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Oecologia

, Volume 189, Issue 1, pp 37–46 | Cite as

Intracanopy adjustment of leaf-level thermal tolerance is associated with microclimatic variation across the canopy of a desert tree (Acacia papyrocarpa)

  • Ellen M. Curtis
  • Charles A. Knight
  • Andrea Leigh
Physiological ecology - original research
  • 124 Downloads

Abstract

Tree crowns are spatially heterogeneous, sometimes resulting in significant variation in microclimate across the canopy, particularly with respect to temperature. Yet it is not known whether such localised temperature variation equates to intracanopy variation in leaf-level physiological thermal tolerance. Here, we studied whether microclimate variation across the canopy of a dominant desert tree equated to localised variation in leaf thermal thresholds (T50) among four canopy positions: upper south, upper north, lower south, lower north. Principal component analysis was used to generate a composite climatic stress variable (CSTRESS) from canopy temperature, vapour pressure deficit, and relative humidity. We also determined the average number of days that maximum temperatures exceeded the air temperature equating to this species’ critical threshold of 49 °C (AT49). To estimate how closely leaf temperatures track ambient temperature, we predicted the thermal time constant (τ) for leaves at each canopy position. We found that CSTRESS and AT49 were significantly greater in lower and north-facing positions in the canopy. Differences in wind speed with height resulted in significantly longer predicted τ for leaves positioned at lower, north-facing positions. Variation in these drivers was correlated with significantly higher T50 for leaves in these more environmentally stressful canopy positions. Our findings suggest that this species may optimise resources to protect against thermal damage at a whole-plant level. They also indicate that, particularly in desert environments with steep intracanopy microclimatic gradients, whole-plant carbon models could substantially under- or overestimate productivity under heat stress, depending on where in the canopy T50 is measured.

Keywords

Canopy microclimate Desert plants Heat stress Leaf plasticity Thermotolerance 

Notes

Acknowledgements

This project was undertaken as part of a research collaboration agreement between the University of Technology, Sydney and the Port Augusta City Council, South Australia, including support from the Friends of the Australian Arid Lands Botanic Gardens and nursery staff. The authors gratefully acknowledge the support of an Australian Wildlife Society grant to EMC for equipment. We also thank Ronda and Peter Hall, Dr, Brad Murray, Alicia Cook and staff at the UTS Workshop for technical assistance. This research was supported by an Australian Government Research Training Program Scholarship.

Author contribution statement

AL and EMC generated hypotheses and designed the thermal tolerance work; EMC collected and analysed the data; CAK provided advice and contributed fundamental intellectual input; EMC led the writing, with AL revising the final text.

Supplementary material

442_2018_4289_MOESM1_ESM.docx (236 kb)
Supplementary material 1 (DOCX 236 kb)

References

  1. Abdi H, Williams LJ (2010) Principal component analysis. Wiley interdisciplinary reviews: computational statistics 2:433–459CrossRefGoogle Scholar
  2. AGBoM (2013) Monthly climate statistics—Port Augusta. http://www.bom.gov.au/. Accessed 2013
  3. AGBoM (2016) Wind roses for selected locations in Australia. Port Augusta. http://www.bom.gov.au/climate/averages/wind/selection_map.shtml. Viewed 14 March 2016
  4. Amthor JS (1984) The role of maintenance respiration in plant growth. Plant Cell Environ 7:561–569.  https://doi.org/10.1111/1365-3040.ep11591833 CrossRefGoogle Scholar
  5. Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II Inactivation, protein damage and turnover. Biochim et Biophys Acta Bioenerg 1143:113–134.  https://doi.org/10.1016/0005-2728(93)90134-2 CrossRefGoogle Scholar
  6. Bauerle WL, Bowden JD, Wang GG (2007) The influence of temperature on within-canopy acclimation and variation in leaf photosynthesis: spatial acclimation to microclimate gradients among climatically divergent Acer rubrum L. genotypes. J Exp Bot 58:3285–3298CrossRefGoogle Scholar
  7. Bernacchi CJ, Rosenthal DM, Pimentel C, Long SP, Farquhar GD (2009) Modeling the temperature dependence of C3 photosynthesis. In: Laisk A, Nedbal L, Govindjee S (eds) Photosynthesis in silico: Understanding complexity from molecules to ecosystems. Springer, Dordrecht, pp 231–246CrossRefGoogle Scholar
  8. Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273.  https://doi.org/10.3389/fpls.2013.00273 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Curtis EM, Knight CA, Petrou K, Leigh A (2014) A comparative analysis of photosynthetic recovery from thermal stress: a desert plant case study. Oecologia 175:1051–1061CrossRefGoogle Scholar
  10. Curtis EM, Gollan JR, Murray BR, Leigh A (2016) Native microhabitats better predict tolerance to warming than latitudinal macro-climatic variables in arid-zone plants. J Biogeogr 43:1156–1165.  https://doi.org/10.1111/jbi.12713 CrossRefGoogle Scholar
  11. Eamus D (2006) Ecohydrology: vegetation function, water and resource management. CSIRO Publishing, ClaytonGoogle Scholar
  12. Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971CrossRefGoogle Scholar
  13. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Ann Rev Plant Physiol 33:317–345CrossRefGoogle Scholar
  14. Frak E et al (2002) Spatial distribution of leaf nitrogen and photosynthetic capacity within the foliage of individual trees: disentangling the effects of local light quality, leaf irradiance, and transpiration. J Exp Bot 53:2207–2216.  https://doi.org/10.1093/jxb/erf065 CrossRefPubMedGoogle Scholar
  15. Garson G (2013a) Factor analysis. Statistical Associates Publishers, AsheboroGoogle Scholar
  16. Garson G (2013b) Generalized linear models/generalized estimating equations, 2013th edn. Statistical Associates Publishers, AsheboroGoogle Scholar
  17. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101CrossRefGoogle Scholar
  18. Georgieva K, Yordanov I (1994) Temperature dependence of photochemical and non-photochemical fluorescence quenching in intact pea leaves. J Plant Physiol 144:754–759Google Scholar
  19. Havaux M, Greppin H, Strasser RJ (1991) Functioning of Photosystem I and Photosystem II in pea leaves exposed to heat—stress in the presence or absence of light: analysis using in-vivo fluorescence, absorbency, oxygen and photoacoustic measurements. Planta.  https://doi.org/10.1007/bf00201502
  20. Hikosaka K, Ishikawa K, Borjigidai A, Muller O, Onoda Y (2006) Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. J Exp Bot 57:291–302.  https://doi.org/10.1093/jxb/erj049 CrossRefPubMedGoogle Scholar
  21. Hoffmann AA (1995) Acclimation: increasing survival at a cost. Trends Ecol Evol 10:1–1CrossRefGoogle Scholar
  22. IPCC (2014) Climate change 2014: mitigation of climate change. In: Edenhofer O, Pichs-Madruga R, Sokona Y, Farahani E, Kadner S, Seyboth K, Adler A, Baum I, Brunner S, Eickemeier P, Kriemann B, Savolainen J, Schlömer S, von Stechow C, Zwickel T, Minx JC (eds) Contribution of working group III to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, New York, pp 1–1435Google Scholar
  23. Jongman RH, Ter Braak CJ, van Tongeren OF (1995) Data analysis in community and landscape ecology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  24. Katja H et al (2012) Temperature responses of dark respiration in relation to leaf sugar concentration. Physiol Plant 144:320–334.  https://doi.org/10.1111/j.1399-3054.2011.01562.x CrossRefGoogle Scholar
  25. Knight C (2010) Small heat shock protein responses differ between chaparral shrubs from contrasting microclimates. J Bot.  https://doi.org/10.1155/2010/171435
  26. Knight C, Ackerly D (2002) An ecological and evolutionary analysis of photosynthetic thermotolerance using the temperature-dependent increase in fluorescence. Oecologia 130:505–514CrossRefGoogle Scholar
  27. Knight CA, Ackerly DD (2003a) Evolution and plasticity of photosynthetic thermal tolerance, specific leaf area and leaf size: congeneric species from desert and coastal environments. New Phytol 160:337–347CrossRefGoogle Scholar
  28. Knight CA, Ackerly DD (2003b) Small heat shock protein responses of a closely related pair of desert and coastal Encelia. Int J Plant Sci 164(1):53–60CrossRefGoogle Scholar
  29. Küppers M, Pfiz M (2009) Role of Photosynthetic Induction for Daily and Annual Carbon Gains of Leaves and Plant Canopies. In: Laisk A, Nedbal L, Govindjee S (eds) Photosynthesis in silico: understanding complexity from molecules to ecosystems. Springer, Dordrecht, pp 417–440Google Scholar
  30. Lange R, Purdie R (1976) Western myall (Acacia sowdenii), its survival prospects and management needs. Rangeland J 1:64–69CrossRefGoogle Scholar
  31. Larkindale J, Hall J, Knight M, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897CrossRefGoogle Scholar
  32. Leigh A et al (2012) Do thick leaves avoid thermal damage in critically low wind speeds? New Phytol 194:477–487CrossRefGoogle Scholar
  33. Leigh A, Sevanto S, Close J, Nicotra A (2017) The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions? Plant Cell Environ 40:237–248CrossRefGoogle Scholar
  34. Leroi AM, Bennett AF, Lenski RE (1994) Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proc Natl Acad Sci 91:1917–1921.  https://doi.org/10.1073/pnas.91.5.1917 CrossRefPubMedGoogle Scholar
  35. Lin Y-S (2012) How will Eucalyptus tree species respond to global climate change?–A comparison of temperature responses of photosynthesis, University of Western, SydneyGoogle Scholar
  36. Loeschcke V, Hoffmann AA (2002) The detrimental acclimation hypothesis. Trends Ecol Evol 17:407–408.  https://doi.org/10.1016/S0169-5347(02)02558-2 CrossRefGoogle Scholar
  37. Macinnis-Ng C, Eamus D (2009) Climate change and water use of native vegetation. Research Report, Land & Water Australia, CanberraGoogle Scholar
  38. Maconochie J, Lange R (1970) Canopy dynamics of trees and shrubs with particular reference to arid-zone topfeed species. Trans R Soc S Aust 94:243–248Google Scholar
  39. Marias DE, Meinzer FC, Still C (2016) Leaf age and methodology impact assessments of thermotolerance of Coffea arabica. Trees:1–9Google Scholar
  40. McVicar TR et al (2008) Wind speed climatology and trends for Australia, 1975–2006: capturing the stilling phenomenon and comparison with near-surface reanalysis output. Geophys Res Lett.  https://doi.org/10.1029/2008gl035627
  41. Meir P et al (2002) Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area. Plant Cell Environ 25:343–357.  https://doi.org/10.1046/j.0016-8025.2001.00811.x CrossRefGoogle Scholar
  42. Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4:130–135CrossRefGoogle Scholar
  43. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489CrossRefGoogle Scholar
  44. Mott JJ (1972) Germination studies on some annual species from an arid region of Western Australia. J Ecol 60:293–304.  https://doi.org/10.2307/2258347 CrossRefGoogle Scholar
  45. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim et Biophys Acta Bioenerg 1767:414–421.  https://doi.org/10.1016/j.bbabio.2006.11.019
  46. Murray FW (1967) On the computation of saturation vapor pressure. J Appl Meteorol 6:203–204.  https://doi.org/10.1175/1520-0450(1967)006<0203:OTCOSV>2.0.CO;2 CrossRefGoogle Scholar
  47. Niinemets Ü (2007) Photosynthesis and resource distribution through plant canopies. Plant Cell Environ 30:1052–1071.  https://doi.org/10.1111/j.1365-3040.2007.01683.x CrossRefPubMedGoogle Scholar
  48. Niinemets Ü (2012) Optimization of foliage photosynthetic capacity in tree canopies: towards identifying missing constraints. Tree Physiol 32:505–509.  https://doi.org/10.1093/treephys/tps045 CrossRefPubMedGoogle Scholar
  49. Niinemets Ü, Anten NPR (2009) Packing the photosynthetic machinery: from leaf to canopy. In: Laisk A, Nedbal L, Govindjee S (eds) Photosynthesis in silico: understanding complexity from molecules to ecosystems. Springer, Dordrecht, pp 363–399Google Scholar
  50. Niinemets Ü, Valladares F (2004) Photosynthetic acclimation to simultaneous and interacting environmental stresses along natural light gradients: optimality and constraints. Plant Biol 6:254–268CrossRefGoogle Scholar
  51. Niinemets Ü, Oja V, Kull O (1999) Shape of leaf photosynthetic electron transport versus temperature response curve is not constant along canopy light gradients in temperate deciduous trees. Plant Cell Environ 22:1497–1513.  https://doi.org/10.1046/j.1365-3040.1999.00510.x CrossRefGoogle Scholar
  52. Nobel PS (2012) Physicochemical and environmental plant physiology. Academic Press, New YorkGoogle Scholar
  53. 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 Environ 36:1268–1284.  https://doi.org/10.1111/pce.12057 CrossRefPubMedGoogle Scholar
  54. Pearcy RW, Björkman O, Caldwell MM, Keeley JE, Monson RK, Strain BR (1987) Carbon gain by plants in natural environments. Bioscience 37:21–29CrossRefGoogle Scholar
  55. Pearcy RW, Roden JS, Gamon JA (1990) Sunfleck dynamics in relation to canopy structure in a soybean (Glycine max (L.) Merr.) canopy. Agric For Meteorol 52:359–372.  https://doi.org/10.1016/0168-1923(90)90092-K CrossRefGoogle Scholar
  56. Russell G, Marshall B, Jarvis PG (1990) Plant canopies: their growth. Cambridge University Press, Form and FunctionGoogle Scholar
  57. Ryan MG (1991) Effects of climate change on plant respiration. Ecol Appl 1:157–167.  https://doi.org/10.2307/1941808 CrossRefPubMedGoogle Scholar
  58. Sack L, Melcher PJ, Liu WH, Middleton E, Pardee T (2006) How strong is intracanopy leaf plasticity in temperate deciduous trees? Am J Bot 93:829–839CrossRefGoogle Scholar
  59. Schrader SM, Wise RR, Wacholtz WF, Ort DR, Sharkey TD (2004) Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. Plant Cell Environ 27:725–735.  https://doi.org/10.1111/j.1365-3040.2004.01172.x CrossRefGoogle Scholar
  60. Stiegel S, Entling MH, Mantilla-Contreras J (2017) Reading the leaves’ palm: leaf traits and herbivory along the microclimatic gradient of forest layers. PLoS One 12:e0169741.  https://doi.org/10.1371/journal.pone.0169741 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51.  https://doi.org/10.1111/j.0031-9317.2005.00582.x CrossRefGoogle Scholar
  62. Teskey R, Wertin T, Bauweraerts I, Ameye M, McGuire MA, Steppe K (2015) Responses of tree species to heat waves and extreme heat events. Plant Cell Environ 38:1699–1712.  https://doi.org/10.1111/pce.12417 CrossRefPubMedGoogle Scholar
  63. Vogel S (2009) Leaves in the lowest and highest winds: temperature, force and shape. New Phytol 183:13–26CrossRefGoogle Scholar
  64. von Caemmerer S, Farquhar G, Berry J (2009) Biochemical model of C 3 photosynthesis. In: Laisk A, Nedbal, L., Govindjee S (eds) Photosynthesis in silico: understanding complexity from molecules to ecosystems. Springer, Dordrecht, pp 209–230Google Scholar
  65. Walter I et al (2005) ASCE’s standardized reference evapotranspiration equation. In: Allen R, Walter I, Elliott R, Howell T, Itenfisu D, Jensen M (eds) ASCE’s standardized reference evapotranspiration equation, pp 1–70Google Scholar
  66. Warner TT (2009) Desert meteorology. Cambridge University Press, CambridgeGoogle Scholar
  67. Whitford WG (2002) Ecology of desert systems. Elsevier Science, AmsterdamGoogle Scholar
  68. World Wide Wattle V2 (2016) Acacia papyrocarpa Benth., Fl. Austral. vol 2, p 338 (1864). www.worldwidewattle.com. Accessed 2017
  69. Zweifel R, Böhm JP, Häsler R (2002) Midday stomatal closure in Norway spruce—reactions in the upper and lower crown. Tree Physiol 22:1125–1136.  https://doi.org/10.1093/treephys/22.15-16.1125 CrossRefPubMedGoogle Scholar
  70. Zwieniecki MA, Boyce CK, Holbrook NM (2004) Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves. Plant Cell Environ 27:357–365.  https://doi.org/10.1111/j.1365-3040.2003.01153.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ellen M. Curtis
    • 1
  • Charles A. Knight
    • 2
  • Andrea Leigh
    • 1
  1. 1.School of Life SciencesUniversity of Technology SydneyBroadwayAustralia
  2. 2.Department of Biological SciencesCalifornia Polytechnic State UniversitySan Luis ObispoUSA

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