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Oecologia

, Volume 188, Issue 3, pp 659–669 | Cite as

To spend or to save? Assessing energetic growth-storage tradeoffs in native and invasive woody plants

  • Elise D. HinmanEmail author
  • Jason D. Fridley
Highlighted Student Research

Abstract

Many non-native woody plants invade low-light forest understories but differ from native species in leaf phenology and seasonality of photosynthesis. It is unknown whether such differences in assimilation patterns are due to contrasting strategies of energy allocation. In a group of native and invasive species in Eastern North America, we hypothesized that invaders employ a grow-first strategy, prioritizing allocation to new structural biomass over carbon storage compared to native congeners. We also hypothesized that species producing a single spring leaf flush exhibit a more conservative carbon storage strategy than species with continuous leaf production. We measured sugar and starch concentrations (non-structural carbohydrates; NSCs) in spring and fall in the stems and roots of 39 species of native and non-native shrubs in a common garden, and compared these to patterns of leaf production across species. Native species had higher soluble sugar concentrations than invaders, but invaders tended to store more root starch in spring. We found no difference in leaf production between natives and invaders. Determinate species had more soluble sugars than indeterminate species but had lower root starch. We found no relationship between aboveground productivity and carbon storage. Our results suggest that closely related species with contrasting evolutionary histories have different carbon storage strategies, although not necessarily in relation to their growth potential. The higher soluble sugar concentrations of native species may reflect their evolutionary response to historical disturbances, or different interactions with soil microbes, while increased spring root starch in invaders may support fine root or fruit production.

Keywords

Carbon allocation Invasions Nonstructural carbohydrates Survival Seasonal 

Notes

Acknowledgements

We thank A. Craddock for field assistance and S. Bergey, H. Coleman, J. Hoagland, O. Judson, C. Poovaiah, C. Phalen, and A. Stipanovic for lab assistance. We also thank D. Frank, D. Leopold, and M. Ritchie for their contributions to the theoretical framework of this paper, and M. Heberling and K. Martinez for manuscript comments. This work was supported by a U.S. NSF Doctoral Dissertation Improvement Grant (04293) and a Sigma Xi Grants-in-Aid of Research Grant to E. Hinman.

Author contribution statement

EH and JF worked together to design this research project. EH carried out the data collection and statistical analysis. EH and JF wrote the manuscript.

Supplementary material

442_2018_4177_MOESM1_ESM.docx (847 kb)
Supplementary material 1 (DOCX 846 kb)

References

  1. Ashworth EN, Stirm VE, Volenec JJ (1993) Seasonal variations in soluble sugars and starch within woody stems of Cornus sericea L. Tree Physiol 13(4):379–388CrossRefGoogle Scholar
  2. Callaway RM, Kim J, Mahall BE (2006) Defoliation of Centaurea solstitialis stimulates compensatory growth and intensifies negative effects on neighbors. Biol Invasions 8(6):1389–1397CrossRefGoogle Scholar
  3. Canham CD, Kobe RK, Latty EF, Chazdon RL (1999) Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia 121(1):1–11CrossRefGoogle Scholar
  4. Chapin FS, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21(1):423–447CrossRefGoogle Scholar
  5. Charrier G, Améglio T (2011) The timing of leaf fall affects cold acclimation by interactions with air temperature through water and carbohydrate contents. Environ Exp Bot 72(3):351–357CrossRefGoogle Scholar
  6. Chow PS, Landhausser SM (2004) A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol 24(10):1129–1136CrossRefGoogle Scholar
  7. Curran PJ (1989) Remote sensing of foliar chemistry. Remote Sens Environ 30(3):271–278CrossRefGoogle Scholar
  8. Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34(1):183–211CrossRefGoogle Scholar
  9. de Villemereuil P, Wells JA, Edwards RD, Blomberg SP (2012) Bayesian models for comparative analysis integrating phylogenetic uncertainty. BMC Evol Biol 12(1):102CrossRefGoogle Scholar
  10. Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65:667–687CrossRefGoogle Scholar
  11. Fridley JD (2008) Of Asian forests and European fields: eastern US plant invasions in a global floristic context. PLoS One 3(11):e3630CrossRefGoogle Scholar
  12. Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–362CrossRefGoogle Scholar
  13. Fridley JD (2017) Plant energetics and the synthesis of population and ecosystem ecology. J Ecol 105:95–110CrossRefGoogle Scholar
  14. Fridley JD, Craddock A (2015) Contrasting growth phenology of native and invasive forest shrubs mediated by genome size. New Phytol 207(3):659–668CrossRefGoogle Scholar
  15. Funk JL (2013) The physiology of invasive plants in low-resource environments. Conserv Physiol 1(1):1–17Google Scholar
  16. Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081CrossRefGoogle Scholar
  17. Gallinat AS, Primack RB, Wagner DL (2015) Autumn, the neglected season in climate change research. Trends Ecol Evol 30(3):169–176CrossRefGoogle Scholar
  18. Gelman A, Hill J (2007) Data analysis using regression and multilevel hierarchical models, vol 1. Cambridge University Press, New YorkGoogle Scholar
  19. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7(4):457–472CrossRefGoogle Scholar
  20. Grant TN, Dami IE (2015) Physiological and biochemical seasonal changes in Vitis genotypes with contrasting freezing tolerance. Am J Enol Vitic ajev-2014Google Scholar
  21. Heberling JM, Fridley JD (2013) Resource-use strategies of native and invasive plants in Eastern North American forests. New Phytol 200(2):523–533CrossRefGoogle Scholar
  22. Heberling JM, Kichey T, Decocq G, Fridley JD (2016) Plant functional shifts in the invaded range: a test with reciprocal forest invaders of Europe and North America. Funct Ecol 30(6):875–884CrossRefGoogle Scholar
  23. Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26(7):1067–1081CrossRefGoogle Scholar
  24. Huang W, Siemann E, Wheeler GS, Zou J, Carrillo J, Ding J (2010) Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J Ecol 98:1157–1167CrossRefGoogle Scholar
  25. Iwasa Y, Cohen D (1989) Optimal growth schedule of a perennial plant. Am Nat 133(4):480–505CrossRefGoogle Scholar
  26. Jo I, Fridley JD, Frank DA (2015) Linking above-and belowground resource use strategies for native and invasive species of temperate deciduous forests. Biol Invasions 17(5):1545–1554CrossRefGoogle Scholar
  27. Jo I, Fridley JD, Frank DA (2016) More of the same? In situ leaf and root decomposition rates do not vary between 80 native and nonnative deciduous forest species. New Phytol 209(1):115–122CrossRefGoogle Scholar
  28. Karst J, Gaster J, Wiley E, Landhäusser SM (2016) Stress differentially causes roots of tree seedlings to exude carbon. Tree Physiol 37(2):154–164Google Scholar
  29. Kennard RW, Stone LA (1969) Computer aided design of experiments. Technometrics 11(1):137–148CrossRefGoogle Scholar
  30. Kobe RK (1997) Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth. Oikos 80(2):226–233CrossRefGoogle Scholar
  31. Kozlowski TT (1992) Carbohydrate sources and sinks in woody plants. Bot Rev 58(2):107–222CrossRefGoogle Scholar
  32. Lechowicz MJ (1984) Why do temperate deciduous trees leaf out at different times? Adaptation and ecology of forest communities. Am Nat 124(6):821–842CrossRefGoogle Scholar
  33. Leishman MR, Thomson VP, Cooke J (2010) Native and exotic invasive plants have fundamentally similar carbon capture strategies. J Ecol 98(1):28–42CrossRefGoogle Scholar
  34. Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Li B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177(3):706–714CrossRefGoogle Scholar
  35. Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80(4):1180–1186CrossRefGoogle Scholar
  36. Martínez-Vilalta J, Sala A, Asensio D, Galiano L, Hoch G, Palacio S, Lloret F (2016) Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis. Ecol Monogr 86(4):495–516CrossRefGoogle Scholar
  37. Mason RAB, Cooke J, Moles AT, Leishman MR (2008) Reproductive output of invasive versus native plants. Glob Ecol Biogeogr 17(5):633–640CrossRefGoogle Scholar
  38. Morin X, Améglio T, Ahas R, Kurz-Besson C, Lanta V, Lebourgeois F, Chuine I (2007) Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiol 27(6):817–825CrossRefGoogle Scholar
  39. Morin X, Lechowicz MJ, Augspurger C, O’Keefe J, Viner D, Chiune I (2009) Leaf phenology in 22 North American tree species during the 21st century. Glob Change Biol 15(4):961–975CrossRefGoogle Scholar
  40. Muffler L, Beierkuhnlein C, Aas G, Jentsch A, Schweiger AH, Zohner C, Kreyling J (2016) Distribution ranges and spring phenology explain late frost sensitivity in 170 woody plants from the Northern Hemisphere. Glob Ecol Biogeogr 25(9):1061–1071CrossRefGoogle Scholar
  41. Navas ML, Ducout B, Roumet C, Richarte J, Garnier J, Garnier E (2003) Leaf life span, dynamics and construction cost of species from Mediterranean old-fields differing in successional status. New Phytol 159(1):213–228CrossRefGoogle Scholar
  42. Palacio S, Hoch G, Sala A, Körner C, Millard P (2013) Does carbon storage limit tree growth? New Phytol 201(4):1096–1100CrossRefGoogle Scholar
  43. Panchen ZA, Primack RB, Nordt B, Ellwood ER, Stevens AD, Renner SS, Willis CG, Fahey R, Whittemore A, Du Y, Davis CC (2014) Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy. New Phytol 203(4):1208–1219CrossRefGoogle Scholar
  44. Philippi T (1993) Bet-hedging germination of desert annuals: variation among populations and maternal effects in Lepidium lasiocarpum. Am Nat 142(3):488–507CrossRefGoogle Scholar
  45. Philippi T, Seger J (1989) Hedging one’s evolutionary bets, revisited. Trends Ecol Evol 4(2):41–44CrossRefGoogle Scholar
  46. Poorter L, Kitajima K, Mercado P, Chubiña J, Melgar I, Prins HH (2010) Resprouting as a persistence strategy of tropical forest trees: relations with carbohydrate storage and shade tolerance. Ecology 91(9):2613–2627CrossRefGoogle Scholar
  47. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715CrossRefGoogle Scholar
  48. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. Ramirez JA, Posada JM, Handa IT, Hoch G, Vohland M, Messier C, Reu B (2015) Near-infrared spectroscopy (NIRS) predicts non-structural carbohydrate concentrations in different tissue types of a broad range of tree species. Methods Ecol Evol 6(9):1018–1025CrossRefGoogle Scholar
  50. Rejmanek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77(6):1655–1661CrossRefGoogle Scholar
  51. Rogers WE, Siemann E (2002) Effects of simulated herbivory and resource availability on native and invasive exotic tree seedlings. Basic Appl Ecol 3(4):297–307CrossRefGoogle Scholar
  52. Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67CrossRefGoogle Scholar
  53. Sakai A, Yoshida S (1968) The role of sugar and related compounds in variations of freezing resistance. Cryobiology 5(3):160–174CrossRefGoogle Scholar
  54. Schierenbeck KA, Mack RN, Sharitz RR (1994) Effects of herbivory on growth and biomass allocation in native and introduced species of Lonicera. Ecology 75(6):1661–1672CrossRefGoogle Scholar
  55. Smith MS, Fridley JD, Goebel M, Bauerle TL (2014) Links between belowground and aboveground resource-related traits reveal species growth strategies that promote invasive advantages. PLoS ONE 9(8):e104189CrossRefGoogle Scholar
  56. Su YS, Yajima M (2015) R2jags: Using R to run ‘JAGS’. R package version 0.5-7Google Scholar
  57. Travert S, Valerio L, Fouraste I, Boudet AM, Teulieres C (1997) Enrichment in specific soluble sugars of two Eucalyptus cell-suspension cultures by various treatments enhances their frost tolerance via a noncolligative mechanism. Plant Physiol 114(4):1433–1442CrossRefGoogle Scholar
  58. Trischuk RG, Schilling BS, Low NH, Gray GR, Gusta LV (2014) Cold acclimation, de-acclimation and re-acclimation of spring canola, winter canola and winter wheat: the role of carbohydrates, cold-induced stress proteins and vernalization. Environ Exp Bot 106:156–163CrossRefGoogle Scholar
  59. van Kleunen M, Weber E, Fischer M (2010a) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13(2):235–245CrossRefGoogle Scholar
  60. van Kleunen M, Dawson W, Schlaepfer D, Jeschke JM, Fischer M (2010b) Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol Lett 13(8):947–958PubMedGoogle Scholar
  61. Wiley E, Helliker B (2012) A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol 195(2):285–289CrossRefGoogle Scholar
  62. Wolfe BE, Rodgers VL, Stinson KA, Pringle A (2008) The invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range. J Ecol 96(4):777–783CrossRefGoogle Scholar
  63. Yin J, Fridley JD, Smith M, Bauerle T (2015) Xylem vessel traits predict the leaf phenology of native and non-native understory species of temperate deciduous forests. Funct Ecol 30:206–214CrossRefGoogle Scholar
  64. Zohner CM, Benito BM, Fridley JD, Svenning JC, Renner SS (2017) Spring predictability explains different leaf-out strategies in the woody floras of North America, Europe and East Asia. Ecol Lett 20(4):452–460CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Biology DepartmentSyracuse UniversitySyracuseUSA

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