Niche opportunities for invasive annual plants in dryland ecosystems are controlled by disturbance, trophic interactions, and rainfall

Abstract

Resource availability and biotic interactions control opportunities for the establishment and expansion of invasive species. Studies on biotic resistance to plant invasions have typically focused on competition and occasionally on herbivory, while resource-oriented studies have focused on water or nutrient pulses. Through synthesizing these approaches, we identify conditions that create invasion opportunities. In a nested fully factorial experiment, we examined how chronic alterations in water availability and rodent density influenced the density of invasive species in both the Mojave Desert and the Great Basin Desert after fire. We used structural equation modeling to examine the direct and mediated effects controlling the density of invasives in both deserts. In the first 2 years after our controlled burn in the Great Basin, we observed that fire had a direct effect on increasing the invasive forb Halogeton glomeratus as well as a mediated effect through reducing rodent densities and herbivory. 4 years after the burn, the invasive annual grass Bromus tectorum was suppressing Halogeton glomeratus in mammal exclusion plots. There was a clear transition from years where invasives were controlled by disturbance and trophic interactions to years were resource availability and competition controlled invasive density. Similarly, in the Mojave Desert we observed a strong early influence of trophic processes on invasives, with Schismus arabicus benefitted by rodents and Bromus rubens negatively influenced by rodents. In the Mojave Desert, post-fire conditions became less important in controlling the abundance of invasives over time, while Bromus rubens was consistently benefitted by increases in fall rainfall.

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References

  1. Abatzoglou JT, Kolden CA (2011) Climate Change in Western US Deserts: potential for Increased Wildfire and Invasive Annual Grasses. Rangeland Ecol Manag 64:471–478. https://doi.org/10.2111/rem-d-09-00151.1

    Article  Google Scholar 

  2. Abella SR, Embrey TM, Schmid SM, Prengaman KA (2012) Biophysical Correlates with the Distribution of the Invasive Annual Red Brome (Bromus rubens) on a Mojave Desert Landscape. Invasive Plant Science and Management 5:47–56. https://doi.org/10.1614/ipsm-d-11-00030.1

    Article  Google Scholar 

  3. Allington GRH, Koons DN, Ernest SKM, Schutzenhofer MR, Valone TJ (2013) Niche opportunities and invasion dynamics in a desert annual community. Ecol Lett 16:158–166. https://doi.org/10.1111/ele.12023

    Article  PubMed  Google Scholar 

  4. Balch JK, Bradley BA, D’Antonio CM, Gomez-Dans J (2013) Introduced annual grass increases regional fire activity across the arid western USA (1980-2009). Glob Change Biol 19:173–183. https://doi.org/10.1111/gcb.12046

    Article  Google Scholar 

  5. Beatley JC (1966) Ecological status of introduce brome grasses (Bromus spp) in desert vegetation of southern Nevada. Ecology 47:548. https://doi.org/10.2307/1933931

    Article  Google Scholar 

  6. Blumenthal D (2005) Ecology - Interrelated causes of plant invasion. Science 310:243–244. https://doi.org/10.1126/science.1114851

    Article  PubMed  CAS  Google Scholar 

  7. Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–895. https://doi.org/10.1111/j.1461-0248.2006.00934.x

    Article  PubMed  Google Scholar 

  8. Blumenthal D, Mitchell CE, Pysek P, Jarosik V (2009) Synergy between pathogen release and resource availability in plant invasion. Proc Natl Acad Sci USA 106:7899–7904. https://doi.org/10.1073/pnas.0812607106

    Article  PubMed  PubMed Central  Google Scholar 

  9. Bowman TR (2015) The Cascading Effects of Invasive Grasses in North American Deserts: The Interactions of Fire, Plants, and Small Mammals. Brigham Young University, Provoe, Utah, MS

    Google Scholar 

  10. Boyd CS, Davies KW (2012) Differential seedling performance and environmental correlates in shrub canopy vs. interspace microsites. J Arid Environ 87:50–57

    Article  Google Scholar 

  11. Bowman D et al (2011) The human dimension of fire regimes on Earth. J Biogeogr 38:2223–2236. https://doi.org/10.1111/j.1365-2699.2011.02595.x

    Article  PubMed  PubMed Central  Google Scholar 

  12. Brown JH, Heske EJ (1990) Control of a desert-grassland transition by a keystone rodent guild. Science 250(4988):1705–1707

    Article  PubMed  CAS  Google Scholar 

  13. Brooks ML, Berry KH (2006) Dominance and environmental correlates of alien annual plants in the Mojave Desert, USA. J Arid Environ 67:100–124. https://doi.org/10.1016/j.jaridenv.2006.09.021

    Article  Google Scholar 

  14. Brooks ML, Matchett JR (2006) Spatial and temporal patterns of wildfires in the Mojave Desert, 1980–2004. J Arid Environ 67:148–164. https://doi.org/10.1016/j.jaridenv.2006.09.027

    Article  Google Scholar 

  15. Bukowski BE, Baker WL (2013) Historical fire regimes, reconstructed from land-survey data, led to complexity and fluctuation in sagebrush landscapes. Ecol Appl 23:546–564

    Article  PubMed  Google Scholar 

  16. Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40. https://doi.org/10.1111/j.1472-4642.2008.00521.x

    Article  Google Scholar 

  17. Chambers JC et al (2014) Resilience and Resistance of Sagebrush Ecosystems: implications for State and Transition Models and Management Treatments. Rangeland Ecol Manag 67:440–454. https://doi.org/10.2111/rem-d-13-00074.1

    Article  Google Scholar 

  18. Condon L, Weisberg PJ, Chambers JC (2011) Abiotic and biotic influences on Bromus tectorum invasion and Artemisia tridentata recovery after fire. International Journal of Wildland Fire 20:597–604. https://doi.org/10.1071/wf09082

    Article  Google Scholar 

  19. Connolly BM, Pearson DE, Mack RN (2014) Granivory of invasive, naturalized, and native plants in communities differentially susceptible to invasion. Ecology 95:1759–1769

    Article  PubMed  CAS  Google Scholar 

  20. Curtis CA, Bradley BA (2015) Climate Change May Alter Both Establishment and High Abundance of Red Brome (Bromus rubens) and African Mustard (Brassica tournefortii) in the Semiarid Southwest United States. Invasive Plant Science and Management 8:341–352. https://doi.org/10.1614/ipsm-d-14-00040.1

    Article  Google Scholar 

  21. Dantonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass fire cycle, and global change. Annu Rev Ecol Syst 23:63–87. https://doi.org/10.1146/annurev.es.23.110192.000431

    Article  Google Scholar 

  22. D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23:63–87

    Article  Google Scholar 

  23. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534. https://doi.org/10.1046/j.1365-2745.2000.00473.x

    Article  Google Scholar 

  24. Dettweiler-Robinson E, Bakker JD, Grace JB (2013) Controls of biological soil crust cover and composition shift with succession in sagebrush shrub-steppe. J Arid Environ 94:96–104. https://doi.org/10.1016/j.jaridenv.2013.01.013

    Article  Google Scholar 

  25. Elton C (1958) The ecology of invasions by animals and plants. Methuen, London

    Google Scholar 

  26. Eskelinen A, Harrison S (2014) Exotic plant invasions under enhanced rainfall are constrained by soil nutrients and competition. Ecology 95:682–692. https://doi.org/10.1890/13-0288.1

    Article  PubMed  Google Scholar 

  27. Grace JB et al. (2012) Guidelines for a graph-theoretic implementation of structural equation modeling. Ecosphere 3. https://doi.org/10.1890/es12-00048.1

  28. Grace JB, Anderson TM, Olff H, Scheiner SM (2010) On the specification of structural equation models for ecological systems. Ecol Monogr 80:67–87. https://doi.org/10.1890/09-0464.1

    Article  Google Scholar 

  29. Horn KJ, St Clair SB (2017) Wildfire and exotic grass invasion alter plant productivity in response to climate variability in the Mojave Desert. Landscape Ecol 32(3):635–646

    Article  Google Scholar 

  30. Horn KJ, McMillan BR, St Clair SB (2012) Expansive fire in Mojave Desert shrubland reduces abundance and species diversity of small mammals. J Arid Environ 77:54–58. https://doi.org/10.1016/j.jaridenv.2011.10.003

    Article  Google Scholar 

  31. Horn KJ, Nettles R, St Clair SB (2015a) Germination response to temperature and moisture to predict distributions of the invasive grass red brome and wildfire. Biol Invasions 17:1849–1857. https://doi.org/10.1007/s10530-015-0841-3

    Article  Google Scholar 

  32. Horn KJ, Wilkinson J, White S, St Clair SB (2015b) Desert wildfire impacts on plant community function. Plant Ecol 216:1623–1634. https://doi.org/10.1007/s11258-015-0546-9

    Article  Google Scholar 

  33. IPCC (2014) Working group 1 Fifth assessment report. Cambridge University Press, Cambridge

    Google Scholar 

  34. Jensen JM, Six DL (2006) Myrmecochory of the exotic plant, Centaurea maculosa: a potential mechanism enhancing invasiveness. Environ Entomol 35:326–331

    Article  Google Scholar 

  35. Kalisz S, Spigler RB, Horvitz CC (2014) In a long-term experimental demography study, excluding ungulates reversed invader’s explosive population growth rate and restored natives. Proc Natl Acad Sci USA 111:4501–4506. https://doi.org/10.1073/pnas.1310121111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Kempel A, Chrobock T, Fischer M, Rohr RP, van Kleunen M (2013) Determinants of plant establishment success in a multispecies introduction experiment with native and alien species. Proc Natl Acad Sci USA 110:12727–12732. https://doi.org/10.1073/pnas.1300481110

    Article  PubMed  PubMed Central  Google Scholar 

  37. Lefcheck JS (2015) piecewiseSEM: piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods Ecol Evol. https://doi.org/10.1111/2041-210X.12512

    Article  Google Scholar 

  38. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989. https://doi.org/10.1111/j.1461-0248.2004.00657.x

    Article  Google Scholar 

  39. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. https://doi.org/10.2307/2641039

    Article  Google Scholar 

  40. Maron JL, Kauffman MJ (2006) Habitat-specific impacts of multiple consumers on plant population dynamics. Ecology 87:113–124. https://doi.org/10.1890/05-0434

    Article  PubMed  Google Scholar 

  41. Maron JL, Pearson DE, Potter T, Ortega YK (2012) Seed size and provenance mediate the joint effects of disturbance and seed predation on community assembly. J Ecol 100:1492–1500. https://doi.org/10.1111/j.1365-2745.2012.02027.x

    Article  Google Scholar 

  42. Montoya JM, Raffaelli D (2010) The effects of climate change on biotic interactions and ecosystem services. Philos Trans R Soc B Biol Sci 365:2011. https://doi.org/10.1098/rstb.2010.0113

    Article  Google Scholar 

  43. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  44. Orrock JL, Witter MS, Reichman OJ (2008) Apparent competition with an exotic plant reduces native plant establishment. Ecology 89:1168–1174. https://doi.org/10.1890/07-0223.1

    Article  PubMed  Google Scholar 

  45. Pearson DE, Callaway RM, Maron JL (2011) Biotic resistance via granivory: establishment by invasive, naturalized, and native asters reflects generalist preference. Ecology 92:1748–1757

    Article  PubMed  Google Scholar 

  46. Pearson DE, Potter T, Maron JL (2012) Biotic resistance: exclusion of native rodent consumers releases populations of a weak invader. J Ecol 100:1383–1390. https://doi.org/10.1111/j.1365-2745.2012.02025.x

    Article  Google Scholar 

  47. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species int he United States. Bioscience 50:53–65

    Article  Google Scholar 

  48. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2016) Linear and nonlinear mixed effects models. R Package Version 3.1-128

  49. Reader RJ (1993) Control of seedling emergence by ground cover and seed predation in relation to seed size for some old-field species. J Ecol 81:169–175. https://doi.org/10.2307/2261232

    Article  Google Scholar 

  50. Rowe RJ, Terry RC (2014) Small mammal responses to environmental change: integrating past and present dynamics. J Mammal 95:1157–1174. https://doi.org/10.1644/13-mamm-s-079

    Article  Google Scholar 

  51. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176. https://doi.org/10.1016/s0169-5347(02)02495-3

    Article  Google Scholar 

  52. Sol D et al (2012) Unraveling the life history of successful invaders. Science 337:580–583. https://doi.org/10.1126/science.1221523

    Article  PubMed  CAS  Google Scholar 

  53. St Clair SB, O’Connor R, Gill R, McMillan B (2016) Biotic resistance and disturbance: rodent consumers regulate post-fire plant invasions and increase plant community diversity. Ecology 97:1700–1711. https://doi.org/10.1002/ecy.1391

    Article  PubMed  Google Scholar 

  54. Soil Survey Staff NRCS, USDA (2014) Web Soil Survey. http://websoilsurvey.sc.egov.usda.gov/App/WebSoilSurvey.aspx

  55. Suazo AA, Spencer JE, Engel EC, Abella SR (2012) Responses of native and non-native Mojave Desert winter annuals to soil disturbance and water additions. Biol Invasions 14:215–227. https://doi.org/10.1007/s10530-011-9998-6

    Article  Google Scholar 

  56. Thomey ML et al (2011) Effect of precipitation variability on net primary production and soil respiration in a Chihuahuan Desert grassland. Glob Change Biol 17:1505–1515. https://doi.org/10.1111/j.1365-2486.2010.02363.x

    Article  Google Scholar 

  57. Tingley R, Vallinoto M, Sequeira F, Kearney M (2014) Realized niche shift during a global biological invasion. Proc Natl Acad Sci 111:10233–10238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Vargas R et al (2012) Precipitation variability and fire influence the temporal dynamics of soil CO2 efflux in an arid grassland. Glob Change Biol 18:1401–1411. https://doi.org/10.1111/j.1365-2486.2011.02628.x

    Article  Google Scholar 

  59. Vila M et al (2010) How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front Ecol Environ 8:135–144. https://doi.org/10.1890/080083

    Article  Google Scholar 

  60. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499. https://doi.org/10.1126/science.277.5325.494

    Article  CAS  Google Scholar 

  61. Wang S-Y, Gillies RR, Reichler T (2012) Multidecadal drought cycles in the Great Basin Recorded by the Great Salt Lake: modulation from a transition-phase teleconnection. J Clim 25:1711–1721. https://doi.org/10.1175/2011JCLI4225.1

    Article  Google Scholar 

  62. WFLC (2009) The true cost of wildfire in the western US. Western Forestry Leadership Coalition, pp 1–15

  63. Williamson MH, Fitter A (1996) The characters of successful invaders. Biol Cons 78:163–170. https://doi.org/10.1016/0006-3207(96)00025-0

    Article  Google Scholar 

  64. Yahdjian L, Sala OE (2002) A rainout shelter design for intercepting different amounts of rainfall. Oecologia 133:95–101. https://doi.org/10.1007/s00442-002-1024-3

    Article  PubMed  Google Scholar 

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Acknowledgements

We appreciate the assistance of the Bureau of Land Management Salt Lake City Field office for providing National Environmental Policy Act clearance and conducting the experimental burn treatments in the Great Basin. We also acknowledge the Washington and Iron County Fire Marshals who conducted the experimental burns in the Mojave Desert. We acknowledge Tiffany Sharp and Brock McMillan for conducting the rodent surveys and Amy Clark and Justin Taylor for assistance with the vegetation surveys. This project was funded by United States Department of Agriculture National Institute of Food and Agriculture Grant: 2010-38415-21908 and by Brigham Young University’s Office of Research and Creative Activities.

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RAG and SBS conceived and designed the experiments. RAG, RCO, TBB, and SBS performed the experiments, RAG, AR, and DCL analyzed the data. RAG and RCO wrote the manuscript; other authors provided editorial advice.

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Correspondence to Richard A. Gill.

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The authors declare that they have no conflict of interest.

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Communicated by Kendi Davies.

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Gill, R.A., O’Connor, R.C., Rhodes, A. et al. Niche opportunities for invasive annual plants in dryland ecosystems are controlled by disturbance, trophic interactions, and rainfall. Oecologia 187, 755–765 (2018). https://doi.org/10.1007/s00442-018-4137-z

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Keywords

  • Niche opportunity
  • Invasive species
  • Precipitation manipulation
  • Fire
  • Rodents