (1995) Responses of Arctic tundra to experimental and observed changes in climate. Ecology 76, 694-711. doi:10.2307/1939337
16. Chapin FS, Sturm M, Serreze MC, McFadden JP, Key JR, Lloyd AH, McGuire AD, Rupp TS, Lynch AH, Schimel JP, Beringer J, Chapman WL, Epstein HE, Euskirchen ES, Hinzman LD, Jia G, Ping C-L, Tape KD, Thompson CDC, Walker DA, Welker JM (2005) Role of land-surface changes in Arctic summer warming. Science 310, 657-660. doi:10.1126/science.1117368
17. Covey-Crump EM, Attwood RG, Atkin OK (2002) Regulation of root respiration in two species of Plantago that differ in relative growth rate: the effect of short and long term changes in temperature. Plant, Cell & Environment 25, 1501-1513. doi:10.1046/j.1365-3040.2002. 00932.x
18. 2 and summer drought. Plant, Cell & Environment 35, 966-981. doi:10.1111/j.1365-3040.2011.02465.x
19. Dungan RJ, Whitehead D, Duncan RP (2003) Seasonal and temperature dependence of photosynthesis and respiration for two co-occurring broad-leaved tree species with contrasting leaf phenology. Tree Physiology 23, 561-568. doi:10.1093/treephys/23.8.561
20. Elmendorf SC, Henry GHR, Hollister RD, Björk RG, Bjorkman AD, Callaghan TV, Collier LS, Cooper EJ, Cornelissen JHC, Day TA, Fosaa AM, Gould WA, Grétarsdóttir J, Harte J, Hermanutz L, Hik DS, Hofgaard A, Jarrad F, Jónsdóttir IS, Keuper F, Klanderud K, Klein JA, Koh S, Kudo G, Lang SI, Loewen V, May JL, Mercado J, Michelsen A, Molau U, Myers-Smith IH, Oberbauer SF, Pieper S, Post E, Rixen C, Robinson CH, Schmidt NM, Shaver GR, Stenström A, Tolvanen A, Totland Ø, Troxler T, Wahren C-H, Webber PJ, Welker JM, Wookey PA (2012) Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecology Letters 15, 164-175. doi:10.1111/j.1461-0248.2011.01716.x
21. Environmental Data Center Team (2011) Meteorological monitoringprogram at Toolik, Alaska. Toolik Field Station, Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK 99775. Available at http://toolik.alaska.edu/ edc/abiotic-monitoring/data-query.php
22. Fetcher N, Shaver GR (1983) Lifehistories of tillers of Eriophorumvaginatum in relation to tundra disturbance. Journal of Ecology 71, 131-147. doi:10.2307/2259967
23. Gough L, Hobbie SE (2003) Responses of moist non-acidic tundra to altered environment: productivity, biomass, and species richness. Oikos 103, 204-216. doi:10.1034/j.1600-0706.2003.12363.x
24. Heskel MA, Anderson OR, Atkin OK, Turnbull MH, Griffin KL(2012) Leaf-and cell-level carbon cycling responses to a nitrogen and phosphorus gradient in two Arctic tundra species. American Journal of Botany 99, 1702-1714. doi:10.3732/ajb.1200251
25. Heskel MA, Greaves HE, Kornfeld A, Gough L, Atkin OK, Turnbull MH, Shaver GR, Griffin KL (2013) Differential physiological responses to environmental change promote woody shrub expansion. Ecology and Evolution 3, 1149-1162. doi:10.1002/ece3.525
26. Hüve K, Bichele I, Ivanova H, Keerberg O, Pärnik T, Rasulov B, Tobias M, Niinemets Ü (2012) Temperatureresponsesofdark respirationinrelations to leaf sugar concentration. Physiologia Plantarum 144, 320-334. doi:10.1111/j.1399-3054.2011.01562.x
27. 2 dependence of quantum yield and respiration in Eucalyptus pauciflora. Plant Physiology 83, 1032-1036.
28. Kok B (1948) A critical consideration of the quantum yield of Chlorella-photosynthesis. Enzymologia 13, 1-56.
29. Korner C, Larcher W (1988) Plant lifeincoldclimates. Symposia of the Society for Experimental Biology 42, 25-57.
30. Kornfeld A, Heskel M, Atkin OK, Gough L, Griffin KL, Horton TW, Turnbull MH (2013) Respiratory flexibility and efficiency are affected by simulated global change in Arctic plants. New Phytologist 197, 1161-1172. doi:10.1111/nph.12083
31. Loranty M, Goetz S, Rastetter E, Rocha A, Shaver G, Humphreys E, Lafleur P (2011) Scaling an instantaneous model of tundra NEE to the Arctic landscape. Ecosystems 14, 76-93. doi:10.1007/s10021-010-9396-4
32. Mitchell KA, Bolstad PV, Vose JM (1999) Interspecific and environmentally induced variation in foliar dark respiration among eighteen southeastern deciduous tree species. Tree Physiology 19, 861-870. doi:10.1093/treephys/19.13. 861
33. Natali SM, Schuur EAG, Trucco C, Hicks-Pries CE, Crummer KG, Baron-Lopez AF (2011) Effects of experimental warming of air, soil and permafrost on carbon balance in Alaskan tundra. Global Change Biology 17, 1394-1407. doi:10.1111/j.1365-2486.2010.02303.x
34. O'Sullivan OS, Weerasinghe KWLK, Evans JR, Egerton JJG, Tjoelker MG, Atkin OK (2013) High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function. Plant, Cell & Environment 36, 1268-1284. doi:10.1111/pce.12057
35. Oberbauer SF, Starr G, Pop EW (1998) Effects of extended growing season and soil warming on carbon dioxide and methane exchange of tussock tundra in Alaska. Journal of Geophysical Research 103, 29075-29082. doi:10.1029/98JD00522
36. 2 fluxes in response to experimental warming across latitudinal and moisture gradients. Ecological Monographs 77, 221-238. doi:10.1890/06-0649
37. 2exchangeinthe Alaskan Arcticinresponse to decadal climate warming. Nature 406, 978-981. doi:10.1038/35023137
38. Ow LF, Whitehead D, Walcroft AS, Turnbull MH (2010) Seasonal variationin foliar carbon exchange in Pinus radiata and Populusdeltoides: respiration acclimates fully to changes in temperature but photosynthesis does not. Global Change Biology 16, 288-302. doi:10.1111/j.1365-2486.2009. 01892.x
39. Pomeroy JW, Bewley DS, Essery RLH, Hedstrom NR, Link T, Granger RJ, Sicart JE, Ellis CR, Janowicz JR (2006) Shrub tundra snowmelt. Hydrological Processes 20, 923-941. doi:10.1002/hyp.6124
40. Post E, Forchhammer MC, Bret-Harte MS, Callaghan TV, Christensen TR, Elberling B, Fox AD, Gilg O, Hik DS, Hoye TT, Ims RA, Jeppesen E, Klein DR, Madsen J, McGuire AD, Rysgaard Sr, Schindler DE, Stirling I, Tamstorf MP, Tyler NJC, van der Wal R, Welker J, Wookey PA, Schmidt NM, Aastrup P (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325, 1355-1358. doi:10.1126/science.1173113
41. 2 assimilation in sub-Arctic mountain birch (Betula pubescens ssp. czerepanovii (Orlova) Hamet-Ahti). Agricultural and Forest Meteorology 158-159, 90-100. doi:10.1016/j.agrformet. 2012.02.009
42. 2 exchange in Arctic tundra. Ecological Applications 21, 477-489. doi:10.1890/10-0255.1
43. 4 photosynthesis. Plant, Cell & Environment 30, 1086-1106. doi:10.1111/j.1365-3040.2007.01682.x
44. Searle SY, Thomas S, Griffin KL, Horton T, Kornfeld A, Yakir D, Hurry V, Turnbull MH (2011) Leaf respiration and alternative oxidase in field-grown alpine grasses respond to natural changes in temperature and light. New Phytologist 189, 1027-1039. doi:10.1111/j.1469-8137. 2010.03557.x
45. Serreze MC, Walsh JE, Chapin FS, Osterkamp T, Dyurgerov M, Romanovsky V, Oechel WC, Morison J, Zhang T, Barry RG (2000) Observational evidence of recent change in the northern high-latitude environment. Climatic Change 46, 159-207. doi:10.1023/A:1005504 031923
46. Shapiro JB, Griffin KL, Lewis JD, Tissue DT (2004) Response of Xanthium strumarium leaf respiration in the light to elevated CO2 concentration, nitrogen availability and temperature. New Phytologist 162, 377-386. doi:10.1111/j.1469-8137.2004.01046.x
47. Sharkey TD, Bernacchi CJ, Farquhar GD, Singaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell and Environment 30, 1035-1040. doi:10.1111/j.1365-3040.2007. 01710.x
48. Shaver GR, Billings WD, Chapin FS, Giblin AE, Nadelhoffer KJ, Oechel WC, Rastetter EB (1992) Global change and the carbon balance of arctic ecosystems. Bioscience 42, 433-441. doi:10.2307/1311862
49. 2 flux in wet sedge tundras: responses to nutrients, temperature, and light. Ecological Monographs 68, 75-97.
50. Shaver GR, Canadell J, Chapin FS, Gurevitch J, Harte J, Henry G, Ineson P, Jonasson S, Melillo J, Pitelka L, Rustad L (2000) Global warming and terrestrial ecosystems: a conceptual framework for analysis. Bioscience 50, 871-882. doi:10.1641/0006-3568(2000)050[0871:GWATEA]2.0. CO;2
51. Starr G, Oberbauer SF, Ahlquist LE (2008) The photosynthetic response of Alaskantundra plantstoincreased season length and soil warming.Arctic, Antarctic, and Alpine Research40, 181-191. doi:10.1657/1523-0430(06-015)[STARR] 2.0.CO;2
52. Stone RS, Dutton EG, Harris JM, Longenecker D (2002) Earlier spring snowmelt in northern Alaska as an indicator of climate change. Journal of Geophysical Research: Atmospheres 107, 4089. doi:10.1029/2000JD000286
53. Sullivan P, Sommerkorn M, Rueth H, Nadelhoffer K, Shaver G, Welker J (2007) Climate and species affect fine root production with long-term fertilization in acidic tussock tundra near Toolik Lake, Alaska. Oecologia 153, 643-652. doi:10.1007/s00442-007-0753-8
54. Sullivan P, Arens S, Chimner R, Welker J (2008) Temperature and microtopography interact to control carbon cycling in a high Arctic fen. Ecosystems 11, 61-76. doi:10.1007/s10021-007-9107-y
55. Tcherkez G, Cornic G, Bligny R, Gout E, Ghashghaie J (2005) In vivo respiratory metabolism of illuminated leaves. Plant Physiology 138, 1596-1606. doi:10.1104/pp.105.062141
56. 2 conditions. Proceedings of the National Academy of Sciences of the United States of America 105, 797-802. doi:10.1073/pnas.0708947105
57. Tcherkez G, Mahe A, Gauthier P, Mauve C, Gout E, Bligny R, Cornic G, Hodges M (2009) In folio respiratory fluxomics revealed by 13C isotopic labeling and H/D isotope effects highlight the noncyclic nature of the tricarboxylic acid "cycle" in illuminated leaves. Plant Physiology 151, 620-630. doi:10.1104/pp.109.142976
58. Tissue DT, Lewis JD, Wullschleger SD, Amthor JS, Griffin KL, Anderson OR (2002) Leaf respiration at different canopy positions in sweetgum (Liquidambar styraciflua) grown in ambient and elevated concentrations of carbon dioxide in the field. Tree Physiology 22, 1157-1166. doi:10.1093/treephys/22.15-16.1157
59. Turnbull MH, Whitehead D, Tissue DT, Schuster WSF, Brown KJ, Griffin KL (2003) Scaling foliar respiration in two contrasting forest canopies. Functional Ecology 17, 101-114. doi:10.1046/j.1365-2435.2003. 00713.x
60. Vose J, Ryan M (2002) Seasonal respiration of foliage, fine roots, and woody tissues in relationto growth, tissue N, and photosynthesis. Global Change Biology 8, 182-193. doi:10.1046/j.1365-2486.2002.00464.x
61. 2 and energy fluxes of an Alaskan tussock tundra ecosystem. Ecology 80, 686-701. doi:10.1890/0012-9658(1999)080[0686:ECMOCA]2.0.CO;2
62. 2 flux, respiration and gross primary production of Arctic tundra ecosystems. Functional Ecology 14, 203-214. doi:10.1046/j.1365-2435.2000.00419.x
63. 2 concentration on leaf dark respiration of Xanthium strumarium in light and in darkness. Proceedings of the National Academy of Sciences of the United States of America 98, 2479-2484. doi:10.1073/pnas.051622998
64. 2 flux in dry and moist Arctic tundra: field responses to increases in summer temperatures and winter snow depth. Climatic Change 44, 139-150. doi:10.1023/A:1005555012742
65. 2 exchange in three Canadian high Arctic ecosystems: response to long-term experimental warming. Global Change Biology 10, 1981-1995. doi:10.1111/j.1365-2486.2004.00857.x
66. Wookey PA, Aerts R, Bardgett RD, Baptist F, Brathen KA, Cornelissen JHC, Gough L, Hartley IP, Hopkins DW, Lavorel S, Shaver GR (2009) Ecosystem feedbacks and cascade processes: understanding their role in the responsesofArctic and alpine ecosystemstoenvironmental change. Global Change Biology 15, 1153-1172. doi:10.1111/j.1365-2486.2008. 01801.x
67. Xu LK, Baldocchi DD (2003) Seasonal trends in photosynthetic parameters and stomatal conductance of blue oak (Quercus douglasii) under prolonged summer drought and high temperature. Tree Physiology 23, 865-877. doi:10.1093/treephys/ 23.13.865
68. Xu C, Schuster W, Griffin KL (2007) Seasonal variation of temperature response of respiration in invasive Berberis thunbergii (Japanese barberry) and two co-occurring native understory shrubs in a northeasternUSdeciduous forest. Oecologia153, 809-819. doi:10.1007/s00442-007-0790-3