Plant Ecology

, Volume 214, Issue 5, pp 787–798 | Cite as

Cold tolerance of photosynthesis as a determinant of tree species regeneration patterns in an evergreen temperate forest

  • Sarah J. Richardson
  • Karen I. Bonner
  • Christopher P. Bickford


Niche partitioning of light among seedling species is a key mechanism supporting coexistence in forests. Species sort along light gradients through direct responses to light and through indirect responses mediated by other environmental factors. Canopy gaps in temperate evergreen rainforests experience sub-zero temperatures and thus gap-dependent species are vulnerable to cold photoinhibition from exposure to high light at low temperatures. We used a shadehouse experiment to test two hypotheses: (1) that gap-dependent species are resistant to cold photoinhibition; and (2) that gap-dependence observed in the field may be driven by the interaction between high light and low temperatures. Specifically, we predicted that some species restricted to shade in the field are excluded from gaps because of low resistance to cold photoinhibition. Gap dependence of angiosperm and conifer seedlings was estimated from expert opinion, and from experimental growth and survival responses to light treatments representing a forest understorey and forest gap. Additional seedlings were used to evaluate resistance to cold photoinhibition (sub-zero temperatures at dawn). Gap-dependent species were resistant to cold photoinhibition. Our second hypothesis was supported by Beilschmiedia tawa (Lauraceae), which had low resistance to photoinhibition, a strong positive growth response to the light treatments, and is restricted to shade in the field. Seedling regeneration niches in temperate rainforest are shaped in part by the interaction between light and low temperatures, and this interaction will be crucial for determining seedling responses to climate warming.


Chlorophyll fluorescence Climate change New Zealand Plant functional trait Regeneration niche Shade tolerance 



We thank Ellen Cieraad, Tahae Doherty, Chris Morse, Rowan Buxton and Gaye Rattray for assistance; Matt McGlone, Norm Mason and Duane Peltzer for reviews; and the NZ Ministry of Business, Innovation and Employment for funding.


  1. Allen RB, Lee WG (2006) Biological invasions in New Zealand. Springer, BerlinCrossRefGoogle Scholar
  2. Antos JA, Guest HJ, Parish R (2005) The tree seedling bank in an ancient montane forest: stress tolerators in a productive habitat. J Ecol 93:536–543CrossRefGoogle Scholar
  3. Augspurger CK (2011) Frost damage and its cascading negative effects on Aesculus glabra. Plant Ecol 212:1193–1203CrossRefGoogle Scholar
  4. Bader MY, Geloof I, Rietkerk M (2007) High solar radiation hinders tree regeneration above the alpine treeline in northern Ecuador. Plant Ecol 191:33–45CrossRefGoogle Scholar
  5. Ball MC, Hodges VS, Laughlin GP (1991) Cold-induced photoinhibition limits regeneration of snow gum at tree-line. Funct Ecol 5:663–668CrossRefGoogle Scholar
  6. Baltzer JL, Thomas SC (2007) Determinants of whole-plant light requirements in Bornean rain forest tree saplings. J Ecol 95:1208–1221CrossRefGoogle Scholar
  7. Bond BJ, Farnsworth BT, Coulombe RA, Winner WE (1999) Foliage physiology and biochemistry in response to light gradients in conifers with varying shade tolerance. Oecologia 120:183–192CrossRefGoogle Scholar
  8. Broncano MJ, Vila M, Boada M (2005) Evidence of Pseudotsuga menziesii naturalization in montane Mediterranean forests. For Ecol Manag 211:257–263CrossRefGoogle Scholar
  9. Canham CD, Denslow JS, Platt WJ, Runkle JR, Spies TA, White PS (1990) Light regimes beneath closed canopies and tree-fall gaps in temperate and tropical forests. Can J For Res 20:620–631CrossRefGoogle Scholar
  10. Carswell FE, Richardson SJ, Doherty JE, Allen RB, Wiser SK (2007) Where do conifers regenerate after selective harvest? A case study from a New Zealand conifer–angiosperm forest. For Ecol Manag 253:138–147CrossRefGoogle Scholar
  11. Carswell FE, Doherty JE, Allen RB, Brignall-Theyer ME, Richardson SJ, Wiser SK (2012) Quantification of the effects of aboveground and belowground competition on growth of seedlings in a conifer–angiosperm forest. For Ecol Manag 269:188–196CrossRefGoogle Scholar
  12. Castro J, Zamora R, Hodar JA, Gomez JM (2004) Seedling establishment of a boreal tree species (Pinus sylvestris) at its southernmost distribution limit: consequences of being in a marginal Mediterranean habitat. J Ecol 92:266–277CrossRefGoogle Scholar
  13. Coomes DA, Grubb PJ (2000) Impacts of root competition in forests and woodlands: a theoretical framework and review of experiments. Ecol Monogr 70:171–207CrossRefGoogle Scholar
  14. Coop JD, Givnish TJ (2008) Constraints on tree seedling establishment in montane grasslands of the Valles Caldera, New Mexico. Ecology 89:1101–1111PubMedCrossRefGoogle Scholar
  15. Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380CrossRefGoogle Scholar
  16. Cunningham SC, Read J (2006) Foliar temperature tolerance of temperate and tropical evergreen rain forest trees of Australia. Tree Physiol 26:1435–1443PubMedCrossRefGoogle Scholar
  17. Dehlin H, Peltzer DA, Allison VJ, Yeates GW, Nilsson MC, Wardle DA (2008) Tree seedling performance and below-ground properties in stands of invasive and native tree species. NZ J Ecol 32:67–79Google Scholar
  18. Dent DH, Burslem D (2009) Performance trade-offs driven by morphological plasticity contribute to habitat specialization of Bornean tree species. Biotropica 41:424–434CrossRefGoogle Scholar
  19. Enright NJ, Ogden J (1995) The southern conifers: a synthesis. In: Enright NJ, Hill RS (eds) Ecology of the southern conifers. Melbourne University Press, Carlton, pp 271–287Google Scholar
  20. Feild TS, Brodribb T (2001) Stem water transport and freeze-thaw xylem embolism in conifers and angiosperms in a Tasmanian treeline heath. Oecologia 127:314–320CrossRefGoogle Scholar
  21. George LO, Bazzaz FA (1999) The fern understory as an ecological filter: growth and survival of canopy-tree seedlings. Ecology 80:846–856CrossRefGoogle Scholar
  22. Grubb PJ, Lee WG, Kollmann J, Wilson JB (1996) Interaction of irradiance and soil nutrient supply on growth of seedlings of ten European tall-shrub species and Fagus sylvatica. J Ecol 84:827–840CrossRefGoogle Scholar
  23. Holdaway RJ, Richardson SJ, Peltzer DA, Coomes DA (2011) Species and community-level patterns in fine root traits along a 120,000 year soil chronosequence. J Ecol 99:954–963CrossRefGoogle Scholar
  24. Houter NC, Pons TL (2012) Ontogenetic changes in leaf traits of tropical rainforest trees differing in juvenile light requirement. Oecologia 169:33–45PubMedCrossRefGoogle Scholar
  25. Inouye DW (2000) The ecological and evolutionary significance of frost in the context of climate change. Ecol Lett 3:457–463CrossRefGoogle Scholar
  26. Kelly D (1987) Slow recovery of Beilschmiedia tawa after severe frosts in inland Taranaki, New Zealand. NZ J Ecol 10:137–140Google Scholar
  27. Knowles B, Beveridge AE (1982) Biological flora of New Zealand. 9. Beilschmiedia tawa (A. Cunn) Benth et Hook. f. ex Kirk (Lauraceae) Tawa. NZ J Bot 20:37–54CrossRefGoogle Scholar
  28. Kobe RK, Pacala SW, Silander JA, Canham CD (1995) Juvenile tree survivorship as a component of shade tolerance. Ecol Appl 5:517–532CrossRefGoogle Scholar
  29. Krause GH (1994) Photoinhibition induced by low temperatures. In: Baker NR, Bowyer JR (eds) Photoinhibition of Photosynthesis: from molecular mechanisms to the field. BIOS Scientific, Oxford, pp 331–348Google Scholar
  30. Lusk CH, Del Pozo A (2002) Survival and growth of seedlings of 12 Chilean rainforest trees in two light environments: gas exchange and biomass distribution correlates. Aust Ecol 27:173–182CrossRefGoogle Scholar
  31. Lusk CH, Reich PB, Montgomery RA, Ackerly DD, Cavender-Bares J (2008) Why are evergreen leaves so contrary about shade? Trends Ecol Evol 23:299–303PubMedCrossRefGoogle Scholar
  32. Lusk CH, Duncan RP, Bellingham PJ (2009) Light environments occupied by conifer and angiosperm seedlings in a New Zealand podocarp–broadleaved forest. NZ J Ecol 33:83–89Google Scholar
  33. Mahmoud A, Grime JP (1974) Comparison of negative relative growth-rates in shaded seedlings. New Phytol 73:1215–1219CrossRefGoogle Scholar
  34. McGlone MS, Dungan RJ, Hall GMJ, Allen RB (2004) Winter leaf loss in the New Zealand woody flora. NZ J Bot 42:1–19CrossRefGoogle Scholar
  35. McGlone MS, Richardson SJ, Jordan GJ (2010) Comparative biogeography of New Zealand trees: species richness, height, leaf traits and range sizes. NZ J Ecol 34:137–151Google Scholar
  36. MfE (2008) Climate change effects and impacts assessment: a guidance manual for local government in New Zealand. Ministry for the Environment, WellingtonGoogle Scholar
  37. Niinemets U, Kull K (1994) Leaf weight per area and leaf size of 85 Estonian woody species in relation to shade tolerance and light availability. For Ecol Man 70:1–10CrossRefGoogle Scholar
  38. Niinemets U, Valladares F (2006) Tolerance to shade, drought, and waterlogging of temperate Northern Hemisphere trees and shrubs. Ecol Monogr 76:521–547CrossRefGoogle Scholar
  39. Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Ann Rev Plant Biol 54:329–355CrossRefGoogle Scholar
  40. Öquist G, Greer DH, Ögren E (1987) Light stress at low temperature. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier Science, Amsterdam, pp 67–87Google Scholar
  41. Peltzer DA, Allen RB, Rogers GM (2005) Dieback and recruitment of the forest dominants Nothofagus fusca and Libocedrus bidwillii, central North Island, New Zealand, vol 255. Department of Conservation, Science for Conservation, Wellington, p 33Google Scholar
  42. Raven JA (2011) The cost of photoinhibition. Physiol Plant 142:87–104PubMedCrossRefGoogle Scholar
  43. Reyes-Díaz M, Ivanov AG, Huner NPA, Alberdi M, Corcuera LJ, Bravo LA (2009) Thermal energy dissipation and its components in two developmental stages of a shade-tolerant species, Nothofagus nitida, and a shade-intolerant species, Nothofagus dombeyi. Tree Phys 29:651–662CrossRefGoogle Scholar
  44. Richardson SJ, Allen RB, Doherty JE (2008) Shifts in leaf N:P ratio during resorption reflect soil P in temperate rainforest. Funct Ecol 22:738–745CrossRefGoogle Scholar
  45. Robakowski P (2005) Susceptibility to low-temperature photoinhibition in three conifers differing in successional status. Tree Phys 25:1151–1160CrossRefGoogle Scholar
  46. Sakai A, Paton DM, Wardle P (1981) Freezing resistance of trees of the south temperate zone, especially subalpine species of Australasia. Ecology 62:563–570CrossRefGoogle Scholar
  47. Sanchez-Gomez D, Zavala MA, Valladares F (2006) Seedling survival responses to irradiance are differentially influenced by low-water availability in four tree species of the Iberian cool temperate-Mediterranean ecotone. Acta Oecol Int J Ecol 30:322–332CrossRefGoogle Scholar
  48. Somersalo S, Krause GH (1989) Photoinhibition at chilling temperature–fluorescence characteristics of unhardened and cold-acclimated spinach leaves. Planta 177:409–416CrossRefGoogle Scholar
  49. Valladares F, Niinemets U (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 2008:237–257CrossRefGoogle Scholar
  50. Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936CrossRefGoogle Scholar
  51. Wardle P (1985) New Zealand timberlines. 3. A synthesis. NZ J Bot 23:263–271CrossRefGoogle Scholar
  52. West CJ (1995) Sustainability of Beilschmiedia tawa-dominated forest in New Zealand: population predictions based on transition matrix model analysis. Aust J Bot 43:51–71CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Sarah J. Richardson
    • 1
  • Karen I. Bonner
    • 1
  • Christopher P. Bickford
    • 1
    • 2
  1. 1.Landcare ResearchLincolnNew Zealand
  2. 2.Department of BiologyKenyon CollegeGambierUSA

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