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Seasonal dry-down rates and high stress tolerance promote bamboo invasion above and below treeline

Abstract

How species invasions impact ecosystem structure and function at important ecotones or boundaries is unknown, but may provide insight into the impacts of climate change and the mechanisms underlying community change. The dwarf bamboo, Sasa kurilensis, may be a good system to understand these issues, as the species impacts ecosystem features as it encroaches beyond treeline into alpine systems. We used remote sensing imagery spanning a 35 year period to quantify S. kurilensis expansion patterns across its range, measured growth and stress tolerances of S. kurilensis above and below treeline, and evaluated components of growth to reveal how shifts in light and water limitations influence the ontogeny of height, branching, and leaf production. We show that S. kurilensis more than doubled its abundance across its range, but more than tripled its abundance near and above treeline. Soil dry-down rates were a key driver of invasion above and below treeline, where growth rates decreased with more rapid rates of soil moisture dry-down. We found S. kurilensis responds to competition and climate stress by increasing allocation to belowground structures at high elevations. Further, it invests more carbon in fewer—yet taller and heavier—aboveground structures in low-light, low elevation environments. It appears this species’ success is driven by considerable morphological and physiological flexibility, coupled with changes in water balance associated with snowmelt that in each habitat results in sites increasingly hospitable to bamboo. Overall, this study links resource allocation strategies and physiological responses to climate change and provides a mechanistic explanation of invasion success.

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References

  1. Allen CD, Breshears DD (1998) Drought-induced shift of a forest-woodland ecotone: rapid landscape response to climate variation. Proc Natl Acad Sci USA 95:14839–14842

  2. Amagai Y, Kaneko M, Kudo G (2015) Habitat-specific responses of shoot growth and distribution of alpine dwarf-pine (Pinus pumila) to climate variation. Ecol Res 30:969–977

  3. Angert AL, Huxman TE, Barron-Gafford GA, Gerst KL, Venable DL (2007) Linking growth strategies to long-term population dynamics in a guild of desert annuals. J Ecol 95:321–331

  4. Barnett TP, Adam JC, Lettenmaier DP (2005) Potential impacts of a warming climate on water availability in snow-dominated regions. Nature 438:303–309

  5. Belyea LR, Malmer N (2004) Carbon sequestration in peatland: patterns and mechanisms of response to climate change. Glob Change Biol 10:1043–1052

  6. Billings WD, Bliss LC (1959) An alpine snowbank environment and its effects on vegetation, plant development, and productivity. Ecology 40:388–397

  7. Bradley BA et al (2012) Global change, global trade, and the next wave of plant invasions. Front Ecol Environ 10:20–28

  8. Cable JM et al (2012) Shrub encroachment alters sensitivity of soil respiration to temperature and moisture. J Geophys Res Biogeosci 117:G01001

  9. Cadenasso ML, Pickett ST, Weathers KC, Bell SS, Benning TL, Carreiro MM, Dawson TE (2003) An interdisciplinary and synthetic approach to ecological boundaries. Bioscience 53:717–722

  10. Cannone N, Sgorbati S, Guglielmin M (2007) Unexpected impacts of climate change on alpine vegetation. Front Ecol Environ 5:360–364

  11. Chen IC et al (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026

  12. Colautti RI, Barrett SCH (2013) Rapid adaptation to climate facilitates range expansion of an invasive plant. Science 342:364–366

  13. Coulatti RI, Ricciardi A, Grigorovich IA, Maclsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

  14. Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Ann Rev Ecol Syst 33:507–559

  15. Drexler JZ, Knifong D, Tuil J, Flint LE, Flint AL (2013) Fens as whole-ecosystem gauges of groundwater recharge under climate change. J Hydrol 481:22–34

  16. Dullinger S, Dirnböck T, Grabherr G (2004) Modelling climate change-driven treeline shifts: relative effects of temperature increase, dispersal and invasibility. J Ecol 92:241–252

  17. Eldridge DJ et al (2011) Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis. Ecol Lett 14:709–722

  18. Etterson JR, Shaw RG (2001) Constraint to adaptive evolution in response to global warming. Science 294:151–154

  19. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Biol 40:503–537

  20. Franklin JF, Maeda T, Ohsumi Y, Matsui M, Yahi H (1979) Subalpine coniferous forests of central Honshu, Japan. Ecol Monogr 49:311–334

  21. Fujita H et al (2009) An inventory of the mires of Hokkaido, Japan—their development, classification, decline, and conservation. Plant Ecol 200:9–36

  22. Fynn RWS, Morris CD, Kirkman KP (2005) Plant strategies and trait trade-offs influence trends in competitive ability along gradients of soil fertility and disturbance. J Ecol 93:384–394

  23. Germino MJ, Smith WK, Resor AC (2002) Conifer seedling distribution and survival in an alpine-treeline ecotone. Plant Ecol 162:157–168

  24. González L, González-Vilar M (2001) Determination of relative water content. In: Reigosa Roger MJ (ed) Handbook of plant ecophysiology techniques. Springer, Netherlands, pp 207–212

  25. Gorham E (1991) Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol Appl 1:182–195

  26. Grant L, Seyfried M, McNamara J (2004) Spatial variation and temporal stability of soil water in a snow-dominated, mountain catchment. Hydrol Process 18:3493–3511

  27. Gremer JR, Kimball S, Keck KR, Huxman TE, Angert AL, Venable DL (2013) Water-use efficiency and relative growth rate mediate competitive interactions in Sonoran Desert winter annual plants. Am J Bot 100:2009–2015

  28. Harsch MA, Hulme PE, McGlone MS, Duncan RP (2009) Are treelines advancing? A global meta-analysis of treeline response to climate warming. Ecol Lett 12:1040–1049

  29. Herben T (2004) Physiological integration affects growth form and competitive ability in clonal plants. Evol Ecol 18:493–520

  30. Higa M et al (2013) Indicator plant species selection for monitoring the impact of climate change based on prediction uncertainty. Ecol Indic 29:307–315

  31. Holtmeier FK, Broll G (2005) Sensitivity and response of northern hemisphere altitudinal and polar treelines to environmental change at landscape and local scales. Glob Ecol Biogeogr 14:395–410

  32. Hudson JMG, Henry GHR (2009) Increased plant biomass in a High Arctic heath community from 1981 to 2008. Ecology 90:2657–2663

  33. Ishikawa M (2003) Thermal regimes at the snow-ground interface and their implications for permafrost investigation. Geomorphology 52:105–120

  34. Jump AS, Peñuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8:1010–1020

  35. Key T, Warner TA, McGraw JB, Faivan MA (2001) A comparison of multispectral and multitemporal information in high spatial resolution imagery for classification of individual tree species in a temperate hardwood forest. Remote Sens Environ 75:100–112

  36. Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7:69–80

  37. Körner C (1998) A re-assessment of high elevation treeline positions and their explanation. Oecologia 115:445–459

  38. Körner C (2012) Alpine treelines: functional ecology of the global high elevation tree limits. Springer, Basel

  39. Körner C, Farquhar GD, Wong SC (1991) Carbon isotope discrimination by plants follows latitudinal and altitudinal trends. Oecologia 88:30–40

  40. Kudo G, Ito K (1992) Plant distribution in relation to the length of the growing season in a snow-bed in the Taisetsu Mountains, Northern Japan. Vegetatio 92:165–174

  41. Kudo G, Amagai Y, Hoshino B, Kaneko M (2011) Invasion of dwarf bamboo into alpine snow-meadows in northern Japan: pattern of expansion and impact on species diversity. Ecol Evol 1:85–90

  42. Larkin DJ, Freyman MJ, Lishawa SC, Geddes P, Tuchman NC (2012) Mechanisms of dominance by the invasive hybrid cattail Typha × glauca. Biol Invasions 14:65–77

  43. Makita A (1992) Survivorship of a monocarpic bamboo grass, Sasa kurilensis, during the early regeneration process after mass flowering. Ecol Res 7:245–254

  44. Moyes AB, Castanha C, Germino MJ, Kueppers LM (2013) Warming and the dependence of limber pine (Pinus flexilis) establishment on summer soil moisture within and above its current elevation range. Oecologia 171:271–282

  45. Nagata O, Takakai F, Hatano R (2004) Effect of Sasa invasion on global warming potential in Sphagnum dominated poor fen in Bibai, Japan. Phyton 45:299–307

  46. Noguchi M, Yoshida T (2005) Factors influencing the distribution of two co-occuring dwarf bamboo species (Sasa kurilensis and S. senanensis) in a conifer-broadleaved mixed stand in northern Hokkaido. Ecol Res 20:25–30

  47. Numata M (1970) Conservation implications of bamboo flowering and death in Japan. Biol Cons 2:227–229

  48. Ohsawa M et al (1998) Impacts on natural ecosystems. In: Nishioka S, Harasaw H (eds) Global warming. Springer, Japan, pp 35–99

  49. Okitsu S, Ito K (1984) Vegetation dynamics of the Siberian dwarf pine (Pinus pumila Regel) in the Taisetsu mountain range, Hokkaido, Japan. Vegetatio 58:105–113

  50. Oshima Y (1961a) Ecological studies of Sasa communities. I. Productive structure of some of the Sasa communities in Japan. Bot Mag Tokyo 74:199–210

  51. Oshima Y (1961b) Ecological studies of Sasa communities. IV. Dry matter production and distribution of products among various organs in Sasa kurilensis. Bot Mag Tokyo 74:473–479

  52. Qing L, Yunxiang L, Zhangcheng Z (2004) Effects of moisture availability on clonal growth in bamboo Pleioblastus maculata. Plant Ecol 173:107–113

  53. R Core Team (2016) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna

  54. Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168:305–312

  55. Ricciardi A (2007) Are modern biological invasions an unprecedented form of global change? Conserv Biol 21:329–336

  56. Richards CL et al (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993

  57. Robinson D et al (2000) Using stable isotope natural abundance (δ15 N and δ13C) to integrate the stress responses of wild barley (Hordeum spontaneum C. Koch.) genotypes. J Exp Bot 51:41–50

  58. Scheffer M et al (2001) Catastrophic shifts in ecosystems. Nature 413:591–596

  59. Scott RL, Humxan TE, Williams DG, Goodrich DC (2006) Ecohydrological impacts of woody-plant encroachment: seasonal patterns of water and carbon dioxide exchange within a semiarid riparian environment. Glob Change Biol 12:311–324

  60. Sharp Z (2007) Principles of stable isotope geochemistry. Pearson Education, New Jersey

  61. Sloat LL, Henderson AN, Lamanna C, Enquist BJ (2015) The effect of foresummer drought on carbon exchange in subalpine meadows. Ecosystems 18:533–545

  62. Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260

  63. Sorte CJ et al (2013) Poised to prosper? A cross-system comparison of climate change effects on native and non-native species performance. Ecol Lett 16:261–270

  64. Sutherland WJ et al (2013) Identification of 100 fundamental ecological questions. J Ecol 101:58–67

  65. Takahashi N (1990) Environmental-geomorphological study on the Holocene mire development in the Daisetsuzan Mountains, Central Hokkaido, Northern Japan. Environ Sci Hokkaido Uni 13:93–156

  66. Taylor RV, Seastedt TR (1994) Short-and long-term patterns of soil moisture in alpine tundra. Arctic Alpine Res 26:14–20

  67. Townsend PA, Walsh SJ (2001) Remote sensing of forested wetlands: application of multitemporal and multispectral satellite imagery to determine plant community composition and structure in southeastern USA. Plant Ecol 157:129–149

  68. Toyooka H, Satoh A, Ishizuka M (1983) Distribution map of the Sasa group in Hokkaido, Explanatory note. Forestry and Forest Products Research Institute, Hokkaido Branch, Sapporo

  69. Tripathi SK et al (2006) Leaf litterfall and decomposition of difference above- and belowground parts of birch (Betula ermanii) trees and dwarf bamboo (Sasa kurilensis) shrubs in a young secondary forest in Northern Japan. Biol Fertil Soils 43:237–246

  70. Tsuyama I, Matsui T, Ogawa M, Kiminami Y, Tanaka N (2008) Habitat prediction and impact assessment of climate change on Sasa kurilensis in eastern Honshu, Japan. Theory Appl GIS 16:11–15

  71. Walker TN, Ward SE, Ostle NJ, Bardgett RD (2015) Contrasting growth responses of dominant peatland plants to warming and vegetation composition. Oecologia 178:141–151

  72. Weatherley PE (1950) Studies in the water relations of the cotton plant. I. The field measurement of water deficits in leaves. New Phytol 49:81–97

  73. Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14:569–580

  74. Wilson JR, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24:136–144

  75. Winkler DE, Chapin KJ, Kueppers LM (2016) Soil moisture mediates alpine life form and community productivity responses to warming. Ecology 97:1553–1563

  76. Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10

  77. Zhou J, Tachibana H (2004) Natural revegetation after elimination of disturbance of human treading in the Tennyogahara Mire, the Taisetsu Mountains, Japan. Veg Sci 21:65–78

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Acknowledgments

This material is based upon work supported by the National Science Foundation under Grant No. IIA-1414603 and the Japan Society for the Promotion of Science (JSPS) Summer Program to DE Winkler. Additional funding was provided by JSPS KAKENHI Grant Nos. 24570015 and 15K00524 to G Kudo. Special thanks to Y Mizunaga for field support, K. Huxman and N Yukino for logistical support, KJ Chapin for comments on earlier drafts of this manuscript, and Daisetsuzan National Park staff and resource managers.

Author information

Correspondence to Daniel E. Winkler.

Additional information

Communicated by Joseph Paul Messina

Appendix

Appendix

See Figs. 6 and 7.

Fig. 6
figure6

Satellite imagery analyses highlighting changes in Sasa kurilensis distributions in our alpine meadow site in 1977 (yellow outlines) and in 2012 (blue patches). Imagery reveals S. kurilensis expansion is occurring independent of trail locations and is increasingly common in backcountry areas where visitor access is not permitted

Fig. 7
figure7

Satellite imagery analyses highlighting 18 changes in Sasa kurilensis distributions in our subalpine mire site in 1977 (yellow outlines) and in 2012 (blue patches). Imagery reveals expansion is occurring beyond our focal site in the center of the image

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Winkler, D.E., Amagai, Y., Huxman, T.E. et al. Seasonal dry-down rates and high stress tolerance promote bamboo invasion above and below treeline. Plant Ecol 217, 1219–1234 (2016). https://doi.org/10.1007/s11258-016-0649-y

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Keywords

  • Alpine
  • Altitudinal shift
  • Climate change
  • Snowmelt
  • Soil moisture
  • Subalpine