Advertisement

Oecologia

, Volume 187, Issue 3, pp 609–623 | Cite as

Size-related shifts in carbon gain and growth responses to light differ among rainforest evergreens of contrasting shade tolerance

  • Kerrie M. Sendall
  • Peter B. Reich
  • Christopher H. Lusk
Physiological ecology - original research

Abstract

Recent work suggests that plant size affects light requirements and carbon balance of juvenile trees, and such shifts may be greater in light-demanding species than in their more shade-tolerant associates. To explore the physiological basis of such shifts, we measured juvenile light interception, carbon gain and growth of four subtropical Australian rainforest trees differing in shade tolerance, comparing individuals ranging from 13 to 238 cm in height, across a wide range of understory environments. We hypothesized that even in a standardized light environment, increasing sapling size would lead to declines in net daily carbon gain of foliage and relative growth rates (RGR) of all species, with declines more pronounced in light-demanding species. Crown architecture of individuals was recorded using a 3-dimensional digitizer, and the YPLANT program was used to estimate the self-shaded fraction of each crown and model net carbon gain. Increased sapling size caused a significant increase in self-shading, and significant declines in net daily carbon gain and RGR of light-demanding species, while such ontogenetic variations were minimal or absent in shade-tolerant species. Additionally, differences in the slope of the relationship between light and RGR led to crossovers in RGR among shade-tolerant and light-demanding species at low light. Our results show that the magnitude of ontogenetic variation in net daily carbon gain and RGR can be substantial and may depend on successional status, making it unsafe to assume that young seedling performance can be used to predict or model responses of larger juvenile trees.

Keywords

Argyrodendron trifoliolatum Diploglottis australis Gas exchange Ontogeny Polyscias murrayi Relative growth rate Succession Toona australis 

Notes

Acknowledgements

We are grateful to the staff at the Rocky Creek Dam in Nightcap National Park for hosting this work. Thanks to Rob Kooyman for helping with site selection, and to Tanja Lenz for help with data collection. This work was supported by the Macquarie University Research Excellence Scholarship and the Australian Research Council (DP0878209).

Author contribution statement

KMS and CHL conceived and designed the project, with input from PBR. KMS conducted fieldwork, ran model simulations and analyzed the data, with input from CHL and PBR. KMS, PBR, CHL wrote the manuscript.

Supplementary material

442_2018_4125_MOESM1_ESM.pdf (834 kb)
Supplementary material 1 (PDF 833 kb)

References

  1. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with Image. J Biophotonics Int 11:36–42Google Scholar
  2. Baltzer JL, Thomas SC (2007) Determinants of whole-plant light requirements in Bornean rain forest tree saplings. J Ecol 95:1208–1221CrossRefGoogle Scholar
  3. Bazzaz FA (1979) The physiological ecology of plants succession. Annu Rev Ecol Syst 10:351–371CrossRefGoogle Scholar
  4. Buchman RG, Pederson SP, Walters NR (1983) A tree survival model with application to species of the Great Lakes region. Can J For Res 13:601–608CrossRefGoogle Scholar
  5. Chabot BF, Hicks DJ (1982) The ecology of leaf lifespans. Annu Rev Ecol Syst 13:229–259CrossRefGoogle Scholar
  6. Coley PD (1983) Herbivory and defense characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–233CrossRefGoogle Scholar
  7. Delagrange S, Messier C, Lechowicz MJ, Dizengremel P (2004) Physiological, morphological and allocational plasticity in understory deciduous trees: importance of plant size and light availability. Tree Physiol 22:775–784CrossRefGoogle Scholar
  8. Eissenstat DM, Yanai RD (2002) Root life span, efficiency, and turnover. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker Inc., New York, pp 221–238Google Scholar
  9. Falster DS, Westoby M (2003) Leaf size and angle vary widely across species: what consequences for light interception? New Phytol 158:509–525CrossRefGoogle Scholar
  10. Falster DS, Reich PB, Ellsworth DS, Wright IJ, Westoby M, Oleksyn J, Lee T (2011) Lifetime return on investment increases with leaf lifespan among 10 Australian woodland species. New Phytol 193:409–419CrossRefPubMedGoogle Scholar
  11. Finzi AC, Canham CD (2000) Sapling growth in response to light and nitrogen availability in a southern New England forest. For Ecol Manage 131:153–165CrossRefGoogle Scholar
  12. Floyd AG (1989) Rainforest trees of mainland south-eastern Australia. Inkata Press, MelbourneGoogle Scholar
  13. Frazer GW, Canham CD, Lertzman KP (1999) Gap Light Analyzer (GLA), Version 2.0: imaging software to extract canopy structure and gap light transmission indices from true-color fisheye photographs, users manual and program documentation. Simon Frazer University, Burnaby, British Columbia, and the Institute of Ecosystem Studies, Millbrook, New YorkGoogle Scholar
  14. Gerrish G (1990) Relating carbon allocation patterns to tree senescence in Metrosideros forests. Ecology 71:1176–1184CrossRefGoogle Scholar
  15. Grime JP, Hunt R (1975) Relative growth-rate: its range and adaptive significance in a local flora. J Ecol 63:393–422CrossRefGoogle Scholar
  16. Grubb PJ, Metcalfe DJ (1996) Adaptation and inertia in the Australian tropical lowland rain-forest flora: contradictory trends in intergeneric and intrageneric comparisons of seed size in relation to light demand. Funct Ecol 10:512–520CrossRefGoogle Scholar
  17. Iqbal M (1983) An introduction to solar radiation. Academic Press, OrlandoGoogle Scholar
  18. King DA (1994) Influence of light level on the growth and morphology of saplings in a Panamanian forest. Am J Bot 81:948–957CrossRefGoogle Scholar
  19. Kitajima K (1994) Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98:419–428CrossRefPubMedGoogle Scholar
  20. Kitajima K, Bolker B (2003) Testing performance rank-reversals among coexisting species: crossover point irradiance analysis. Funct Ecol 17:276–281CrossRefGoogle Scholar
  21. Knapp AK, Carter GA (1998) Variability in leaf optical properties among 26 species from a broad range of habitats. Am J Bot 85:940–946CrossRefPubMedGoogle Scholar
  22. Kobe RK (1996) Intraspecific variation in sapling mortality and growth predicts geographic variation in forest composition. Ecol Monogr 66:181–201CrossRefGoogle Scholar
  23. Kobe RK (1997) Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth. Oikos 80:226–233CrossRefGoogle Scholar
  24. Kobe RK (1999) Light gradient partitioning among tropical tree species through differential seedling mortality and growth. Ecology 80:187–201CrossRefGoogle Scholar
  25. Kobe RK, Pacala SW, Silander JA, Canham CD (1995) Juvenile tree survivorship as a component of shade tolerance. Ecol Appl 5:527–532CrossRefGoogle Scholar
  26. Kohyama T, Hotta M (1990) Significance of allometry in tropical saplings. Funct Ecol 4:515–521CrossRefGoogle Scholar
  27. Lin J, Harcombe PA, Fulton MR, Hall RW (2002) Sapling growth and survivorship as a function of light in a mesic forest of southeastern Texas, USA. Oecologia 132:428–435CrossRefPubMedGoogle Scholar
  28. Lusk CH (2002) Leaf area accumulation helps juvenile evergreen trees tolerate shade in a temperate rainforest. Oecologia 132:188–196CrossRefPubMedGoogle Scholar
  29. Lusk CH (2004) Leaf area and growth of juvenile temperate evergreens in low light: species of contrasting shade tolerance change rank during ontogeny. Funct Ecol 18:820–828CrossRefGoogle Scholar
  30. Lusk CH, Jorgensen MA (2013) The whole-plant compensation point as a measure of juvenile tree light requirements. Funct Ecol 27:1286–1294CrossRefGoogle Scholar
  31. Lusk CH, Reich PB (2000) Relationships of leaf dark respiration with light environment and tissue nitrogen content in juveniles of 11 cold-temperate tree species. Oecologia 123:318–329CrossRefPubMedGoogle Scholar
  32. Lusk CH, Falster DS, Perez-Millaqueo M, Saldana A (2004) Ontogenetic variation in light interception, self-shading and biomass distribution of seedlings of the conifer Araucaria araucana (Molina) K. Koch. Rev Chil Hist Nat 79:321–328Google Scholar
  33. Lusk CH, Falster DS, Jara-Vergara CK, Jimenez-Castillo M, Saldana-Mendoza A (2008) Ontogenetic variation in light requirements of juvenile rainforest evergreens. Funct Ecol 22:454–459CrossRefGoogle Scholar
  34. Lusk CH, Perez-Millaqueo M, Piper FI, Saldana A (2011) Ontogeny, understory light interception and simulated carbon gain of juvenile rainforest evergreens differing in shade tolerance. Ann Bot 108:419–428CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lusk CH, Jorgensen MA, Bellingham PJ (2015) A conifer-angiosperm divergence in the growth vs. shade tolerance trade-off underlies the dynamics of a New Zealand warm-temperate rain forest. J Ecol 103:479–488CrossRefGoogle Scholar
  36. Machado JL, Reich PB (2006) Dark respiration rate increases with plant size in saplings of three temperate tree species despite decreasing tissue nitrogen and nonstructural carbohydrates. Tree Physiol 26:915–923CrossRefPubMedGoogle Scholar
  37. Messier C, Nikinmaa E (2000) Effects of light availability and sapling size on the growth, biomass allocation, and crown morphology of understory sugar maple, yellow birch, and beech. Ecoscience 7:345–356CrossRefGoogle Scholar
  38. Moad AS (1992) Dipterocarp juvenile growth and understory light availability in Malaysian tropical forest. University of Aberdeen, AberdeenGoogle Scholar
  39. Niklas KJ, Cobb ED (2008) Evidence for “diminishing returns” from the scaling of stem diameter and specific leaf area. Am J Bot 95:549–557CrossRefPubMedGoogle Scholar
  40. Niklas KJ, Enquist BJ (2001) Invariant scaling relationships for interspecific plant biomass production rates and body size. Proc Natl Acad Sci 98:2922–2927CrossRefPubMedPubMedCentralGoogle Scholar
  41. Pacala SW, Canham CD, Silander JAJ (1993) Forest models defined by field measurements: I. The design of a northeastern forest simulator. Can J For Res 23:1980–1988CrossRefGoogle Scholar
  42. Pacala SW, Canham CD, Silander JA, Kobe RK (1994) Sapling growth as a function of resources in a north temperate forest. Can J For Res 24:2172–2183CrossRefGoogle Scholar
  43. Pearcy RW, Yang WM (1996) A three-dimensional crown architecture model for assessment of light capture and carbon gain by understory plants. Oecologia 108:1–12CrossRefPubMedGoogle Scholar
  44. Poorter L (1999) Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morphological and physiological traits. Funct Ecol 13:396–410CrossRefGoogle Scholar
  45. Poorter L, Bongers F, Sterck FJ, Woll H (2005) Beyond the regeneration phase: differentiation of height-light trajectories among tropical tree species. J Ecol 93:256–267CrossRefGoogle Scholar
  46. Reich PB, Ellsworth DS, Uhl C (1995) Leaf carbon and nutrient assimilation and conservation in species of differing successional status in an oligotrophic Amazonian forest. Funct Ecol 9:65–76CrossRefGoogle Scholar
  47. Reich PB, Tjoelker M, Buschena C, Knops J, Wrage K, Machado J, Tilman D (2003) Variation in growth rate and ecophysiology among 34 grassland and savanna species under contrasting N supply: a test of functional group differences. New Phytol 157:617–631CrossRefGoogle Scholar
  48. Reich PB, Uhl C, Walters MB, Prugh L, Ellsworth DS (2004) Leaf demography and phenology in Amazonian rain forest: a census of 40,000 leaves of 23 tree species. Ecol Monogr 74:3–23CrossRefGoogle Scholar
  49. Sack L, Grubb PJ (2001) Why do species of woody seedlings change rank in relative growth rate between low and high irradiance? Funct Ecol 15:145–154CrossRefGoogle Scholar
  50. Sendall KM, Lusk CH, Reich PB (2015a) Becoming less tolerant with age: sugar maple shade, and ontogeny. Oecologia 179:1011–1021CrossRefPubMedGoogle Scholar
  51. Sendall KM, Lusk CH, Reich PB (2015b) Trade-offs in juvenile growth potential vs. shade tolerance among subtropical rainforest trees on soils of contrasting fertility. Funct Ecol 30:845–855CrossRefGoogle Scholar
  52. Shugart HH (1984) A theory of forest dynamics: the ecological implications of forest succession models. Springer, New YorkCrossRefGoogle Scholar
  53. Singsaas EL, Ort DR, DeLucia EH (2001) Variation in measured values of photosynthetic quantum yield in ecophysiological studies. Oecologia 128:15–23CrossRefPubMedGoogle Scholar
  54. Smith NJC, Zahid DM, Ashwath N, Midmore DJ (2008) Seed ecology and successional status of 27 tropical rainforest cabinet timber species from Queensland. For Ecol Manag 256:1031–1038CrossRefGoogle Scholar
  55. Sterck FJ, Bongers F (1998) Ontogenetic changes in size, allometry, and mechanical design of tropical rain forest trees. Am J Bot 85:266–272CrossRefPubMedGoogle Scholar
  56. Sterck FJ, Schieving F, Lemmens A, Pons TL (2005) Performance of trees in forest canopies: explorations with a bottom-up functional-structural plant growth model. New Phytol 166:827–843CrossRefPubMedGoogle Scholar
  57. Tjoelker MG, Oleksyn J, Reich PB (2001) Modelling respiration of vegetation: evidence for a general temperature-dependent Q10. Glob Change Biol 7:223–230CrossRefGoogle Scholar
  58. Turner J, Kelly J (1981) Relationships between soil nutrients and vegetation in a north coast forest, New South Wales. Aust For J 11:201–208Google Scholar
  59. Valladares F, Stillman JB, Pearcy RW (2002) Convergence in light capture efficiencies among tropical forest understory plants with contrasting crown architecture: a case of morphological compensation. Am J Bot 89:1275–1284CrossRefPubMedGoogle Scholar
  60. Walters MB, Reich PB (1996) Are shade tolerance, survival, and growth linked? Low light and nitrogen effects on hardwood seedlings. Ecology 77:841–853CrossRefGoogle Scholar
  61. Walters MB, Reich PB (1999) Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ? New Phytol 143:143–154CrossRefGoogle Scholar
  62. Walters MB, Reich PB (2000) Seed size, nitrogen supply, and growth rate affect tree seedling survival in deep shade. Ecology 81:1887–1901CrossRefGoogle Scholar
  63. Walters MB, Kruger EL, Reich PB (1993) Relative growth-rate in relation to physiological and morphological traits for northern hardwood tree seedlings—species, light environment and ontogenic considerations. Oecologia 96:219–231CrossRefPubMedGoogle Scholar
  64. Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291CrossRefPubMedGoogle Scholar
  65. Wright EF, Coates KD, Canham CD, Bartemucci P (1998) Species variability in growth response to light across climatic regions in northwestern British Colombia. Can J For Res 28:871–886CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of BiologyGeorgia Southern UniversityStatesboroUSA
  2. 2.Department of Forest ResourcesUniversity of MinnesotaSt. PaulUSA
  3. 3.Department of Biological SciencesMacquarie UniversitySydneyAustralia
  4. 4.Hawkesbury Institute for the EnvironmentWestern Sydney UniversityPenrithAustralia
  5. 5.Department of Biological SciencesUniversity of WaikatoHamiltonNew Zealand

Personalised recommendations