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Limits to biocontrol: the effects of urbanization and elevation on Bruchidius villosus and Exapion fuscirostre—two biological control agents of Cytisus scoparius

Abstract

Both invasive species and their biological control agents face barriers to expansion, which provide opportunities to limit invasions or may enable target invasive species to exist in enemy-free space. A better understanding of the various barriers to the spread of insects introduced to control invasive plants will allow for more targeted release programs and potentially shorter lag times from introduction to management. In the Pacific Northwest of the United States, two seed eating beetles (Exapion fuscirostre and Bruchidius villosus) have been introduced to control the invasive plant Cytisus scoparius. These biological controls are predicted to be effective only at high rates of seed destruction, so any factors that limit their colonization or population sizes may allow C. scoparius populations to grow, leading to ecological and economic harm. In this study, we investigate relative impacts of biological control agents in relation to two barriers to insect movement: urbanization and elevation. We find that the impacts of B. villosus are not different between urban and rural sites, but that relative impacts of both biological control agents decrease with increasing elevation, a pattern consistent across 2 years of measurements. Cytisus scoparius populations experience substantial seed destruction in urban settings, strongly suggesting successful population control. The low seed destruction at high elevation sites could indicate that biological control agents are ineffective there, and that C. scoparius may exist in enemy-reduced space.

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References

  1. Abatzoglou JT, Rupp DE, Mote PW (2013) Seasonal climate variability and change in the pacific northwest of the United States. J Clim 27:2125–2142

    Article  Google Scholar 

  2. Andreas JE (2016) Pest watch: biological control of Scotch broom, FS203E. Washington State University Extension, p 6

  3. Andreas JE, Wax T, Coombs EM, Gaskin J, Markin G, Sing S (2013) The scotch broom gall mite: accidental introduction to classic biological control agent? In: XIII International symposium on the biological control of weeds

  4. Andreas JE, Winston RL, Coombs EM, Miller TW, Pitcairn MJ, Randall CB, Turner S, Williams W (2017) Biology and biological control of Scotch broom and gorse. USDA Forest Service, Forest Health Technology Enterprise Team, Morgantown, West Virginia. FHTET-2017-01

  5. Andres LA, Hawkes RB, Rizza A (1967) Apion seed weevil introduced for biological control of Scotch broom. Calif Agric 21:13

    Google Scholar 

  6. Bang C, Faeth SH (2011) Variation in arthropod communities in response to urbanization: seven years of arthropod monitoring in a desert city. Landsc Urban Plan 103:383–399

    Article  Google Scholar 

  7. Bode RF, Gilbert A (2016) Seed predators, not herbivores, exert natural selection on Solidago spp. in an urban archipelago. Environ Entomol 45(1):150–154

    PubMed  CAS  Article  Google Scholar 

  8. Bode RF, Maciejewski A (2014) Herbivore biodiversity varies with patch size in an urban archipelago. Int J Insect Sci 6:49–55

    Article  Google Scholar 

  9. Bode RF, Tong R (2017) Pollinators exert positive selection on flower size on urban, but not rural Scotch broom (Cytisus scoparius L. Link). J Plant Ecol 11:493–501

    Article  Google Scholar 

  10. Bossard CC (1991) The role of habitat disturbance, seed predation and ant dispersal on establishment of the exotic shrub Cytisus scoparius in California. Am Midl Natl 126(1):1–13

    Article  Google Scholar 

  11. Bossard CC, Rejmanek M (1994) Herbivory, growth, seed production, and resprouting of an exotic invasive shrub Cytisus scoparius. Biol Conserv 67(3):193–200

    Article  Google Scholar 

  12. Carson BD, Landis DA (2014) Phenology and dispersal of Larinus minutus Gyllenhal and Larinus obtusus Gyllenhal (Coleoptera: Curculionidae), two biological control agents of Centaurea stoebe ssp. Micranthos (spotted knapweed) in Michigan. Biol Control 79:84–91

    Article  Google Scholar 

  13. Cavallero L, Morales CL, Montero-Castano A, Gowda JH, Aizen MA (2018) Scale-dependent effects of conspecific flower availability on pollination quantity and quality in an invasive shrub. Oecologia 188:501–513

    PubMed  CAS  Article  Google Scholar 

  14. Community Attributes Inc (2017) Economic impact of invasive species: Direct costs estimates and economic impacts for Washington State, pp 23-24

  15. Coombs EM, Isaacson DL, Hawkes RB (1995) The status of biological control of weeds in Oregon. Oregon Department of Agriculture, Salem

  16. Coombs EM, Clarke JK, Piper GL, Cofrancesco AF (2004) Biological Control of Invasive Plants in the United States. Oregon State University Press, Corvallis

    Google Scholar 

  17. Coombs EM, Markin GP, and Andreas J (2008) Release and Establishment of the Scotch broom seed beetle, Bruchidius villosus, in Oregon and Washington, USA. XII International Symposium on Biological Control of Weeds. 526-520

  18. Cordero RL, Torchelsen FP, Overbeck GE, Anand M (2016) Cytisus scoparius (Fabaceae) in southern Brazil—First step of an invasion process? Ann Braz Acad Sci 88(1):149–154

    Article  Google Scholar 

  19. DeWalt SJ (2006) Population dynamics and potential for biological control of an exotic invasive shrub in Hawaiian rainforests. Biol Invasions 8:1145–1158

    Article  Google Scholar 

  20. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    PubMed  CAS  Article  Google Scholar 

  21. Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142

    PubMed  Article  Google Scholar 

  22. Faeth SH, Kane TC (1978) Urban biogeography. City Parks as Islands for Diptera and Coleoptera. Oecologia 32(1):127–133

    PubMed  Article  Google Scholar 

  23. Fowler SV, Paynter Q, Hayes L, Dodd S, Groenteman R (2010) Biocontrol of weeds in New Zealand: an overview of nearly 85 years. In: Seventeenth Australasian weeds conference, pp 211–214

  24. Frick KE (1964) Leucoptera spartifoliella an introduced enemy of Scotch broom (Cytisus scoparius) in the western United States. J Econ Entomol 57(4):589–591

    Article  Google Scholar 

  25. Gavini SS, Farji-Brener AG (2015) La Importancia del Color: morfos florales, tasas de visita y éxito reproductivo en el arbusto Sarothamnus scoparius. Ecol Austral 25:204–211

    Google Scholar 

  26. Gillespie SD, Bayley J, Elle E (2017) Native bumble bee (Hymenoptera: Apidae) pollinators vary in floral resource use across an invasion gradient. Can J Entomol 149:204–213

    Article  Google Scholar 

  27. Grevstad FS (2006) Ten-year impacts of the biological control agents Galerucella pusilla and G. calmariensis (Coleoptera:Chrysomelidae) on Purple Loosestrife (Lythrum salicaria) in Central New York State. Biol Control 39:1–8

    Article  Google Scholar 

  28. Grove S, Haubensak KA, Parker I (2012) Direct and indirect effects of allelopathy in the soil legacy of an exotic plant invasion. Plant Ecol 213:1869–1882

    Article  Google Scholar 

  29. Harman HM (1999) The effect of variability in the phenology of the reproductive stages of Scotch broom (Cytisus scoparius) on the synchronization of the life stages of broom seed beetle (Bruchidius villosus) in New Zealand. Biol Control 15:228–234

    Article  Google Scholar 

  30. Harris P, Peschken D, Milroy J (1969) The status of biological control of the weed Hypericum perforatum in British Columbia. Can Entomol 101(1):1–15

    Article  Google Scholar 

  31. Herrera-Reddy AM, Carruthers RI, Mills NJ (2012) Integrated management of Scotch broom (Cytisus scoparius) using biological control. Invasive Plant Sci Manag 5(1):69–82

    Article  Google Scholar 

  32. Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513

    PubMed  Article  Google Scholar 

  33. Hogg BN, Smith L, Daane KM (2016) Impacts of the adventive Psyllid Arytainilla spartiophila (Hemiptera: Psyllidae) on growth of the invasive weed cytisus scoparius under controlled and field conditions in California. Environ Entomol 45(1):109–116

    PubMed  Article  Google Scholar 

  34. Huffaker CB, Kennett CE (1959) A ten-year study of vegetational changes associated with biological control of Klamath weed. J Range Manag 12:69–82

    Article  Google Scholar 

  35. Johnson K, Scriber JM (1994) Geographic variation in plant allelochemicals of significance to insect herbivores. In: Ananthakrishnan TN (ed) Functional dynamics of phytophagous insects. Science Publishers, Lebanon, pp 7–31

    Google Scholar 

  36. Julien MH (1989) Biological control of weeds worldwide: trends, rates of success and the future. Biocontrol News Inf 10:299–306

    Google Scholar 

  37. Kang M, Buckley YM, Lowe AJ (2007) Testing the role of genetic factors across multiple independent invasions of the shrub Scotch broom (Cytisus scoparius). Mol Ecol 16:4662–4673

    PubMed  CAS  Article  Google Scholar 

  38. Magda D, Gleizes B, Jarry M (2013) Maternal effect on seed survival and emergence in Cytisus scoparius: an experimental approach. Ecol Res 28:927–934

    Article  Google Scholar 

  39. Malo JE, Baonza J (2002) Are there predictable clines in plant-pollinator interactions along altitudinal gradients? The example of Cytisus scoparius (L.) Link in the Sierra de Guadarrama (Central Spain). Divers Distrib 8:365–371

    Article  Google Scholar 

  40. McCoy ED (1990) The Distribution of insects along elevational gradients. Oikos 58(3):313–322

    Article  Google Scholar 

  41. McEvoy PB, Coombs EM (1999) Biological control of plant invaders: Regional patterns, field experiments, and structured population models. Ecol Appl 9(2):387–401

    Article  Google Scholar 

  42. McEvoy PB, Cox C, Coombs EM (1991) Successful biological control of ragwort, Senecio jacobaea, by introduced insects in Oregon. Ecol Appl 1(4):430–442

    PubMed  Article  Google Scholar 

  43. Mkhize VS, Mhlambi N, Nanni I (2013) Scotch broom (Cytisus scoparius), a horticultural escapee targeted for eradication in South Africa. S Afr J Bot 86:178

    Article  Google Scholar 

  44. Mote PW, Salathe EP (2010) Future climate in the Pacific Northwest. Clim Change 102:29–50

    Article  Google Scholar 

  45. Muller-Scharer H, Schroeder D (1993) The biological control of Centaurea spp. in North America: Do insects solve the problem? Pestic Sci 37:343–353

    Article  Google Scholar 

  46. Parker IM (1996) Ecological factors affecting rates of spread in Cytisus scoparius, an invasive exotic shrub. Dissertation. University of Washington, Seattle, Washington, USA

  47. Parker IM (1997) Pollinator limitation of Cytisus scoparius (Scotch broom), an invasive exotic shrub. Ecology 78(5):1457–1470

    Article  Google Scholar 

  48. Parker IM (2000) Invasion dynamics of Cytisus scoparius: a matrix model approach. Ecol Appl 10(3):726–743

    Article  Google Scholar 

  49. Parnell JR (1966) Observations on the population fluctuations and life histories of the we Bruchidius ater (Bruchidae) and Apion fuscirostre (Curculionidae) on broom (Sarothamnus scoparius). J Anim Ecol 35:157–188

    Article  Google Scholar 

  50. Paynter Q, Main A, Gourlay AH, Peterson PG, Fowler SV, Buckley YM (2010) Disruption of an exotic mutualism can improve management of an invasive plant: varroa mite, honeybees and biological control of Scotch broom Cytisus scoparius in New Zealand. J Appl Ecol 47:309–317

    Article  Google Scholar 

  51. Paynter Q, Buckley YM, Peterson PG, Gourlay AH, Fowler SV (2015) Breaking and remaking a seed and seed predator interaction in the introduced range of Scotch broom (Cytisus scoparius) in New Zealand. J Ecol 104(1):1–11

    Google Scholar 

  52. Pojar J, MacKinnon A (1994) Plants of the Pacific Northwest Coast. Lone Pine Publishing, Redmond

    Google Scholar 

  53. Poveda K, Martinez E, Kersch-Becker MF, Bonilla MA, Tscharntke T (2012) Landscape simplification and altitude affect biodiversity, herbivory and Andean potato yield. J Appl Ecol 49:513–522

    Article  Google Scholar 

  54. Rassmann S, Pellissier L, Defossez E, Jactel H, Kunstler G (2014) Climate-driven change in plant–insect interactions along elevation gradients. Funct Ecol 28:46–54

    Article  Google Scholar 

  55. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  56. Redmon SG, Forrest TG, Markin GP (2000) Biology of Bruchidius villosus (Coleoptera: Bruchidae) on Scotch broom in North Carolina. Fla Entomol 83(3):242–253

    Article  Google Scholar 

  57. Rees M, Paynter Q (1997) Biological control of Scotch broom: modelling the determinants of abundance and the potential impact of introduced insect herbivores. J Appl Ecol 34(5):1203–1221

    Article  Google Scholar 

  58. Rodriguez E, Peco B, Gurrea MP (2012) Effect of Scotch broom. Cytisus scoparius, pod size and patch density on Exapion fuscirostre (Coleoptera, Apionidae) seed weevil predation. Aust J Entomol 51:127–132

    Article  Google Scholar 

  59. Saari S, Richter S, Higgins M, Oberhofer M, Jennings A, Faeth SH (2016) Urbanization is not associated with increased abundance or decreased richness of terrestrial animals—dissecting the literature through meta-analysis. Urban Ecosyst 19(3):1251–1264

    Article  Google Scholar 

  60. Srinivasan MP, Shenoy K, Gleeson SK (2007) Population structure of Scotch broom (Cytisus scoparius) and its invasion impacts on the resident plant community in the grasslands of Nilgiris, India. Curr Sci 93(8):1108–1113

    Google Scholar 

  61. Srinivasan MP, Kalita R, Gurung IK, Bhattacharjee SK, Antony PM, Krishnan S, Gleeson SK (2012) Seedling germination success and survival of the invasive shrub Scotch broom (Cytisus scoparius) in response to fire and experimental clipping in the montane grasslands of the Nilgiris, south India. Acta Oecol 38:41–48

    Article  Google Scholar 

  62. Stout J (2000) Does size matter? bumblebee behavior and the pollination of Cytisus scoparius L. (Fabaceae). Apidologie 31(1):129–139

    Article  Google Scholar 

  63. Suzuki N (2003) Significance of flower exploding pollination on the reproduction of the Scotch broom, Cytisus scoparius (Leguminosae). Ecol Res 18:523–532

    Article  Google Scholar 

  64. Swope SM, Satterthwaite WH, Parker IM (2017) Spatiotemporal variation in the strength of density dependence: implications for biocontrol of Centaurea solstitialis. Biol Invasions 19:2675–2691

    Article  Google Scholar 

  65. Syrett P (1996) Insects for biological control of broom (Cytisus scoparius) in New Zealand. In: Shepherd RCH (ed) Proceedings of the 11th Australian weeds conference, University of Melbourne, pp 525–528

  66. Syrett P, Fowler SV, Coombs EM, Hosking JR, Markin GP, Paynter QE, Sheppard AW (1999) The potential for biological control of Scotch broom (Cytisus scoparius) (Fabaceae) and related weedy species. Biocontrol News Inf 20(1):17–34

    Google Scholar 

  67. Tscharntke T, Steffan-Dewenter I, Kruess A, Theis C (2002) Characteristics of insect populations on habitat fragments: a mini-review. Ecol Res 17:229–239

    Article  Google Scholar 

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Acknowledgements

We would like to thank Rebecca Tong, Danner Linhart and Emily Prall for helping in seed collection. Jennifer Andreas provided us with an early release of her biological control identification book, which helped students learn the difference between a weevil and a beetle. She also looked over an early version and provided helpful feedback. We also thank Mikala Marbach, Leslie Maya, Sheridan Menard, Catherine and Emily Pham for counting seeds in 2016. Guilia Perini, Gia Sheppard, Karlee Kawasaki and Hasley Villadelgado helped count seeds in 2017. Saint Martin’s University provided laboratory space and equipment. A special thanks to the Murdock Charitable Trust (Grant Number 2015277) for funding the elevation portion of this research.

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Correspondence to Robert Frederick Bode.

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Bode, R.F., Grove, S. & Krueger, N. Limits to biocontrol: the effects of urbanization and elevation on Bruchidius villosus and Exapion fuscirostre—two biological control agents of Cytisus scoparius. Biol Invasions 21, 1021–1031 (2019). https://doi.org/10.1007/s10530-018-1882-1

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Keywords

  • Plant–insect interactions
  • Urban ecosystems
  • Elevation
  • Invasive species