International Journal of Biometeorology

, Volume 58, Issue 8, pp 1789–1797 | Cite as

Testing a growth efficiency hypothesis with continental-scale phenological variations of common and cloned plants

  • Liang LiangEmail author
  • Mark D. Schwartz
Short Communication


Variation in the timing of plant phenology caused by phenotypic plasticity is a sensitive measure of how organisms respond to weather and climate variability. Although continental-scale gradients in climate and consequential patterns in plant phenology are well recognized, the contribution of underlying genotypic difference to the geography of phenology is less well understood. We hypothesize that different temperate plant genotypes require varying amount of heat energy for resuming annual growth and reproduction as a result of adaptation and other ecological and evolutionary processes along climatic gradients. In particular, at least for some species, the growing degree days (GDD) needed to trigger the same spring phenology events (e.g., budburst and flower bloom) may be less for individuals originated from colder climates than those from warmer climates. This variable intrinsic heat energy requirement in plants can be characterized by the term growth efficiency and is quantitatively reflected in the timing of phenophases—earlier timing indicates higher efficiency (i.e., less heat energy needed to trigger phenophase transitions) and vice versa compared to a standard reference (i.e., either a uniform climate or a uniform genotype). In this study, we tested our hypothesis by comparing variations of budburst and bloom timing of two widely documented plants from the USA National Phenology Network (i.e., red maple-Acer rubrum and forsythia-Forsythia spp.) with cloned indicator plants (lilac-Syringa x chinensis ‘Red Rothomagensis’) at multiple eastern US sites. Our results indicate that across the accumulated temperature gradient, the two non-clonal plants showed significantly more gradual changes than the cloned plants, manifested by earlier phenology in colder climates and later phenology in warmer climates relative to the baseline clone phenological response. This finding provides initial evidence supporting the growth efficiency hypothesis, and suggests more work is warranted. More studies investigating genotype-determined phenological variations will be useful for better understanding and prediction of the continental-scale patterns of biospheric responses to climate change.


Bioclimatology Geographic pattern Climate change Growth efficiency Phenology USA-NPN 



In different occasions when a part of these analyses were presented to academic audiences, Scott Gleeson and William Hargrove provided helpful feedback. Jonathan Philips, Julio L. Betancourt, Susan Mazer, and Alison Donnelly reviewed the entire manuscript and provided valuable comments. We are grateful to these individuals for their help and support. Red maple, forsythia, and cloned lilac phenological data since 2009 were provided by the USA National Phenology Network and the many participants who contribute to its Nature’s Notebook program. Cloned lilac phenological data prior to 2009 were provided by the USA National Phenology Network, Joseph M. Caprio, Mark D. Schwartz, and all contributors to past US Department of Agriculture regional phenology projects. Finally we thank two anonymous reviewers for their helpful and constructive comments.


  1. Badeck F-W, Bondeau A, Bottcher K, Doktor D, Lucht W, Schaber J, Sitch S (2004) Responses of spring phenology to climate change. New Phytol 162:295–309CrossRefGoogle Scholar
  2. Barnosky AD, Hadly EA, Bascompte J, Berlow EL, Brown JH, Fortelius M, Getz WM, Harte J, Hastings A, Marquet PA, Martinez ND, Mooers A, Roopnarine P, Vermeij G, Williams JW, Gillespie R, Kitzes J, Marshall C, Matzke N, Mindell DP, Revilla E, Smith AB (2012) Approaching a state shift in Earth's biosphere. Nature 486:52–58CrossRefGoogle Scholar
  3. Bradshaw A (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:15–11Google Scholar
  4. Burns RM, Honkala BH (1990) Silvics of North America, vol 1. United States Department of Agriculture, Forest Service, Fort Collins, COGoogle Scholar
  5. Campoy JA, Ruiz D, Allderman L, Cook N, Egea J (2012) The fulfilment of chilling requirements and the adaptation of apricot (Prunus armeniaca L.) in warm winter climates: An approach in Murcia (Spain) and the Western Cape (South Africa). Eur J Agron 37:43–55CrossRefGoogle Scholar
  6. Campoy JA, Ruiz D, Nortes M, Egea J (2013) Temperature efficiency for dormancy release in apricot varies when applied at different amounts of chill accumulation. Plant Biol 15:28–35CrossRefGoogle Scholar
  7. Caprio JM (1974) The solar thermal unit concept in problems related to plant development and potential evapotranspiration. In: Lieth H (ed) Phenology and seasonality modeling. Springer, New York, pp 353–364CrossRefGoogle Scholar
  8. Celton JM, Martinez S, Jammes MJ, Bechti A, Salvi S, Legave JM, Costes E (2011) Deciphering the genetic determinism of bud phenology in apple progenies: a new insight into chilling and heat requirement effects on flowering dates and positional candidate genes. New Phytol 192:378–392CrossRefGoogle Scholar
  9. Chmielewski FM (2003) Phenology and agriculture. In: Schwartz MD (ed) Phenology: an integrative environmental science. Kluwer/Springer, Dordrecht, pp 505–522Google Scholar
  10. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365CrossRefGoogle Scholar
  11. De Wolf G, Hebb RS (1971) The story of Forsythia. Arnoldia 31:41–61Google Scholar
  12. Ghelardini L, Falusi M, Santini A (2006) Variation in timing of bud-burst of Ulmus minor clones from different geographical origins. Can J For Res 36:1982–1991CrossRefGoogle Scholar
  13. Gienapp P, Teplitsky C, Alho J, Mills J, Merila J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178CrossRefGoogle Scholar
  14. Gupta S, Narayan R (2012) Phenotypic plasticity of Chenopodium murale across contrasting habitat conditions in peri-urban areas in Indian dry tropics: is it indicative of its invasiveness? Plant Ecol 213:493–503CrossRefGoogle Scholar
  15. Hopkins AD (1920) The bioclimatic law. Mon Weather Rev 48:355–355CrossRefGoogle Scholar
  16. Hopkins AD (1919) The bioclimatic law as applied to entomological research and farm practise. Sci Mon 8:496–513Google Scholar
  17. Kriebel H, Wang CW (1962) The interaction between provenance and degree of chilling in bud-break of sugar maple. Silvae Genet 11:125–130Google Scholar
  18. Li HLH, Wang XWX, Hamann AHA (2010) Genetic adaptation of aspen (Populus tremuloides) populations to spring risk environments: a novel remote sensing approach. Can J For Res 40:2082–2090CrossRefGoogle Scholar
  19. Matías L, Jump AS (2012) Interactions between growth, demography and biotic interactions in determining species range limits in a warming world: the case of Pinus sylvestris. Forest Ecol Manag 282:10–22CrossRefGoogle Scholar
  20. McClain W, Ebinger J (1995) Naturalized Forsythia suspensa (Thunb.) Vahl (Oleaceae) in Illinois. Trans III State Acade Sci 88:119–121Google Scholar
  21. Meehan T (1883) Observations on Forsythia. Proc Acad Nat Sci Phila 35:111–112Google Scholar
  22. Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397:659CrossRefGoogle Scholar
  23. Pau S, Wolkovich EM, Cook BI, Davies TJ, Kraft NJB, Bolmgren K, Betancourt JL, Cleland EE (2011) Predicting phenology by integrating ecology, evolution and climate science. Glob Change Biol 17:3633–3643CrossRefGoogle Scholar
  24. Rehder A (1940) Manual of cultivated trees and shrubs hardy in North America exclusive of the subtropical and warmer temperature regions. MacMillan, New YorkGoogle Scholar
  25. Richter S, Kipfer T, Wohlgemuth T, Calderón GC, Ghazoul J, Moser B (2012) Phenotypic plasticity facilitates resistance to climate change in a highly variable environment. Oecologia 169:269–279CrossRefGoogle Scholar
  26. Schwartz MD (1997) Spring index models: an approach to connecting satellite and surface phenology. In: Lieth H, Schwartz MD (eds) Phenology in seasonal climates I. Backbuys, Leiden, pp 23–38Google Scholar
  27. Schwartz MD, Hanes JM (2010) Continental scale phenology: warming and chilling. Int J Climatol 30:1595–1598CrossRefGoogle Scholar
  28. Schwartz MD, Ahas R, Aasa A (2006) Onset of spring starting earlier across the Northern Hemisphere. Glob Change Biol 12:343–351CrossRefGoogle Scholar
  29. Schwartz MD, Betancourt JL, Weltzin JF (2012) From Caprio's lilacs to the USA National Phenology Network. Front Ecol Environ 10:324–327CrossRefGoogle Scholar
  30. Smith TM, Smith RL (2012) Elements of ecology, 8th edn. Benjamin Cummings, San FranciscoGoogle Scholar
  31. Sokal RR, Rohlf FJ (2012) Biometry: the principles and practice of statistics in biological research, 4th edn. Freeman, New YorkGoogle Scholar
  32. Team R (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  33. Rosenzweig C, Karoly D, Vicarelli M, Neofotis P, Wu QG, Casassa G, Menzel A, Root TL, Estrella N, Seguin B, Tryjanowski P, Liu CZ, Rawlins S, Imeson A (2008) Attributing physical and biological impacts to anthropogenic climate change. Nature 453(7193):353–358CrossRefGoogle Scholar
  34. USA National Phenology Network (2012) Plant phenology data for the United States, 2009–2012. Tucson, Arizona, USA, USA-NPN. Data set accessed 8 November 2012 at
  35. Vitasse Y, Delzon S, Bresson CC, Michalet R, Kremer A (2009) Altitudinal differentiation in growth and phenology among populations of temperate-zone tree species growing in a common garden. Can J For Res 39:1259–1269CrossRefGoogle Scholar
  36. Worrall J (1983) Temperature-bud-burst relationships in amabilis and subalpine fir provenance tests replicated at different elevations. Silvae Genet 32:203–209Google Scholar
  37. Zhang XY, Tarpley D, Sullivan JT (2007) Diverse responses of vegetation phenology to a warming climate. Geophys Res Lett 34:L19405CrossRefGoogle Scholar

Copyright information

© ISB 2013

Authors and Affiliations

  1. 1.Department of GeographyUniversity of KentuckyLexingtonUSA
  2. 2.Department of GeographyUniversity of Wisconsin-MilwaukeeMilwaukeeUSA

Personalised recommendations