, Volume 55, Issue 2, pp 219–230 | Cite as

Ecophysiological responses of native invasive woody Juniperus virginiana L. to resource availability and stand characteristics in the semiarid grasslands of the Nebraska Sandhills

  • J. Msanne
  • T. Awada
  • N. M. Bryan
  • W. Schacht
  • R. Drijber
  • Y. Li
  • X. Zhou
  • J. Okalebo
  • D. Wedin
  • J. Brandle
  • J. Hiller
Open Access
Original Paper


Vegetation in grasslands is changing at an unprecedented rate. In the Nebraska Sandhills, this shift is attributed in part to encroachment of the woody species Juniperus virginiana. We investigated changes in resource availability and their feedback on seasonal trends in photosynthetic characteristics of J. virginiana trees scattered in open grasslands vs. a dense 57-year-old stand. Dense stand exhibited lower volumetric soil water content, NH4 +, NO3 , and δ13C, as well as foliage δ13C, δ15N, and N content, compared to grasslands. Water potential was higher in trees in grasslands compared to dense stand. J. virginiana in dense stand exhibited similar trends to trees in grasslands for net photosynthetic rate (P N), stomatal conductance, transpiration, maximum photochemical efficiency of PSII, maximum carboxylation velocity, and maximum rate of electron transport. P N peaked early summer and declined in the fall, with trees in open grasslands lagging behind those in dense stand. Plasticity of this species may place it at a competitive advantage in the Sandhills, further altering grasslands vegetation and ecosystem processes.

Additional key words

carboxylation velocity eastern red cedar electron transport fluorescence gas exchange isotope ratio soil nutrients 





intercellular CO2 concentration


vapor pressure deficit between the leaf and air


diameter at breast height


day of year




minimal fluorescence yield of the dark-adapted state


maximal fluorescent yield of the dark-adapted state


variable fluorescence


maximum quantum efficiency of PSII


stomatal conductance


rate of electron transport




Nebraska National Forest


net primary production


net photosynthetic rate


photosynthetic nitrogen-use efficiency


temperature of the air


temperature of the leaf


maximum carboxylation velocity


volumetric soil water content


water-use efficiency


carbon isotope ratio


nitrogen isotope ratio


predawn water potential


midday water potential


water potential


  1. Archer S.R: Woody plant encroachment into southwestern grasslands and savannas: rates, patterns and proximate causes. — In: Vavra M., Laycock W.A., Pieper R.D. (ed.): Ecological Implications of Livestock Herbivory in the West. Pp. 13–68. Soc. Range Manage., Denver 1994.Google Scholar
  2. Archer S.R.: Rangeland conservation and shrub encroachment: new perspectives on an old problem. — In: du Toit J.T., Kock R., Deutsch J.C. (ed.): Wild Rangelands: Conserving Wildlife While Maintaining Livestock in Semi-arid Ecosystems. Pp. 53–97. John Wiley and Sons Ltd., Chichester 2010.CrossRefGoogle Scholar
  3. Archer S.R.: Tree-grass dynamics in a Prosopis-thornscrub savanna parkland: Reconstructing the past and predicting the future. — Ecoscience 2: 83–99, 1995.CrossRefGoogle Scholar
  4. Archer S.R., Predick K.I.: An ecosystem services perspective on brush management: research priorities for competing land use objectives. — J. Ecol. 102: 1394–1407, 2014.CrossRefGoogle Scholar
  5. Awada T., El-Hage R., Geha M. et al.: Intra-annual variability and environmental controls over transpiration in a 58-year-old even-aged stand of invasive woody Juniperus virginiana L. in the Nebraska Sandhills, USA. — Ecohydrology 6: 731–740, 2013.Google Scholar
  6. Bestelmeyer B.T., Okin G.S., Duniway M.C. et al.: Desertification, land use, and the transformation of global drylands. — Front. Ecol. Environ. 13: 28–36, 2015.CrossRefGoogle Scholar
  7. Bihmidine S., Bryan N.M., Payne K.R. et al.: Photosynthetic performance of invasive Pinus ponderosa and Juniperus virginiana seedlings under gradual soil water depletion. — Plant Biol. 12: 668–675, 2010.PubMedGoogle Scholar
  8. Bihmidine S., Cao M., Kang M. et al.: Expression of the Chlorovirus MT325 aquaglyceroporin (aqpv1) in tobacco and its role in mitigating drought stress. — Planta 240: 209–221, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Billings S.A.: Soil organic matter dynamics and land use change at a grassland/forest ecotone. — Soil Biol. Biochem. 38: 2934–2943, 2006.CrossRefGoogle Scholar
  10. Binggeli P.: A taxonomic, biogeographical and ecological overview of invasive woody plants. — J. Veg. Sci. 7: 121–124, 1996.CrossRefGoogle Scholar
  11. Bleed A.S., Flowerday C.A.: An Atlas of the Sandhills. Pp. 260. Conservation and Survey Division, University of Nebraska, Lincoln 1998.Google Scholar
  12. Bond W.J.: What limits trees in C4 grasslands and savannas? — Annu. Rev. Ecol. Syst. 39: 641–659, 2008.CrossRefGoogle Scholar
  13. Boutton T.W., Liao J.D.: Changes in soil nitrogen storage and δ15N with woody plant encroachment in a subtropical savanna parkland landscape. — J. Geophys. Res 115: G03019, 2010.CrossRefGoogle Scholar
  14. Briggs J.M., Knapp A.K., Blair J.M. et al.: An ecosystem in transition: causes and consequences of the conversion of mesic grassland to shrubland. — BioScience 55: 243–254, 2005.CrossRefGoogle Scholar
  15. Brooks M.L., D'Antonio C.M., Richardson D.M. et al.: Effects of invasive alien plants on fire regimes. — BioScience 54: 677–688, 2004.CrossRefGoogle Scholar
  16. Caterina G.L., Will R.E., Turton D.J. et al.: Water use of Juniperus virginiana trees encroached into mesic prairies in Oklahoma, USA. — Ecohydrology 7: 1124–1134, 2014.Google Scholar
  17. Chapin F.S., Matson P.A., Vitousek P.: Principles of Terrestrial Ecosystem Ecology. Pp. 123–181. Springer-Verlag, New York 2011.CrossRefGoogle Scholar
  18. Chapin F.S., Sala O.E., Burke I.C. et al.: Ecosystem consequences of changing biodiversity. — BioScience 48: 45–52, 1998.CrossRefGoogle Scholar
  19. Craine J.M., Ocheltree T.W., Nippert J.B. et al.: Global diversity of drought tolerance and grassland climate-change resilience. — Nat. Clim. Change 3: 63–67, 2013.CrossRefGoogle Scholar
  20. Dray S., Dufour A.B.: The ade4 package: implementing the duality diagram for ecologists. — J. Stat. Softw. 22: 1–20, 2007.CrossRefGoogle Scholar
  21. D’Antonio C.M., Vitousek P.M.: Biological invasions by exotic grasses, the grass/fire cycle, and global change. — Annu. Rev. Ecol. Syst. 23: 63–87, 1992.CrossRefGoogle Scholar
  22. Diez J.M., D’Antonio C.M., Dukes J.S. et al.: Will extreme climatic events facilitate biological invasions? — Front. Ecol. Environ. 10: 249–257, 2012.CrossRefGoogle Scholar
  23. Dobson A.P., Bradshaw A.D., Baker J.M.: Hopes for the future: restoration ecology and conservation biology. — Science 277: 515–525, 1997.CrossRefGoogle Scholar
  24. Eggemeyer K.D., Awada T., Harvey F.E. et al.: Seasonal changes in depth of water uptake for encroaching trees Juniperus virginiana and Pinus ponderosa and two dominant C4 grasses in a semiarid grassland. — Tree Physiol. 29: 157–169, 2009.CrossRefPubMedGoogle Scholar
  25. Eggemeyer K.D., Awada T., Wedin D.A. et al.: Ecophysiology of two native invasive woody species and two dominant warmseason grasses in the semiarid grasslands of the Nebraska Sandhills. — Int. J. Plant Sci. 167: 991–999, 2006.CrossRefGoogle Scholar
  26. Ehleringer J.R., Field C.B., Lin Z.F., Kuo C.Y.: Leaf carbon isotope and mineral composition in subtropical plants along an irradiance cline. — Oecologia 70: 520–526, 1986.CrossRefGoogle Scholar
  27. Ganguli A.C., Engle D.M., Mayer P.M., Hellgren E.C.: Plant community diversity and composition provide little resistance to Juniperus encroachment. — Botany 86: 1416–1426, 2008.CrossRefGoogle Scholar
  28. Ganguli A.C., Engle D.M., Mayer P.M., Salo L.F.: Influence of resouce availability on Juniperus virginiana expansion in a forest-prairie ecotone. — Ecosphere 7:e01433, 2016.CrossRefGoogle Scholar
  29. Givnish T.J.: Adaptation to sun and shade: A whole-plant perspective. — Aus. J. Plant Physiol. 15: 63–92, 1988.CrossRefGoogle Scholar
  30. Hamada S., Kumagai T., Kochi K. et al.: Spatial and temporal variations in photosynthetic capacity of a temperate deciduousevergreen forest. — Trees 30: 1083–1093, 2016.CrossRefGoogle Scholar
  31. Helmink S.: Nebraska Forest Service Annual Report. Pp. 10–12. University of Nebraska, Lincoln 2012.Google Scholar
  32. Huxman T.E., Wilcox B.P., Breshears D.D. et al.: Ecohydrological implications of woody plant encroachment. — Ecology 86: 308–319, 2005.CrossRefGoogle Scholar
  33. Jackson R.B., Banner J.L., Jobbágy E.G. et al.: Ecosystem carbon loss with woody plant invasion of grasslands. — Nature 418: 623–626, 2002.CrossRefPubMedGoogle Scholar
  34. Kassambara A.: Factoextra: Visualization of the outputs of a multivariate analysis. R package version 1, kassambara/factoextra, 2015.Google Scholar
  35. Li Y., Awada T., Zhou X. et al.: Mongolian pine plantations enhance soil physico-chemical properties and carbon and nitrogen capacities in semi-arid degraded sandy land in China. — Appl. Soil Ecol. 56: 1–9, 2012.CrossRefGoogle Scholar
  36. Liang Z., Drijber R.A., Lee D.J. et al.: A DGGE-cloning method to characterize arbuscular mycorrhizal community structure in soil. — Soil Biol. Biochem. 40: 956–966, 2008.CrossRefGoogle Scholar
  37. Liao C., Peng R., Luo Y. et al.: Altered ecosystem carbon and nitrogen cycles by plant invasion: A meta-analysis. — New Phytol. 177: 706–714, 2008.CrossRefPubMedGoogle Scholar
  38. Liu F., Archer S.R., Gelwick F. et al.: Woody plant encroachment into grasslands: spatial patterns of functional group distribution and community development. — PLoS ONE 8: e84364, 2013.CrossRefGoogle Scholar
  39. Long S.P., Bernacchi C.J.: Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. — J. Exp. Bot. 54: 2393–2401, 2003.CrossRefPubMedGoogle Scholar
  40. McCulley R.L., Jackson R.B.: Conversion of tallgrass prairie to woodland: consequences for carbon and nitrogen cycling. — Am. Midl. Nat. 167: 307–321, 2012.CrossRefGoogle Scholar
  41. McKinley D.C.: Consequences of Conversion of Native Mesic Grassland to Coniferous Forest on Soil Proceses and Ecosystem C and N storage. Pp. 186. Kansas State University, Manhattan 2007.Google Scholar
  42. McKinley D.C., Blair J.M.: Woody plant encroachment by Juniperus virginiana in a mesic native grassland promotes rapid carbon and nitrogen accrual. — Ecosystems 11: 454–468, 2008.CrossRefGoogle Scholar
  43. McKinley D.C., Rice C.W., Blair J.M.: Conversion of grassland to coniferous woodland has limited effects on soil nitrogen cycle processes. — Soil Biol. Biochem. 40: 2627–2633, 2008.CrossRefGoogle Scholar
  44. Mellor N.J., Hellerich J., Drijber R. et al.: Changes in ecosystem carbon following afforestation of native sand prairie. — Soil Sci. Soc. Am. J. 77: 1613–1624, 2013.CrossRefGoogle Scholar
  45. Miyazawa Y., Kikuzawa K., Otsuki K.: Decrease in the capacity of RuBP carboxylation and regeneration with the progession of cold-induced photoinhibition during winter evergreen broadleaf tree species in a temperate forest. — Funct. Plant Biol. 34: 393–401, 2007.CrossRefGoogle Scholar
  46. Muller O., Oguchi R., Hirose T. et al.: The anatomy of a broadleaved evergreen allows an increase in leaf nitrogen content in winter. — Physiol. Plantarum 136: 299–309, 2009.CrossRefGoogle Scholar
  47. Nippert J.B., Ocheltree T.W., Orozco G.L. et al.: Evidence of physiological decoupling from grassland ecosystem drivers by an encroaching woody shrub. — PLoS ONE 8: e81630, 2013.CrossRefGoogle Scholar
  48. Norris M.D., Blair J.M., Johnson L.C.: Altered ecosystem nitrogen dynamics as a consequence of land cover change in tallgrass prairie. — Am. Midl. Nat. 158: 432–445, 2007.CrossRefGoogle Scholar
  49. Norris M.D., Blair J.M., Johnson L.C., McKane R.B.: Assessing changes in biomass, productivity, and C and N stores following Juniperus virginiana forest expansion into tallgrass prairie. — Can. J. Forest Res. 31: 1940–1946, 2001.CrossRefGoogle Scholar
  50. Pacala S.W., Hurtt G.C., Baker D. et al.: Consistent land-and atmosphere-based U.S. carbon sink estimates. — Science 292: 2316–2320, 2001.CrossRefPubMedGoogle Scholar
  51. Pardo L.H., Hemond H.F., Montoya J.P., Siccama T.G.: Response of the natural abundance of 15N in forest soils and foliage to high nitrate loss following clear-cutting. — Can. J. Forest Res. 32: 1126–1136, 2002.CrossRefGoogle Scholar
  52. Pierce A.M., Reich P.B.: The effects of eastern red cedar (Juniperus virginiana) invasion and removal on a dry bluff prairie ecosystem. — Biol. Invasions 12: 241–252, 2010.CrossRefGoogle Scholar
  53. Rout M.E., Callaway R.M.: An invasive plant paradox. — Science 324: 734–735, 2009.CrossRefPubMedGoogle Scholar
  54. Sharkey T.D., Bernacchi C.J., Farquhar G.D., Singsaas E.L.: Fitting photosynthetic carbon dioxide response curves for C3 leaves. — Plant Cell Environ. 30: 1035–1040, 2007.CrossRefPubMedGoogle Scholar
  55. Shinneman D.J., Baker W.L.: Nonequilibrium dynamics between catastrophic disturbances and old-growth forests in ponderosa landscapes of the Black Hills. — Conserv. Biol. 11: 1276–1288, 1997.CrossRefGoogle Scholar
  56. Starks P.J., Venuto B.C., Dugas W.A., Kiniry J.: Measurements of canopy interception and transpiration of eastern redcedar grown in open environments. — Environ. Nat. Resour. Res. 4: 103–122, 2014.Google Scholar
  57. Szilagyi J., Harvey F.E., Ayers J.F.: Regional estimation of total recharge to ground water in Nebraska. — Ground Water 43: 63–69, 2005.CrossRefPubMedGoogle Scholar
  58. Throop H.L., Archer S.R., Monger H.C., Waltman S.: When bulk density methods matter: Implications for estimating soil organic carbon pools in rocky soils. — J. Arid Environ. 77: 66–71, 2012.CrossRefGoogle Scholar
  59. Twidwell D., Rogers W.E., Fuhlendorf S.D. et al.: The rising Great Plains fire campaign: citizens’ response to woody plant encroachment. — Front. Ecol. Environ. 11: e64–e71, 2013.CrossRefGoogle Scholar
  60. van der Sleen P., Vlam M., Groenendijk P. et al.: 15N in tree rings as a bio-indicator of changing nitrogen cycling in tropical forests: an evaluation at three sites using two sampling methods. — Front. Plant Sci. 6: 229, 2015.PubMedPubMedCentralGoogle Scholar
  61. Volder A., Tjoelker M., Briske D.: Contrasting physiological responsiveness of establishing trees and a C4 grass to rainfall events, intensified summer drought, and warming in oak savanna. — Glob. Change Biol. 16: 3349–3362, 2010.CrossRefGoogle Scholar
  62. Walker B.H., Noy-Meir I.: Aspects of the stability and resilience of savanna ecosystems. — Ecol. Stud. 42: 556–590, 1982.CrossRefGoogle Scholar
  63. Wilcox B.P.: Transformative ecosystem change and ecohydrology: ushering in a new era for watershed management. — Ecohydrology 3: 126–130, 2010.Google Scholar
  64. Williams R.J., Hallgren S.W., Wilson G.W.T., Palmer M.W.: Juniperus virginiana encroachment into upland oak forests alters arbuscular mycorrhizal abundance and litter chemistry. — Appl. Soil Ecol. 65: 23–30, 2013.CrossRefGoogle Scholar
  65. Willson C.J., Manos P.S., Jackson R.B.: Hydraulic traits are influenced by phylogenetic history in the drought-resistant invasive genus Juniperus (Cupressaceae). — Am. J. Bot. 95: 299–314, 2008.CrossRefPubMedGoogle Scholar
  66. Wilson K.B., Baldocchi D., Hanson P.J.: Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. — Tree Physiol. 20: 565–573, 2000.CrossRefPubMedGoogle Scholar
  67. Yahdjian L., Sala O.E., Havstad K.M.: Rangeland ecosystem services: shifting focus from supply to reconciling supply and demand. — Front. Ecol. Environ. 13: 44–51, 2015.CrossRefGoogle Scholar
  68. Zou C.B., Turton D.J., Will R.E. et al.: Alteration of hydrological processes and streamflow with juniper (Juniperus virginiana) encroachment in a mesic grassland catchment. — Hydrol. Process. 28: 6173–6182, 2014.CrossRefGoogle Scholar

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© The Author(s) 2017

Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

Authors and Affiliations

  • J. Msanne
    • 1
  • T. Awada
    • 1
  • N. M. Bryan
    • 1
  • W. Schacht
    • 1
    • 2
  • R. Drijber
    • 2
  • Y. Li
    • 3
  • X. Zhou
    • 1
    • 4
  • J. Okalebo
    • 1
  • D. Wedin
    • 1
  • J. Brandle
    • 1
  • J. Hiller
    • 1
  1. 1.School of Natural ResourcesUniversity of NebraskaLincolnUSA
  2. 2.Department of Agronomy and HorticultureUniversity of NebraskaLincolnUSA
  3. 3.Cold and Arid Regions Environmental and Engineering Research InstituteChinese Academy of SciencesLanzhouChina
  4. 4.Campbell Scientific Inc.LoganUSA

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