Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

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

Mary A. Heskel A B E , Danielle Bitterman A , Owen K. Atkin B , Matthew H. Turnbull C and Kevin L. Griffin A D
+ Author Affiliations
- Author Affiliations

A Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, NY 10027, USA.

B Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.

C School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8041, New Zealand.

D Department of Earth and Environmental Sciences, Lamont-Doherty Earth Observatory, Columbia University, Palisades, NY 10964-8000, USA.

E Corresponding author. Email: mary.heskel@anu.edu.au

Functional Plant Biology 41(3) 287-300 https://doi.org/10.1071/FP13137
Submitted: 9 May 2013  Accepted: 22 September 2013   Published: 31 October 2013

Abstract

Direct measurements of foliar carbon exchange through the growing season in Arctic species are limited, despite the need for accurate estimates of photosynthesis and respiration to characterise carbon cycling in the tundra. We examined seasonal variation in foliar photosynthesis and respiration (measured at 20°C) in two field-grown tundra species, Betula nana L. and Eriophorum vaginatum L., under ambient and long-term warming (LTW) conditions (+5°C), and the relationship of these fluxes to intraseasonal temperature variability. Species and seasonal timing drove most of the variation in photosynthetic parameters (e.g. gross photosynthesis (Agross)), respiration in the dark (Rdark) and light (Rlight), and foliar nitrogen concentration. LTW did not consistently influence fluxes through the season but reduced respiration in both species. Alongside the flatter respiratory response to measurement temperature in LTW leaves, this provided evidence of thermal acclimation. The inhibition of respiration by light increased by ~40%, with Rlight : Rdark values of ~0.8 at leaf out decreasing to ~0.4 after 8 weeks. Though LTW had no effect on inhibition, the cross-taxa seasonal decline in Rlight : Rdark greatly reduced respiratory carbon loss. Values of Rlight : Agross decreased from ~0.3 in both species to ~0.15 (B. nana) and ~0.05 (E. vaginatum), driven by decreases in respiratory rates, as photosynthetic rates remained stable. The influence of short-term temperature variability did not exhibit predictive trends for leaf gas exchange at a common temperature. These results underscore the influence of temperature on foliar carbon cycling, and the importance of respiration in controlling seasonal carbon exchange.

Additional keywords: Betula nana, Eriophorum vaginatum, Kok effect, photosynthesis, seasonality.


References

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.
On the developmental dependence of leaf respiration: responses to short and long-term changes in growth temperature.Crossref | GoogleScholarGoogle Scholar | 21642108PubMed |

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.
Heterogeneity of plant mitochondrial responses underpinning respiratory acclimation to the cold in Arabidopsis thaliana leaves.Crossref | GoogleScholarGoogle Scholar |

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.
Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSgt7rJ&md5=8adf64f1b0f3e2442ac3fff636d08cfdCAS |

Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343–351.
Thermal acclimation and the dynamic response of plant respiration to temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1CjtLk%3D&md5=9f04e0b89109b04172cb710701d9678dCAS | 12878019PubMed |

Atkin OK, Bruhn D, Tjoelker MG (2005) Response of plant respiration to changes in temperature: mechanisms and consequences of variations in Q10; values and acclimation. In ‘Plant respiration’. (Eds H. Lambers & M. Ribas-Carbo), pp. 95–135. (Springer: Dordrecht, The Netherlands)

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. Global Change Biology 12, 500–515.
High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric.Crossref | GoogleScholarGoogle Scholar |

Ayub G, Smith RA, Tissue DT, Atkin OK (2011) Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature. New Phytologist 190, 1003–1018.
Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature.Crossref | GoogleScholarGoogle Scholar | 21434926PubMed |

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.
Photosynthetic response and adaptation to temperature in higher plants.Crossref | GoogleScholarGoogle Scholar |

Bret-Harte MS, Shaver GR, Zoerner JP, Johnstone JF, Wagner JL, Chavez AS, Gunkelman RF, Lippert SC, Laundre JA (2001) Developmental plasticity allows Betula nana to dominate tundra subjected to an altered environment. Ecology 82, 18–32.

Bret-Harte MS, Shaver GR, Chapin FS (2002) Primary and secondary stem growth in Arctic shrubs: implications for community response to environmental change. Journal of Ecology 90, 251–267.
Primary and secondary stem growth in Arctic shrubs: implications for community response to environmental change.Crossref | GoogleScholarGoogle Scholar |

Buckley TN, Adams MA (2011) An analytical model of non-photorespiratory CO2 release in the light and dark in leaves of C3 species based on stoichiometric flux balance. Plant, Cell & Environment 34, 89–112.
An analytical model of non-photorespiratory CO2 release in the light and dark in leaves of C3 species based on stoichiometric flux balance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Gnurc%3D&md5=bfe056aa6cc153f525bfea164da04c41CAS |

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.
Pea leaf mitochondrial pyruvate dehydrogenase complex is inactivated in vivo in a light-dependent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhtFGrtLY%3D&md5=5785039f9d94ec94af6ebd1d2452cbd5CAS | 11607058PubMed |

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.
Interactions among shrub cover and the soil microclimate may determine future Arctic carbon budgets.Crossref | GoogleScholarGoogle Scholar |

Chapin FS, Shaver GR (1996) Physiological and growth responses of Arctic plants to a field experiment simulating climatic change. Ecology 77, 822–840.
Physiological and growth responses of Arctic plants to a field experiment simulating climatic change.Crossref | GoogleScholarGoogle Scholar |

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.
Responses of Arctic tundra to experimental and observed changes in climate.Crossref | GoogleScholarGoogle Scholar |

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.
Role of land-surface changes in Arctic summer warming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFChsLvL&md5=f70a754fb731dd779754a3048965f16cCAS | 16179434PubMed |

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.
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.Crossref | GoogleScholarGoogle Scholar |

Crous KY, Zaragoza-Castells J, Ellsworth DS, Duursma RA, Low M, Tissue DT, Atkin OK (2012) Light inhibition of leaf respiration in field-grown Eucalyptus saligna in whole-tree chambers under elevated atmospheric CO2 and summer drought. Plant, Cell & Environment 35, 966–981.
Light inhibition of leaf respiration in field-grown Eucalyptus saligna in whole-tree chambers under elevated atmospheric CO2 and summer drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosFSqsb4%3D&md5=52f530b252be135ff82c559f819a4c99CAS |

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.
Seasonal and temperature dependence of photosynthesis and respiration for two co-occurring broad-leaved tree species with contrasting leaf phenology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVyhtro%3D&md5=0d55e02e5177cf024fe1fe9c110c37d3CAS | 12730048PubMed |

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.
Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time.Crossref | GoogleScholarGoogle Scholar | 22136670PubMed |

Environmental Data Center Team (2011) Meteorological monitoring program 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

Fetcher N, Shaver GR (1983) Life histories of tillers of Eriophorum vaginatum in relation to tundra disturbance. Journal of Ecology 71, 131–147.
Life histories of tillers of Eriophorum vaginatum in relation to tundra disturbance.Crossref | GoogleScholarGoogle Scholar |

Gough L, Hobbie SE (2003) Responses of moist non-acidic tundra to altered environment: productivity, biomass, and species richness. Oikos 103, 204–216.
Responses of moist non-acidic tundra to altered environment: productivity, biomass, and species richness.Crossref | GoogleScholarGoogle Scholar |

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.
Leaf- and cell-level carbon cycling responses to a nitrogen and phosphorus gradient in two Arctic tundra species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVSnt7nJ&md5=30a59efe882c5dec54e11b0dcaffd74eCAS | 22984095PubMed |

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.
Differential physiological responses to environmental change promote woody shrub expansion.Crossref | GoogleScholarGoogle Scholar |

Hüve K, Bichele I, Ivanova H, Keerberg O, Pärnik T, Rasulov B, Tobias M, Niinemets Ü (2012) Temperature responses of dark respiration in relations to leaf sugar concentration. Physiologia Plantarum 144, 320–334.
Temperature responses of dark respiration in relations to leaf sugar concentration.Crossref | GoogleScholarGoogle Scholar | 22188403PubMed |

Kirschbaum MUF, Farquhar GD (1987) Investigation of the CO2 dependence of quantum yield and respiration in Eucalyptus pauciflora. Plant Physiology 83, 1032–1036.

Kok B (1948) A critical consideration of the quantum yield of Chlorella-photosynthesis. Enzymologia 13, 1–56.

Korner C, Larcher W (1988) Plant life in cold climates. Symposia of the Society for Experimental Biology 42, 25–57.

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.
Respiratory flexibility and efficiency are affected by simulated global change in Arctic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVOju7o%3D&md5=c7794e488279a11472e52163ab35c801CAS | 23278298PubMed |

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.
Scaling an instantaneous model of tundra NEE to the Arctic landscape.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOqs7Y%3D&md5=dd359270bf4583162bff4869203ed15dCAS |

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.
Interspecific and environmentally induced variation in foliar dark respiration among eighteen southeastern deciduous tree species.Crossref | GoogleScholarGoogle Scholar | 10562403PubMed |

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.
Effects of experimental warming of air, soil and permafrost on carbon balance in Alaskan tundra.Crossref | GoogleScholarGoogle Scholar |

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.
High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function.Crossref | GoogleScholarGoogle Scholar |

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, 29 075–29 082.
Effects of extended growing season and soil warming on carbon dioxide and methane exchange of tussock tundra in Alaska.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotFGqsLs%3D&md5=02c7be661c0d4f5ddd4c819d42ef2692CAS |

Oberbauer SF, Tweedie CE, Welker JM, Fahnestock JT, Henry GHR, Webber PJ, Hollister RD, Walker MD, Kuchy A, Elmore E, Starr G (2007) Tundra CO2 fluxes in response to experimental warming across latitudinal and moisture gradients. Ecological Monographs 77, 221–238.
Tundra CO2 fluxes in response to experimental warming across latitudinal and moisture gradients.Crossref | GoogleScholarGoogle Scholar |

Oechel W, Vourlitis G, Hastings S, Zulueta R, Hinzman L, Kane D (2000) Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming. Nature 406, 978–981.
Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtlKqsbg%3D&md5=a0d8d57a3f54ae539e93207e8d9544c9CAS | 10984048PubMed |

Ow LF, Whitehead D, Walcroft AS, Turnbull MH (2010) Seasonal variation in foliar carbon exchange in Pinus radiata and Populus deltoides: respiration acclimates fully to changes in temperature but photosynthesis does not. Global Change Biology 16, 288–302.
Seasonal variation in foliar carbon exchange in Pinus radiata and Populus deltoides: respiration acclimates fully to changes in temperature but photosynthesis does not.Crossref | GoogleScholarGoogle Scholar |

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.
Shrub tundra snowmelt.Crossref | GoogleScholarGoogle Scholar |

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.
Ecological dynamics across the Arctic associated with recent climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2ltbnK&md5=f57083c36891af8378d9a93db264751cCAS | 19745143PubMed |

Poyatos R, Gornall J, Mencuccini M, Huntley B, Baxter R (2012) Seasonal controls on net branch CO2 assimilation in sub-Arctic mountain birch (Betula pubescens ssp. czerepanovii (Orlova) Hamet-Ahti). Agricultural and Forest Meteorology 158–159, 90–100.
Seasonal controls on net branch CO2 assimilation in sub-Arctic mountain birch (Betula pubescens ssp. czerepanovii (Orlova) Hamet-Ahti).Crossref | GoogleScholarGoogle Scholar |

Rocha AV, Shaver GR (2011) Burn severity influences postfire CO2 exchange in Arctic tundra. Ecological Applications 21, 477–489.
Burn severity influences postfire CO2 exchange in Arctic tundra.Crossref | GoogleScholarGoogle Scholar | 21563578PubMed |

Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant, Cell & Environment 30, 1086–1106.
The temperature response of C3 and C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiurrP&md5=e94f29c8de8a7fc666f92a7e0859b4d0CAS |

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.
Leaf respiration and alternative oxidase in field-grown alpine grasses respond to natural changes in temperature and light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXivFWltrY%3D&md5=9220d92ca4b834a3e5cfbce9067fbb92CAS | 21128944PubMed |

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.
Observational evidence of recent change in the northern high-latitude environment.Crossref | GoogleScholarGoogle Scholar |

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.
Response of Xanthium strumarium leaf respiration in the light to elevated CO2 concentration, nitrogen availability and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVWjur0%3D&md5=4d652a1df17c83aab42ca0f37c129ff0CAS |

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.
Fitting photosynthetic carbon dioxide response curves for C3 leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiur3F&md5=dd89a3df7229523795151fc64a2761feCAS | 17661745PubMed |

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.
Global change and the carbon balance of arctic ecosystems.Crossref | GoogleScholarGoogle Scholar |

Shaver GR, Johnson LC, Cades DH, Murray G, Laundre JA, Rastetter EB, Nadelhoffer KJ, Giblin AE (1998) Biomass and CO2 flux in wet sedge tundras: responses to nutrients, temperature, and light. Ecological Monographs 68, 75–97.

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.
Global warming and terrestrial ecosystems: a conceptual framework for analysis.Crossref | GoogleScholarGoogle Scholar |

Starr G, Oberbauer SF, Ahlquist LE (2008) The photosynthetic response of Alaskan tundra plants to increased season length and soil warming. Arctic, Antarctic, and Alpine Research 40, 181–191.
The photosynthetic response of Alaskan tundra plants to increased season length and soil warming.Crossref | GoogleScholarGoogle Scholar |

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
Earlier spring snowmelt in northern Alaska as an indicator of climate change.Crossref | GoogleScholarGoogle Scholar |

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.
Climate and species affect fine root production with long-term fertilization in acidic tussock tundra near Toolik Lake, Alaska.Crossref | GoogleScholarGoogle Scholar | 17497180PubMed |

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.
Temperature and microtopography interact to control carbon cycling in a high Arctic fen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1Wisrw%3D&md5=1abbb82083fa9bf719abf19b96675cfcCAS |

Tcherkez G, Cornic G, Bligny R, Gout E, Ghashghaie J (2005) In vivo respiratory metabolism of illuminated leaves. Plant Physiology 138, 1596–1606.
In vivo respiratory metabolism of illuminated leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvV2ks70%3D&md5=7f49838c27bbad82ad4c1d411bf3cdceCAS | 15980193PubMed |

Tcherkez G, Bligny R, Gout E, Mahe A, Hodges M, Cornic G (2008) Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions. Proceedings of the National Academy of Sciences of the United States of America 105, 797–802.
Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSjtLw%3D&md5=190172953ce9ae776045e5ca0c491bdeCAS | 18184808PubMed |

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.
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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht12qu7fK&md5=8b294952a3fcb32098e8aea1ded69e5eCAS | 19675152PubMed |

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.
Leaf respiration at different canopy positions in sweetgum (Liquidambar styraciflua) grown in ambient and elevated concentrations of carbon dioxide in the field.Crossref | GoogleScholarGoogle Scholar | 12414375PubMed |

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.
Scaling foliar respiration in two contrasting forest canopies.Crossref | GoogleScholarGoogle Scholar |

Vose J, Ryan M (2002) Seasonal respiration of foliage, fine roots, and woody tissues in relation to growth, tissue N, and photosynthesis. Global Change Biology 8, 182–193.
Seasonal respiration of foliage, fine roots, and woody tissues in relation to growth, tissue N, and photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Vourlitis GL, Oechel WC (1999) Eddy covariance measurements of CO2 and energy fluxes of an Alaskan tussock tundra ecosystem. Ecology 80, 686–701.
Eddy covariance measurements of CO2 and energy fluxes of an Alaskan tussock tundra ecosystem.Crossref | GoogleScholarGoogle Scholar |

Vourlitis GL, Harazono Y, Oechel WC, Yoshimoto M, Mano M (2000) Spatial and temporal variations in hectare-scale net CO2 flux, respiration and gross primary production of Arctic tundra ecosystems. Functional Ecology 14, 203–214.
Spatial and temporal variations in hectare-scale net CO2 flux, respiration and gross primary production of Arctic tundra ecosystems.Crossref | GoogleScholarGoogle Scholar |

Wang X, Lewis JD, Tissue DT, Seemann JR, Griffin KL (2001) Effects of elevated atmospheric CO2 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.
Effects of elevated atmospheric CO2 concentration on leaf dark respiration of Xanthium strumarium in light and in darkness.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslKmsrg%3D&md5=261a9f7e0fbd5593fb501e4a5afc0d92CAS | 11226264PubMed |

Welker JM, Fahnestock JT, Jones MH (2000) Annual CO2 flux in dry and moist Arctic tundra: field responses to increases in summer temperatures and winter snow depth. Climatic Change 44, 139–150.
Annual CO2 flux in dry and moist Arctic tundra: field responses to increases in summer temperatures and winter snow depth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtFOksLw%3D&md5=91efccfd6a4c19a5e958eafbf0b479bbCAS |

Welker JM, Fahnestock JT, Henry GHR, O’Dea KW, Chimner RA (2004) CO2 exchange in three Canadian high Arctic ecosystems: response to long-term experimental warming. Global Change Biology 10, 1981–1995.
CO2 exchange in three Canadian high Arctic ecosystems: response to long-term experimental warming.Crossref | GoogleScholarGoogle Scholar |

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 responses of Arctic and alpine ecosystems to environmental change. Global Change Biology 15, 1153–1172.
Ecosystem feedbacks and cascade processes: understanding their role in the responses of Arctic and alpine ecosystems to environmental change.Crossref | GoogleScholarGoogle Scholar |

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.
Seasonal trends in photosynthetic parameters and stomatal conductance of blue oak (Quercus douglasii) under prolonged summer drought and high temperature.Crossref | GoogleScholarGoogle Scholar |

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 northeastern US deciduous forest. Oecologia 153, 809–819.
Seasonal variation of temperature response of respiration in invasive Berberis thunbergii (Japanese barberry) and two co-occurring native understory shrubs in a northeastern US deciduous forest.Crossref | GoogleScholarGoogle Scholar | 17609983PubMed |