Skip to main content
Log in

Post-fire management targeting invasive annual grasses may have inadvertently released the exotic perennial forb Chondrilla juncea and suppressed its biocontrol agent

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Top-down and bottom-up factors affecting invasive populations are rarely considered simultaneously, yet their interactive responses to disturbances and management interventions can be essential to understanding invasion patterns. We evaluated post-fire responses of the exotic perennial forb Chondrilla juncea (rush skeletonweed) and its biocontrol agents to landscape factors and a post-fire combined herbicide (imazapic) and bacteria (Pseudomonas fluorescens strain MB906) treatment that targeted invasive annual grasses in a sagebrush steppe ecosystem. Biocontrol agents released against C. juncea in previous decades included Cystiphora schmidti (gall midge), Aceria chondrillae (gall mite), and Puccinia chondrillina (rust fungus). C. juncea abundance was greater in sprayed than unsprayed plots, and where soils were coarser, slopes faced southwest, solar heat loads and topographic water accumulation were greater, and cover of deep-rooted native perennials was lower. Mite infestation was greater in unsprayed plots, midge infestation was greater at higher elevations on steeper slopes, and midges were more abundant while rust was less abundant on gravelly soils. Biocontrol infestation levels varied considerably between years and could not be predicted in 2019 from 2018 infestation levels. Multiple biocontrol species were often present at the same plots but were rarely present on the same C. juncea individuals. These results suggest that spatial patterns of invasion by C. juncea are related to deep-soil water availability, warmer conditions, and alleviation of competition. Treatments designed to reduce invasive annual grasses may inadvertently release C. juncea by both reducing plant competition for soil resources and affecting biocontrol agent (mite) abundance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available in the ScienceBase repository: Lazarus BE, Germino MJ (2021) Post-fire Chondrilla juncea and biocontrol at Boise River Wildlife Management Area 2018–2019: U.S. Geological Survey data release. https://doi.org/10.5066/P9QFBHZ3.

References

  • Abella SR (2014) Effectiveness of exotic plant treatments on National Park Service lands in the United States. Invasive Plant Sci Manag 7:147–163

    Google Scholar 

  • Aksoy HM, Ozman-Sullivan SK, Ocal H, Celik N, Sullivan GT (2008) The effects of Pseudomonas putida biotype B on Tetranychus urticae (Acari: Tetranychidae). In: Diseases of Mites and Ticks. Springer, Dordrecht, pp 223–230

  • Al-Sohim AS, Fouly AF (2015) Biological effects of two bacterial isolates and mutants of Pseudomonas fluorescens on date palm red spider mite, Oligonychus afrasiaticus (Acari: Tertanychidae). Egypt J Biol Pest Control 25:513–518

    Google Scholar 

  • Applestein C, Germino MJ, Fisk MR (2018) Vegetative community response to landscape-scale post-fire herbicide (imazapic) application. Invasive Plant Sci Manag 11:127–135

    Google Scholar 

  • 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). Global Change Biol 19:173–183. https://doi.org/10.1111/gcb.12046

    Article  Google Scholar 

  • Blanchette BL, Lee GA (1981) The influence of environmental factors on infection of rush skeletonweed (Chondrilla juncea) by Puccinia chondrillina. Weed Sci 29:364–367

    Google Scholar 

  • Bouyoucos GJ (1962) Hydrometer method improved for making particle size analyses of soils 1. Agron J 54:464–465

    Google Scholar 

  • Burdon JJ, Groves RH, Cullen JM (1981) The impact of biological control on the distribution and abundance of Chondrilla juncea in south-eastern Australia. J Appl Ecol 18:957–966

    Google Scholar 

  • Burdon JJ, Groves RH, Kaye PE, Speer SS (1984) Competition in mixtures of susceptible and resistant genotypes of Chondrilla juncea differentially infected with rust. Oecologia 64:199–203

    CAS  PubMed  Google Scholar 

  • Campanella DM, McEvoy PB, Mundt CC (2009) Interaction effects of two biological control organisms on resistant and susceptible weed biotypes of Chondrilla juncea in western North America. Biol Control 50:50–59. https://doi.org/10.1016/j.biocontrol.2009.01.005

    Article  Google Scholar 

  • Caresche LA, Wapshere AJ (1974) Biology and host specificity of the Chondrilla gall mite Aceria chondrillae (G. Can.)(Acarina, Eriophyidae). Bull Entomol Res 64:183–192

    Google Scholar 

  • Caresche LA, Wapshere AJ (1975) Biology and host specificity of the Chondrilla root moth Bradyrrhoa gilveolella (Treitschke)(Lepidoptera, Phycitidae). Bull Entomol Res 65:171–185

    Google Scholar 

  • Caresche LA, Wapshere AJ (1975) The Chondrillagall midge, Cystiphora schmidti (Rübsaamen)(Diptera, Cecidomyiidae). II. biology and host specificity. Bull Entomol Res 65:55–64

    Google Scholar 

  • Chambers JC, Germino MJ, Belnap J, Brown CS, Schupp EW, St. Clair SB, (2016) Plant community resistance to invasion by Bromus species: the roles of community attributes, Bromus interactions with plant communities, and Bromus traits. In: Germino MJ, Chambers JC, Brown CS (eds) Exotic brome-grasses in arid and semiarid ecosystems of the Western US: causes, consequences, and management implications. Springer International, Switzerland, pp 275–304

    Google Scholar 

  • Cohen-Kupiec R, Chet I (1998) The molecular biology of chitin digestion. Curr Opin Biotechnol 9:270–277

    CAS  PubMed  Google Scholar 

  • Crowe M, Bourchier R (2006) Interspecific interactions between the gall-fly Urophora affinis Frfld. (Diptera: Tephritidae) and the weevil Larinus minutus Gyll. (Coleoptera: Curculionidae), two biological control agents released against spotted knapweed, Centaurea stobe L. ssp micranthos. Biocontrol Sci Technol 16:417–430. https://doi.org/10.1080/09583150500532238

    Article  Google Scholar 

  • Cullen JM, Groves RH, Alex JF (1982) The influence of Aceria chondrillae on the growth and reproductive capacity of Chondrilla juncea. J Appl Ecol 19(2):529–537

    Google Scholar 

  • 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. https://doi.org/10.1146/annurev.es.23.110192.000431

    Article  Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534

    Google Scholar 

  • Denoth M, Frid L, Myers JH (2002) Multiple agents in biological control: improving the odds? Biol Control 24:20–30

    Google Scholar 

  • Emge RG, Melching JS, Kingsolver CH (1981) Epidemiology of Puccinia chondrillina, a rust pathogen for the biological control of rush skeleton weed in the United States. Phytopathology 71:839–843

    Google Scholar 

  • Gaskin JF, Schwarzländer M, Kinter CL, Smith JF, Novak SJ (2013) Propagule pressure, genetic structure, and geographic origins of Chondrilla juncea (Asteraceae): an apomictic invader on three continents. Am J Bot 100:1871–1882

    PubMed  Google Scholar 

  • Germino MJ, Lazarus BE (2020) Synthesis of weed-suppressive bacteria studies in rangelands of the western United States: special section of articles in Rangeland ecology and management provides little evidence of effectiveness. Range Ecol Manag 73(6):737–740

    Google Scholar 

  • Germino MJ, Belnap J, Stark JM, Allen EB, Rau BM (2016) Ecosystem impacts of exotic annual invaders in the genus Bromus. In: Germino MJ, Chambers JC, Brown CS (eds) Exotic brome-grasses in arid and semiarid ecosystems of the Western US: causes, consequences and management implications. Springer International, Switzerland, pp 61–95

    Google Scholar 

  • Groves RH, Williams JD (1975) Growth of skeleton weed (Chondrilla juncea L.) as affected by growth of subterranean clover (Trifolium subterraneum L.) and infection by Puccinea chondrillina Bubak and Syd. Aust J Agric Res 26:975–983

    Google Scholar 

  • Hasan S, Wapshere AJ (1973) The biology of Puccinia chondrillina a potential biological control agent of skeleton weed. Ann Appl Biol 74:325–332

    Google Scholar 

  • Herrick JE, Van Zee JW, Havstad KM, Burkett LM, Whitford WG (2005) Monitoring Manual For Grassland, Shrubland and Savanna Ecosystems. Volume I: Quick Start. Department of Agriculture, Agricultural Research Service, Jornada Experimental Range, Las Cruces, NM https://www.fs.usda.gov/Internet/FSE_DOCUMENTS/stelprdb5172119.pdf Accessed 4 June 2020

  • Hill JP, Germino MJ, Wraith JM, Olson BE, Swan MB (2006) Advantages in water relations contribute to greater photosynthesis in Centaurea maculosa compared with established grasses. Int J Plant Sci 167:269–277. https://doi.org/10.1086/499505

    Article  Google Scholar 

  • Humphrey LD (1984) Patterns and mechanisms of plant succession after fire on Artemisia-grass sites in southeastern Idaho. Vegetatio 57:91–101

    Google Scholar 

  • Jacobs J, Goodwin K, Ogle D (2009) Plant Guide for rush skeletonweed (Chondrilla juncea L.) USDA-Natural Resources Conservation Service, Montana State Office, Bozeman, MT https://plants.usda.gov/plantguide/pdf/pg_chju.pdf Accessed 4 June 2020

  • Kashefi J, Markin GP, Littlefield JL (2007) Field studies of the biology of the moth Bradyrrhoa gilveolella (Treitschke)(Lepidoptera: Pyralidae) as potential biocontrol agent for Chondrilla juncea. CAB International. In: Proceedings of the XII International Symposium on Biological Control of Weeds, 2007 pp 22-27

  • Kettenring KM, Adams CR (2011) Lessons learned from invasive plant control experiments: a systematic review and meta-analysis. J Appl Ecol 48:970–979. https://doi.org/10.1111/j.1365-2664.2011.01979.x

    Article  Google Scholar 

  • Kinter CL, Mealor BA, Shaw NL, Hild AL (2007) Postfire invasion potential of rush skeletonweed (Chondrilla juncea). Rangeland Ecol Manage 60:386–394

    Google Scholar 

  • Konigsberg ER (2014) Factors involved in the success and establishment of the field bindweed gall mite Aceria malherbae Nuzzaci (Acari: eriophyidae), MS Thesis, Montana State University

  • Kuebbing SE, Nuñez MA, Simberloff D (2013) Current mismatch between research and conservation efforts: the need to study co-occurring invasive plant species. Biol Conserv 160:121–129

    Google Scholar 

  • Kulmatiski A, Beard KH, Stark JM (2006) Exotic plant communities shift water-use timing in a shrub-steppe ecosystem. Plant Soil 288:271–284

    CAS  Google Scholar 

  • Kyser GB, Wilson RG, Zhang JM, DiTomaso JM (2013) Herbicide-assisted restoration of Great Basin sagebrush steppe infested with medusahead and downy brome Rangeland Ecol. Manage 66:588–596. https://doi.org/10.2111/Rem-D-12-00184.1

    Article  Google Scholar 

  • Lajeuness S, Sheley R, Duncan C, Lym R (1999) Leafy spurge. In: Sheley RL, Petroff JK (eds) Biology and management of noxious rangeland weeds. Oregon State University Press, Corvallis, OR, pp 249–260

    Google Scholar 

  • Lazarus BE, Germino MJ (accepted) A chemical and bio-herbicide mixture increased exotic invaders, both targeted and non-targeted, across a diversely invaded landscape after fire. Applied Vegetation Science

  • Lazarus BE, Germino MJ, Brabec M, Peterson L, Walker RN, Moser A (2020) Post-fire management-scale trials of bacterial soil amendment MB906 show inconsistent control of invasive annual grasses. Rangeland Ecol Manage 73(6):741–748

    Google Scholar 

  • Liao JD, Monsen SB, Anderson VJ, Shaw NL (2000) Seed biology of rush skeletonweed in sagebrush steppe. J Range Manag 53(5):544–549

    Google Scholar 

  • Maddox DM, Mayfield A, Poritz NH (1985) Distribution of yellow starthistle (Centaurea solstitialis) and Russian knapweed (Centaurea repens). Weed Sci 33:315–327. https://doi.org/10.1017/S0043174500082357

    Article  Google Scholar 

  • Mangold J, Parkinson H, Duncan C, Rice P, Davis E, Menalled F (2013) Downy brome (Bromus tectorum) control with imazapic on Montana grasslands. Invasive Plant Sci Manag 6:554–558. https://doi.org/10.1614/Ipsm-D-13-00016.1

    Article  Google Scholar 

  • McCune B (2007) Improved estimates of incident radiation and heat load using non-parametric regression against topographic variables. J Veg Sci 18:751–754

    Google Scholar 

  • McEvoy P, Coombs E (1999) Biological control of plant invaders: Regional patterns, field experiments, and structured population models. Ecol Appl 9:387–401

    Google Scholar 

  • McFadyen REC (1998) Biological control of weeds. Annu Rev Entomol 43:369–393

    CAS  PubMed  Google Scholar 

  • McVean DN (1966) Ecology of Chondrilla juncea L. in south-eastern Australia. J Ecol 54:345–365

    Google Scholar 

  • Milan, J (2005) Control efficacy of the biological control agents Eriophyes chondrillae and Puccinia chondrillina on rush skeletonweed, Chondrilla juncea L. MS Thesis, University of Idaho

  • Milan JD, Harmon BL, Prather TS, Schwarzländer M (2006) Winter mortality of Aceria chondrillae, a biological control agent released to control rush skeletonweed (Chondrilla juncea) in the western United States. J Appl Entomol 130:473–479

    Google Scholar 

  • Milan J, Randall CB, Andreas JE, Winston RL (2016) Biology and Biological Control of Rush Skeletonweed. U.S. Forest Service, Forest Health Technology Enterprise Team, Morgantown, West Virginia. FHTET-2016–06 https://bugwoodcloud.org/resource/pdf/Rush_skeletonweed.pdf Accessed 8 June 2020

  • Moore ID, Grayson RB, Ladson AR (1991) Digital terrain modelling: a review of hydrological, geomorphological, and biological applications. Hydrol Process 5:3–30

    Google Scholar 

  • Morishita DW (1999) Canada thistle. In: Sheley RL, Petroff JK (eds) Biology and management of noxious rangeland weeds. Oregon State University Press, Corvallis, pp 162–174

    Google Scholar 

  • Morris C, Monaco TA, Rigby CW (2009) Variable impacts of imazapic rate on downy brome (Bromus tectorum) and seeded species in two rangeland communities. Invasive Plant Sci Manag 2:110–119. https://doi.org/10.1614/Ipsm-08-104.1

    Article  Google Scholar 

  • Muller, K (2014) Boise River Wildlife Management Area 2014 – 2023 management plan, Idaho Department of Fish and Game, Nampa, ID https://idfg.idaho.gov/sites/default/files/2014-2023-BoiseRiverWMA-Plan-Final.pdf Accessed 25 June 2020

  • Mulligan GA, Findlay JN (1974) The biology of Canadian weeds. 3. Cardaria draba, C. chalepensis, and C. pubescens. Can J Plant Sci 54:149–160

    Google Scholar 

  • Neiendam Nielsen M, Sørensen J (1999) Chitinolytic activity of Pseudomonas fluorescens isolates from barley and sugar beet rhizosphere. FEMS Microbiol Ecol 30:217–227. https://doi.org/10.1111/j.1574-6941.1999.tb00650.x

    Article  CAS  PubMed  Google Scholar 

  • Noy-Meir I (1973) Desert ecosystems: environment and producers. Annu Rev Ecol Syst 4:25–51

    Google Scholar 

  • Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190

    CAS  Google Scholar 

  • Panetta FD (1989) Emergence and early establishment of Chondrilla juncea L.(skeleton weed) in the Western Australian wheatbelt Aust. J Ecol 14:115–122

    Google Scholar 

  • Pearson DE, Ortega YK, Runyon JB, Butler JL (2016) Secondary invasion: the bane of weed management. Biol Conserv 197:8–17

    Google Scholar 

  • Pearson DE, Ortega YK, Eren Ö, Hierro JL (2016) Quantifying “apparent” impact and distinguishing impact from invasiveness in multispecies plant invasions. Ecol Appl 26:162–173

    PubMed  Google Scholar 

  • Prevéy J, Germino M, Huntly N (2010) Loss of foundation species increases population growth of exotic forbs in sagebrush steppe. Ecol Appl 20:1890–1902. https://doi.org/10.1890/09-0750.1

    Article  PubMed  Google Scholar 

  • Prevéy J, Germino M, Huntly N, Inouye R (2010) Exotic plants increase and native plants decrease with loss of foundation species in sagebrush steppe. Plant Ecol 207:39–51. https://doi.org/10.1007/s11258-009-9652-x

    Article  Google Scholar 

  • Qessaoui R et al (2017) Ecological applications of Pseudomonas as a biopesticide to control two-spotted mite Tetranychusurticae: chitinase and HCN production. J Plant Prot Res 57:409–416

    CAS  Google Scholar 

  • Reid AM, Morin L, Downey PO, French K, Virtue JG (2009) Does invasive plant management aid the restoration of natural ecosystems? Biol Conserv 142:2342–2349. https://doi.org/10.1016/j.biocon.2009.05.011

    Article  Google Scholar 

  • Roobakkumar A, Babu A, Vasantha Kumar D, Jasin Rahman V, Sarkar S (2011) Pseudomonas fluorescens as an efficient entomopathogen against Oligonychus coffeae Nietner (Acari: Tetranychidae) infesting tea. J Entomol Nematol 3:73–77

    Google Scholar 

  • Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends in Ecology & Evolution 17:170–176. https://doi.org/10.1016/S0169-5347(02)02495-3

    Article  Google Scholar 

  • Sheley RL (1994) The Identification, Distribution, Impacts, Biology and Management of Noxious Rangeland Weeds. All U.S. Government Documents (Utah Regional Depository). Paper 446. https://digitalcommons.usu.edu/govdocs/446

  • Sheley RL, Jacobs JS, Carpinelli MF (1998) Distribution, biology, and management of diffuse knapweed (Centaurea diffusa) and spotted knapweed (Centaurea maculosa). Weed Technol 12:353–362

    Google Scholar 

  • Sheppard AW (1996) The interaction between natural enemies and interspecific plant competition in the control of invasive pasture weeds. In, Proceedings of the IX International Symposium on Biological Control of Weeds, 1996. University of Cape Town Stellenbosch,, South Africa, pp l-26

  • Supkoff DM, Joley DB, Marois JJ (1988) Effect of introduced biological control organisms on the density of Chondrilla juncea in California. J Appl Ecol 25(3):1089–1095

    Google Scholar 

  • Tu, M, Hurd, C, Randall, JM (2001) Weed Control Methods Handbook Chp. 16 Imazapic. The Nature Conservancy. Available online at https://www.invasive.org/gist/products/handbook/16.imazapic.pdf Accessed 5 November, 2020

  • USDA (2016) Weed risk assessment for Chondrilla juncea L. (Aseteraceae)—rush skeletonweed. Available online at https://www.aphis.usda.gov/plant_health/plant_pest_info/weeds/downloads/wra/Chondrilla-juncea.pdf Accessed 5 October, 2020

  • Wehling WF, Piper GL (1988) Efficacy diminution of the rush skeletonweed gall midge, Cystiphora schmidti (Diptera: Cecidomyiidae), by an indigenous parasitoid. Pan-Pacific Entomol 64:83–85

    Google Scholar 

Download references

Acknowledgements

We are grateful to Merry Davidson, Molly Felix, and Jennifer Butt for assistance with fieldwork, to Krista Biorn and Peter Ott (Idaho Department of Fish and Game) for help with logistics, to Cara Applestein for GIS assistance, and to Allison Simler-Williamson for statistical advice. We also thank Joey Milan and two anonymous reviewers for helpful comments on an earlier draft of the manuscript. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Funding

Funding was provided by a grant from the USDA National Institute of Food and Agriculture Exploratory Research Program, award no. 2018–67030-27353.

Author information

Authors and Affiliations

Authors

Contributions

MJG designed the study with input from BEL. BEL oversaw data collection, analyzed the data, and wrote the first draft of the manuscript. Both authors edited the manuscript.

Corresponding author

Correspondence to Brynne E. Lazarus.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lazarus, B.E., Germino, M.J. Post-fire management targeting invasive annual grasses may have inadvertently released the exotic perennial forb Chondrilla juncea and suppressed its biocontrol agent. Biol Invasions 23, 1915–1932 (2021). https://doi.org/10.1007/s10530-021-02481-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-021-02481-z

Keywords

Navigation