Advertisement

Biological Invasions

, Volume 17, Issue 6, pp 1729–1742 | Cite as

Patterns of herbivory-induced mortality of a dominant non-native tree/shrub (Tamarix spp.) in a southwestern US watershed

  • Kevin R. HultineEmail author
  • Tom L. Dudley
  • Dan F. Koepke
  • Daniel W. Bean
  • Ed P. Glenn
  • Adam M. Lambert
Original Paper

Abstract

The capacity for plant species or populations to cope with herbivory depends in large part on the complex interactions between resource availability, life history and adaptive strategies to maximize defense and/or tolerance to herbivory. Given these complex interactions, the impacts of repeated herbivory on plant stress and subsequent mortality is often difficult to predict. To better understand relationships between herbivory and environmental condition, we studied the relationship between the non-native shrub/tree tamarisk (Tamarix spp.) and a specialist herbivore, the northern tamarisk leaf beetle (Diorhabda carinulata) released as a biological control agent of Tamarix in the Virgin River watershed in the southwestern United States. The beetle feeds exclusively on Tamarix foliage resulting in complete stand foliage desiccation (i.e. defoliation) that lasts several weeks. Approximately 900 Tamarix plants were surveyed over three consecutive growing seasons for canopy dieback and mortality across 10 sites varying in the number of defoliation events, tree height, soil salinity, soil texture and bulk leaf carbon isotope ratios (δ13C). Canopy dieback increased from 27 % by volume in the spring of 2012 to 41 % and 54 % in 2013 and 2014, respectively. Tree mortality increased from 0 % in 2012 to 6 % and 10 % in 2013 and 2014, respectively. Surprisingly, percent canopy dieback was not related to the number of defoliation events that ranged from 2 to 7 across the 10 sites prior to the 2013 growing season. On the other hand, canopy dieback increased with soil salinity in both 2013 (R 2 = 0.39, F = 5.07, P = 0.055) and 2014 (R 2 = 0.56, F = 10.26, P = 0.015). Canopy dieback in 2013 increased with bulk leaf δ13C (R 2 = 0.38, F = 4.08, P = 0.078), although δ13C also decreased with the number of defoliation events (R 2 = 0.64, F = 14.17, P = 0.0055), suggesting that photosynthetic rate or drought stress (as indicated by leaf δ13C) may serve as a poor predictor for Tamarix canopy dieback in response to defoliation. Percent canopy dieback was correlated with shifts in NDVI measured from annual MODIS imagery (R 2 = 0.61, F = 12.32, P = 0.008), demonstrating that the tree surveys reflect site-scale changes in canopy cover. Results show that patterns of Tamarix canopy dieback and subsequent mortality following episodic defoliation by D. carinulata are likely to vary across broad gradients in soil salinity and other abiotic and biotic factors. Documented impacts of this biocontrol agent reported here will aid management efforts aimed at preserving riparian habitat in the short-term with conservation efforts targeting the removal and control of Tamarix over the long term.

Keywords

Plant mortality Tamarix Diorhabda carinulata δ13MODIS Riparian ecosystems 

Notes

Acknowledgments

Thanks to B. Klink and D. Orr for assistance with field monitoring. Thanks to D. Dehn and V. Nixon for technical assistance. This research was supported by a grant from the Bureau of Reclamation, Desert Landscape Conservation Cooperative (Agreement Number R12AP80909).

References

  1. Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD et al (2009) Temperature sensitivity of drought-induced tree mortality: implications for regional-die-off under global-change-type drought. Proc Nat Acad Sci 106:7063–7066CrossRefPubMedCentralPubMedGoogle Scholar
  2. Allen CA, Macalady AK, Chenchouni H, Bachelet D, McDowell N et al (2010) A global review of drought and heat-induced tree mortality reveals emerging climate change risks in forests. For Ecol Manag 259:660–684CrossRefGoogle Scholar
  3. Armas C, Padilla FM, Pugnaire FI, Jackson RB (2009) Hydraulic lift and tolerance to salinity of semiarid species: consequences for species interactions. Oecologia 162:11–21CrossRefGoogle Scholar
  4. Ayres MP (1993) Plant defense, herbivory, and climate change. In: Kareiva PM, Kingsolver JG, Huey RB (eds) Biotic interactions and global change. Sinauer Associates, Sunderland, MA, pp 75–94Google Scholar
  5. Bateman HL, Dudley TL, Bean DW, Ostoja SM, Hultine KR, Kuehn MJ (2010) A river system to watch: documenting the effects of saltcedar (Tamarix spp.) biocontrol in the Virgin River Valley. Ecol Res 28:405–410CrossRefGoogle Scholar
  6. Bean DW, Dalin P, Dudley TL (2012) Evolution of critical day length for diapause induction enables range expension of Diorhabda carinulata, a biological control agent against tamarisk (Tamarix spp.). Evol App 5:511–523CrossRefGoogle Scholar
  7. Bean D, Dudley T, Hultine K (2013) Bring on the Beetles! In: Sher A, Quigley MF (eds) Tamarix: a case study of ecological change in the American West. Oxford University Press, OxfordGoogle Scholar
  8. Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants-an economic analogy. Ann Rev Ecol Syst 16:363–392Google Scholar
  9. Breshears DD, Cobb NS, Rich PM, Price KP, Allen CD et al (2005) Regional vegetation die-off in response to global-change-type drought. Proc Nat Acad Sci 102:15144–15148CrossRefPubMedCentralPubMedGoogle Scholar
  10. Breshears DD, Myers OB, Meyer CW, Barnes FJ, Zou CB et al (2009) Tree die-off in response to global-change-type drought: mortality insights from a decade of plant water potential measurements. Fron Ecol Environ 7:185–189CrossRefGoogle Scholar
  11. Chapin FS III, Shulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Ann Rev Ecol Syst 21:423–447CrossRefGoogle Scholar
  12. Coley PD, Bryant JP, Chapin SF III (1985) Resource availability and plant antiherbivore defense. Science 230:895–899CrossRefPubMedGoogle Scholar
  13. Cooke BJ, Nealis VG, Régnière J (2007) Insect defoliators as periodic disturbances in northern forest ecosystems. In: Johnson EA, Miyanishi K (eds) Plant disturbance ecology: the process and the response. Elsevier Academic Press, Burlington, MA, pp 487–525Google Scholar
  14. DeLoach CJ, Lewis PA, Herr JC, Carruthers RI, Tracy JL, Johnson J (2003) Host specificity of the leaf beetle, Diorhabda elongata desrticola (Coleoptera: Chrysomelidae) from Asia, a biocontrol agent for saltcedars (Tamarix: Tamaricaceae) in the Western United States. Biol Con 27:117–147CrossRefGoogle Scholar
  15. Dennison PE, Nagler PL, Hultine KR, Glenn EP, Ehleringer JR (2009) Remote monitoring of tamarisk defoliation and evapotranspiration following saltcedar leaf beetle attack. Remote Sen Environ 113:1462–1472CrossRefGoogle Scholar
  16. Dudley TL (2005) Progress and pitfalls in the biological control of saltcedar (Tamarix spp.) in North America. In: Proceedings of the 16th U.S. Department of Agriculture interagency research forum on gypsy moth and other invasive species; 18–21 Jan 2005; Annapolis, MD. Morgantown WV: USDA Forest Service. General technical report NE-337Google Scholar
  17. Dudley TL, Bean DW (2012) Tamarisk biocontrol, endangered species effects and resolution of conflict through riparian restoration. Biol Con 57:331–347Google Scholar
  18. Ehleringer JR (1991) 13C/12C fractionation and its utility in terrestrial plant studies. In: Coleman DC, Fry B (eds) Carbon isotope techniques. Academic Press, New York, pp 187–200CrossRefGoogle Scholar
  19. Evans JR, Seemann JR (1989) The allocation of protein N in the photosynthetic apparatus costs, consequences, and control. In: Briggs WR (ed) Photosynthesis. Alan R Liss, New York, pp 183–205Google Scholar
  20. Friedman JM, Auble GT, Shafroth PB, Scott ML, Merigliano MF, Freehling MD, Griffin ER (2005) Dominance of non-native riparian trees in the western USA. Biol Inv 7:747–751CrossRefGoogle Scholar
  21. Gaskin JF, Schaal BA (2002) Hybrid Tamarix widespread in U.S. invasion and undetected in native Asian range. Proc Nat Acad Sci 99:11256–11259CrossRefPubMedCentralPubMedGoogle Scholar
  22. Gaskin JF, Birken AS, Cooper DJ (2012) Levels of novel hybridization in the saltcedar invasion compared over seven decades. Biol Inv 14:693–699CrossRefGoogle Scholar
  23. Gee GW, Bauder JW (1979) Particle size analysis by hydrometer: a simplified method for routine textural analysis and a sensitivity test of measurement parameters. Soil Sci Soc Am J 43:1004–1007CrossRefGoogle Scholar
  24. Glenn EP, Tanner R, Mendez S, Kehret T, Moore D, Garcia J, Valdez C (1998) Growth rates, salt tolerance and water use characteristics of native and invasive riparian plants from the delta of the Colorado River delta, Mexico. J Arid Environ 40:281–294CrossRefGoogle Scholar
  25. Glenn EP, Nelson SG, Ambrose B, Martinez R, Soliz D, Pabendinskas V, Hultine K (2012a) Comparison of salinity tolerance of three Atriplex spp. in well-watered and drying soils. Environ Exp Bot 83:62–72CrossRefGoogle Scholar
  26. Glenn EP, Morino K, Nagler PL, Murray RS, Pearlstein S, Hultine KR (2012b) Roles of saltcedar (Tamarix spp.) and capillary rise in salinizing a non-flooding terrace on a flow-regulated desert river. J Arid Environ 79:56–65CrossRefGoogle Scholar
  27. Glenn EP, Nagler PL, Morino K, Hultine KR (2013) Phreatophytes under stress: transpiration and stomatal conductance of saltcedar (Tamarix spp.) in a high-salinity environment. Plant Soil 371:655–672CrossRefGoogle Scholar
  28. Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081CrossRefGoogle Scholar
  29. Hultine KR, Dudley TL (2013) Tamarix from organism to landscape. In: Sher A, Quigley MF (eds) Tamarix: a case study of ecological change in the American West. Oxford University Press, OxfordGoogle Scholar
  30. Hultine KR, Belnap J, van Riper IIIC, Ehleringer JR, Dennison PE, Lee ME, Nagler PL, Snyder KA, Uselman SM, West JB (2010) Tamarisk biocontrol in the western United States: ecological and societal implications. Fron Ecol Env 8:467–474CrossRefGoogle Scholar
  31. Hultine KR, Dudley TL, Leavitt SW (2013) Herbivory-induced mortality increases with radial growth in an invasive riparian phreatophyte. Ann Bot 111:1197–1206CrossRefPubMedCentralPubMedGoogle Scholar
  32. Imada S, Archarya K, Yp Li, Taniguchi T, Iwanaga F, Yamamoto F, Yamanaka N (2013) Salt dynamics in Tamarix ramosissima in the lower Virgin River floodplain, Nevada. Trees 27:949–958CrossRefGoogle Scholar
  33. Jolly I, McWan K, Holland K (2008) A review of groundwater-surface water interactions in arid/semi-arid wetlands and the consequence for wetland ecology. Ecohydrology 1:43–58CrossRefGoogle Scholar
  34. Koepke DF, Kolb TE, Adams HD (2010) Variation in woody plant mortality and dieback from severe drought among soils, plant groups, and species within a northern Arizona ecotone. Oecologia 163:1079–1090CrossRefPubMedGoogle Scholar
  35. Lichtenthaler HK (1998) The stress concept in plants: an introduction. Ann N Y Acad Sci 851:187–198CrossRefPubMedGoogle Scholar
  36. Looney CE, Sullivan BW, Kolb TE, Kane JM, Hart SC (2012) Pinyon pine (Pinus edulis) mortality and response to water additions across a three million year substrate age gradient in northern Arizona, USA. Plant Soil 357:89–102CrossRefGoogle Scholar
  37. Manion PD (1991) Tree disease concepts, 2nd edn. Prentice-Hall, Upper Saddle River, NJ, USA 416pGoogle Scholar
  38. Merritt DM, Shafroth PB (2012) Edaphic, salinity, and stand structural trends in chronosequence of native and non-native dominated riparian forests along the Colorado River, USA. Biol Inv 14:2665–2685CrossRefGoogle Scholar
  39. Nagler PL, Brown T, Hultine KR, van Riper IIIC, Bean DW, Dennison PE, Murray RS, Glenn EP (2012) Regional scale impacts of Tamarix leaf beetles (Diorhabda carinulata) on the water availability of western U.S. rivers as determined by multiscale remote sensing methods. Remote Sen Environ 118:227–240CrossRefGoogle Scholar
  40. Nagler PL, Pearlstein S, Glenn EP, Brown TB, Bateman HL, Bean DW, Hultine KR (2014) Rapid dispersal of saltcedar (Tamarix spp.) biocontrol beetles (Diorhabda carinulata) on a desert river detected by phenocams, MODIS imagery and ground detection. Remote Sen Environ 140:206–219CrossRefGoogle Scholar
  41. Oren R, Sperry JS, Katul G, Pataki DE, Ewers BE, Phillips N, Schäfer KVR (1999) Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant Cell Environ 22:1515–1526CrossRefGoogle Scholar
  42. Pataki DE, Oren R, Phillips N (1998) Responses of sap flux and stomatal conductance of Pinus taeda L. trees to stepwise reductions in leaf area. J Exp Bot 49:871–878CrossRefGoogle Scholar
  43. Pataki DE, Bush SE, Gardener P, Solomon DK, Ehleringer JR (2005) Ecohydrology in a Colorado River riparian forest: implications for the decline of Populus femontii. Ecol Appl 15:1009–1018CrossRefGoogle Scholar
  44. Pattison RR, D’Antonio CM, Dudley TL (2011) Biological control reduces the growth, and alters water relations of the saltcedar tree (Tamarix spp.) in western Nevada, USA. J Arid Environ 75:346–352CrossRefGoogle Scholar
  45. Paxton EH, Theimer TC, Sogge MK (2011) Tamarisk biocontrol using tamarisk leaf beetles: potential consequences for riparian birds in the southwestern United States. The Condor 113:255–265CrossRefGoogle Scholar
  46. Rouse JW, Haas RS, Schell JA, Deering DW (1973) Monitoring vegetation systems in the Great Plains with ERTS. Proc 3rd ERTS Symp 1:48–62Google Scholar
  47. Ruel J, Whitham TG (2002) Fast-growing juvenile pinions suffer greater herbivory when mature. Ecology 83:2691–2699CrossRefGoogle Scholar
  48. Sala A, Woodruff DR, Meinzer F (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32:764–775CrossRefPubMedGoogle Scholar
  49. Shafroth PB, Cleverly JR, Dudley TL, Taylor JP, van Riper IIIC, Weeks EP, Stuart JN (2005) Control of Tamarix spp. In the western US: implications for water salvage, wildlife use, and riparian restoration. Environ Manag 35:231–246CrossRefGoogle Scholar
  50. Shah SHH, Vervoort RW, Suweis S, Guswa AJ, Rinaldo A, van der Zee SEATM (2011) Stochastic modeling of salt accumulation in the root zone due to capillary flux from brackish groundwater. Water Resour Res 47. doi: 10.1029/2010WR009790
  51. Sthultz CM, Gehring CA, Whitham TG (2009) Deadly combination of genes and drought: increased mortality of herbivory-resistant trees in a foundation species. Global Change Biol 15:1949–1961CrossRefGoogle Scholar
  52. Stromberg JC (2013) Root patterns and hydrogeomorphic niches of riparian plants in the American Southwest. J Arid Environ 94:1–9CrossRefGoogle Scholar
  53. Uselman SM, Snyder KA, Blank RR (2011) Insect biological control accelerates leaf litter decomposition and alters short-term nutrient dynamics in a Tamarix-invaded riparian ecosystem. Oikos 120:409–417CrossRefGoogle Scholar
  54. van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF et al (2009) Widespread increase of tree mortality rates in the western United States. Science 323:521–524CrossRefPubMedGoogle Scholar
  55. Warren CR, Adams MA (2006) Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant Cell Environ 29:192–201CrossRefPubMedGoogle Scholar
  56. Williams WI, Friedman JM, Gaskin JF, Norton AP (2014) Hybridization of an invasive shrub affects tolerance and resistance to defoliation by a biological control agent. Evol Appl 7:381–393CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Kevin R. Hultine
    • 1
    Email author
  • Tom L. Dudley
    • 2
  • Dan F. Koepke
    • 1
  • Daniel W. Bean
    • 3
  • Ed P. Glenn
    • 4
  • Adam M. Lambert
    • 2
  1. 1.Department of Research, Conservation and CollectionsDesert Botanical GardenPhoenixUSA
  2. 2.Marine Science InstituteUniversity of CaliforniaSanta BarbaraUSA
  3. 3.Colorado Department of AgriculturePalisade InsectaryPalisadeUSA
  4. 4.Environmental Research Laboratory, Department of Soil, Water and Environmental ScienceUniversity of ArizonaTucsonUSA

Personalised recommendations