Urban trees: bridge-heads for forest pest invasions and sentinels for early detection

Abstract

Urban trees have been increasingly appreciated for the many benefits they provide. As concentrated hubs of human-mediated movement, the urban landscape is, however, often the first point of contact for exotic pests including insects and plant pathogens. Consequently, urban trees can be important for accidentally introduced forest pests to become established and potentially invasive. Reductions in biodiversity and the potential for stressful conditions arising from anthropogenic disturbances can predispose these trees to pest attack, further increasing the likelihood of exotic forest pests becoming established and increasing in density. Once established in urban environments, dispersal of introduced pests can proceed to natural forest landscapes or planted forests. In addition to permanent long-term damage to natural ecosystems, the consequences of these invasions include costly attempts at eradication and post establishment management strategies. We discuss a range of ecological, economic and social impacts arising from these incursions and the importance of global biosecurity is highlighted as a crucially important barrier to pest invasions. Finally, we suggest that urban trees may be viewed as ‘sentinel plantings’. In particular, botanical gardens and arboreta frequently house large collections of exotic plantings, providing a unique opportunity to help predict and prevent the invasion of new pests, and where introduced pests with the capacity to cause serious impacts in forest environments could potentially be detected during the initial stages of establishment. Such early detection offers the only realistic prospect of eradication, thereby reducing damaging ecological impacts and long term management costs.

This is a preview of subscription content, access via your institution.

References

  1. Alvey AA (2006) Promoting and preserving biodiversity in the urban forest. Urban For Urban Green 5:195–201

    Article  Google Scholar 

  2. Armson D, Stringer P, Ennos AR (2012) The effect of tree shade and grass on surface and globe temperatures in an urban area. Urban For Urban Green 11:245–255

    Article  Google Scholar 

  3. Aukema JE, McCullough DG, Von Holle B et al (2010) Historical accumulation of nonindigenous forest pests in the continental United States. Bioscience 60:886–897

    Article  Google Scholar 

  4. Aukema JE, Leung B, Kovacs K et al (2011) Economic impacts of non-native forest insects in the continental United States. PLoS ONE 6:e24587

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Barham E (2016) The unique role of sentinel trees, botanic gardens and arboreta in safeguarding global plant health. Plant Biosyst 150:377–380

    Article  Google Scholar 

  6. Barham E, Sharrock S, Lane C et al (2016) The international plant sentinel network: a tool for regional and national plant protection organizations. EPPO Bull 46:156–162

    Article  Google Scholar 

  7. Barrett LG, Thrall PH, Burdon JJ et al (2008) Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol Evol 23:678–685

    Article  PubMed  PubMed Central  Google Scholar 

  8. Bradshaw CJA, Leroy B, Bellard C et al (2016) Massive yet grossly underestimated global costs of invasive insects. Nat Commun 7:12986

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Brasier CM (2008) The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol 57:792–808

    Article  Google Scholar 

  10. Brasier C, Denman S, Brown A et al (2004) Sudden oak death (Phytophthora ramorum) discovered on trees in Europe. Mycol Res 108:1108–1110

    Article  Google Scholar 

  11. Brasier CM, Beales PA, Kirk SA et al (2005) Phytophthora kernoviae sp. nov., an invasive pathogen causing bleeding stem lesions on forest trees and foliar necrosis of ornamentals in the UK. Mycol Res 109:853–859

    Article  PubMed  Google Scholar 

  12. Britton K, White P, Kramer A et al (2010) A new approach to stopping the spread of invasive insects and pathogens: early dection and rapid response via a global network of sentinel plantings. N Z J For Sci 40:109–114

    Google Scholar 

  13. Brockerhoff EG, Kimberley M, Liebhold AM et al (2014) Predicting how altering propagule pressure changes establishment rates of biological invaders across species pools. Ecology 95:594–601

    Article  PubMed  Google Scholar 

  14. Burgess TI, Wingfield MJ (2017) Pathogens on the move: a 100-year global experiment with planted eucalypts. Bioscience 67:14–25

    Article  Google Scholar 

  15. Chavez V, Parnell S, Bosch F (2015) Designing strategies for epidemic control in a tree nursery: the case of ash dieback in the UK. Forests 6:4135

    Article  Google Scholar 

  16. Christie FJ, Hochuli DF (2005) Elevated levels of herbivory in urban landscapes: are declines in tree health more than an edge effect? Ecol Soc 10:1–9

    Article  Google Scholar 

  17. Coetzee MPA, Wingfield BD, Harrington TC et al (2001) The root rot fungus Armillaria mellea introduced into South Africa by early Dutch settlers. Mol Ecol 10:387–396

    CAS  Article  PubMed  Google Scholar 

  18. Colunga-Garcia M, Magarey RA, Haack RA et al (2010) Enhancing early detection of exotic pests in agricultural and forest ecosystems using an urban-gradient framework. Ecol Appl 20:303–310

    Article  PubMed  Google Scholar 

  19. Crous PW, Groenewald JZ (2005) Hosts, species and genotypes: opinions versus data. Australas Plant Path 34:463–470

    Article  Google Scholar 

  20. Crous PW, Groenewald JZ, Slippers B et al (2016) Global food and fibre security threatened by current inefficiencies in fungal identification. Philos Trans R Soc B 371:20160024

    Article  Google Scholar 

  21. Davison EM, Drenth A, Kumar S et al (2006) Pathogens associated with nursery plants imported into Western Australia. Australas Plant Path 35:473–475

    Article  Google Scholar 

  22. Desprez-Loustau M-L, Robin C, Buée M et al (2007) The fungal dimension of biological invasions. Trends Ecol Evol 22:472–480

    Article  PubMed  Google Scholar 

  23. Desprez-Loustau M-L, Courtecuisse R, Robin C et al (2010) Species diversity and drivers of spread of alien fungi (sensu lato) in Europe with a particular focus on France. Biol Invasions 12:157–172

    Article  Google Scholar 

  24. Dobbs C, Escobedo FJ, Zipperer WC (2011) A framework for developing urban forest ecosystem services and goods indicators. Landsc Urban Plan 99:196–206

    Article  Google Scholar 

  25. Dobbs C, Kendal D, Nitschke CR (2014) Multiple ecosystem services and disservices of the urban forest establishing their connections with landscape structure and sociodemographics. Ecol Indic 43:44–55

    Article  Google Scholar 

  26. Dodds KJ, Orwig DA (2011) An invasive urban forest pest invades natural environments—Asian longhorned beetle in northeastern US hardwood forests. Can J For Res 41:1729–1742

    Article  Google Scholar 

  27. Donaldson JE, Hui C, Richardson DM et al (2014) Invasion trajectory of alien trees: the role of introduction pathway and planting history. Glob Chang Biol 20:1527–1537

    Article  PubMed  Google Scholar 

  28. Donovan GH, Butry DT, Michael YL et al (2013) The relationship between trees and human health. Am J Prev Med 44:139–145

    Article  PubMed  Google Scholar 

  29. Engelbrecht CJB, Harrington TC, Steimel J et al (2004) Genetic variation in eastern North American and putatively introduced populations of Ceratocystis fimbriata f. platani. Mol Ecol 13:2995–3005

    CAS  Article  PubMed  Google Scholar 

  30. Epanchin-Niell RS, Haight RG, Berec L et al (2012) Optimal surveillance and eradication of invasive species in heterogeneous landscapes. Ecol Lett 15:803–812

    Article  PubMed  Google Scholar 

  31. Eschen R, Britton K, Brockerhoff E et al (2015a) International variation in phytosanitary legislation and regulations governing importation of plants for planting. Environ Sci Policy 51:228–237

    Article  Google Scholar 

  32. Eschen R, Rigaux L, Sukovata L et al (2015b) Phytosanitary inspection of woody plants for planting at European Union entry points: a practical enquiry. Biol Invasions 17:2403–2413

    Article  Google Scholar 

  33. Faccoli M, Gatto P (2015) Analysis of costs and benefits of Asian longhorned beetle eradication in Italy. Forestry 89:301–309

    Article  Google Scholar 

  34. Fagan L, Bithell S, Dick M (2008) Systems for identifying invasive threats to New Zealand flora by using overseas plantings of New Zealand native plants. Surveillence for biosecurity: pre-border to pest management. New Zealand Plant Protection Society (Inc), Auckland

    Google Scholar 

  35. Gaertner M, Larson BMH, Irlich UM et al (2016) Managing invasive species in cities: a framework from Cape Town, South Africa. Landsc Urban Plan 151:1–9

    Article  Google Scholar 

  36. Ganley RJ, Bulman LS (2016) Dutch elm disease in New Zealand: impacts from eradication and management programmes. Plant Pathol 65:1047–1055

    Article  Google Scholar 

  37. Goss EM, Larsen M, Vercauteren A et al (2010) Phytophthora ramorum in Canada: evidence for migration within North America and from Europe. Phytopathology 101:166–171

    Article  Google Scholar 

  38. Groenteman R, Forgie SA, Hoddle MS et al (2015) Assessing invasion threats: novel insect-pathogen-natural enemy associations with native New Zealand plants in southern California. Biol Invasions 17:1299–1305

    Article  Google Scholar 

  39. Grote R, Samson R, Alonso R et al (2016) Functional traits of urban trees: air pollution mitigation potential. Front Ecol Environ 14:543–550

    Article  Google Scholar 

  40. Grünwald NJ, Garbelotto M, Goss EM et al (2012) Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends Microbiol 20:131–138

    Article  PubMed  Google Scholar 

  41. Haack RA, Hérard F, Sun J et al (2010) Managing invasive populations of Asian longhorned beetle and citrus longhorned beetle: a worldwide perspective. Annu Rev Entomol 55:521–546

    CAS  Article  PubMed  Google Scholar 

  42. Haack RA, Britton KO, Brockerhoff EG et al (2014) Effectiveness of the international phytosanitary standard ISPM No. 15 on reducing wood borer infestation rates in wood packaging material entering the United States. PLoS ONE 9:e96611

    Article  PubMed  PubMed Central  Google Scholar 

  43. Haight RG, Homans FR, Horie T et al (2011) Assessing the cost of an invasive forest pathogen: a case study with oak wilt. Environ Manag 47:506–517

    Article  Google Scholar 

  44. Herms DA, McCullough DG (2014) Emerald ash borer invasion of North America: history, biology, ecology, impacts, and management. Annu Rev Entomol 59:13–30

    CAS  Article  PubMed  Google Scholar 

  45. Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  46. Jung T, Orlikowski L, Henricot B et al (2016) Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. For Pathol 46:134–163

    Article  Google Scholar 

  47. Keller RP, Lodge DM, Finnoff DC (2007) Risk assessment for invasive species produces net bioeconomic benefits. Proc Natl Acad Sci USA 104:203–207

    CAS  Article  PubMed  Google Scholar 

  48. Klapwijk MJ, Hopkins AJM, Eriksson L et al (2016) Reducing the risk of invasive forest pests and pathogens: combining legislation, targeted management and public awareness. Ambio 45:223–234

    Article  PubMed  PubMed Central  Google Scholar 

  49. Kovacs KF, Haight RG, McCullough DG et al (2010) Cost of potential emerald ash borer damage in U.S. communities, 2009–2019. Ecol Econ 69:569–578

    Article  Google Scholar 

  50. Kovacs K, Václavík T, Haight RG et al (2011a) Predicting the economic costs and property value losses attributed to sudden oak death damage in California (2010–2020). J Environ Manag 92:1292–1302

    Article  Google Scholar 

  51. Kovacs KF, Mercader RJ, Haight RG et al (2011b) The influence of satellite populations of emerald ash borer on projected economic costs in U.S. communities, 2010–2020. J Environ Manag 92:2170–2181

    Article  Google Scholar 

  52. Kuo FE (2003) The role of arboriculture in a healthy social ecology. J Arboric 29:148

    Google Scholar 

  53. Lane CR, Beales PA, Hughes KJD et al (2003) First outbreak of Phytophthora ramorum in England, on Viburnum tinus. Plant Pathol 52:414

    Article  Google Scholar 

  54. Leung B, Springborn MR, Turner JA et al (2014) Pathway-level risk analysis: the net present value of an invasive species policy in the US. Front Ecol Environ 12:273–279

    Article  Google Scholar 

  55. Liebhold AM, MacDonald WL, Bergdahl D et al (1995) Invasion by exotic forest pests: a threat to forest ecosystems. For Sci 41:1–49

    Google Scholar 

  56. Liebhold AM, Brockerhoff EG, Garrett LJ et al (2012) Live plant imports: the major pathway for forest insect and pathogen invasions of the US. Front Ecol Environ 10:135–143

    Article  Google Scholar 

  57. Liebhold AM, McCullough DG, Blackburn LM et al (2013) A highly aggregated geographical distribution of forest pest invasions in the USA. Divers Distrib 19:1208–1216

    Article  Google Scholar 

  58. Liebhold AM, Berec L, Brockerhoff EG et al (2016) Eradication of invading insect populations: from concepts to applications. Annu Rev Entomol 61:335–352

    CAS  Article  PubMed  Google Scholar 

  59. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228

    Article  PubMed  Google Scholar 

  60. Lombaert E, Guillemaud T, Cornuet J-M et al (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE 5:e9743

    Article  PubMed  PubMed Central  Google Scholar 

  61. Loo JA (2009) Ecological impacts of non-indigenous invasive fungi as forest pathogens. Biol Invasions 11:81–96

    Article  Google Scholar 

  62. Lovett GM, Weiss M, Liebhold AM et al (2016) Nonnative forest insects and pathogens in the United States: impacts and policy options. Ecol Appl 26:1437–1455

    Article  PubMed  Google Scholar 

  63. MacFarlane DW, Meyer SP (2005) Characteristics and distribution of potential ash tree hosts for emerald ash borer. For Ecol Manag 213:15–24

    Article  Google Scholar 

  64. McCullough DG, Work TT, Cavey JF et al (2006) Interceptions of nonindigenous plant pests at US ports of entry and border crossings over a 17-year period. Biol Invasions 8:611–630

    Article  Google Scholar 

  65. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260

    Article  Google Scholar 

  66. Migliorini D, Ghelardini L, Tondini E et al (2015) The potential of symptomless potted plants for carrying invasive soilborne plant pathogens. Divers Distrib 21:1218–1229

    Article  Google Scholar 

  67. Mitchell RJ, Beaton JK, Bellamy PE et al (2014) Ash dieback in the UK: a review of the ecological and conservation implications and potential management options. Biol Conserv 175:95–109

    Article  Google Scholar 

  68. Morin RS, Liebhold AM, Pugh SA, Crocker SJ (2017) Regional assessment of emerald ash borer, Agrilus planipennis, impacts in forests of the Eastern United States. Biol Invasions 19:703–711

    Article  Google Scholar 

  69. Nowak DJ, Crane DE, Stevens JC (2006) Air pollution removal by urban trees and shrubs in the United States. Urban For Urban Green 4:115–123

    Article  Google Scholar 

  70. Ocasio-Morales RG, Tsopelas P, Harrington TC (2007) Origin of Ceratocystis platani on native Platanus orientalis in Greece and its impact on natural forests. Plant Dis 91:901–904

    Article  Google Scholar 

  71. Pautasso M, Aas G, Queloz V et al (2013) European ash (Fraxinus excelsior) dieback: a conservation biology challenge. Biol Conserv 158:37–49

    Article  Google Scholar 

  72. Pautasso M, Schlegel M, Holdenrieder O (2015) Forest health in a changing world. Microb Ecol 69:826–842

    Article  PubMed  Google Scholar 

  73. Pereyra PJ (2016) Revisiting the use of the invasive species concept: an empirical approach. Austral Ecol 41:519–528

    Article  Google Scholar 

  74. Poland TM, McCullough DG (2006) Emerald ash borer: invasion of the urban forest and the threat to North America’s ash resource. J For 104:118–124

    Google Scholar 

  75. Ramsfield T, Bentz B, Faccoli M et al (2016) Forest health in a changing world: effects of globalization and climate change on forest insect and pathogen impacts. Forestry 89:245–253

    Article  Google Scholar 

  76. Rassati D, Faccoli M, Petrucco Toffolo E et al (2015) Improving the early detection of alien wood-boring beetles in ports and surrounding forests. J Appl Ecol 52:50–58

    CAS  Article  Google Scholar 

  77. Raupp MJ, Cumming AB, Raupp EC (2006) Street tree diversity in eastern North America and its potential for tree loss to exotic borers. Arboric Urban For 32:297

    Google Scholar 

  78. Richardson DM, Pyšek P, Carlton JT (2011) A compendium of essential concepts and terminology in invasion ecology. In: Richardson DM (ed) Fifty years of invasion ecology. The legacy of Charles Elton. Wiley, Oxford, pp 409–420

    Google Scholar 

  79. Rizzo DM, Garbelotto M, Hansen EM (2005) Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annu Rev Phytopathol 43:309–335

    Article  PubMed  Google Scholar 

  80. Roques A, J-t Fan, Courtial B et al (2015) Planting sentinel European trees in Eastern Asia as a novel method to identify potential insect pest invaders. PLoS ONE 10:e0120864

    Article  PubMed  PubMed Central  Google Scholar 

  81. Roy BA, Alexander HM, Davidson J et al (2014) Increasing forest loss worldwide from invasive pests requires new trade regulations. Front Ecol Environ 12:457–465

    Article  Google Scholar 

  82. Santini A, Ghelardini L, De Pace C et al (2013) Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol 197:238–250

    CAS  Article  PubMed  Google Scholar 

  83. Schrader G, Unger J-G (2003) Plant quarantine as a measure against invasive alien species: the framework of the international plant protection convention and the plant health regulations in the European Union. Biol Invasions 5:357–364

    Article  Google Scholar 

  84. Scott P, Burgess T, Hardy G (2013) Globalisation and Phytophthora. In: Lamour K (ed) Phytophthora: a global perspective. CAB International, Wallingford, pp 226–232

    Google Scholar 

  85. Siegert NW, McCullough DG, Liebhold AM et al (2014) Dendrochronological reconstruction of the epicentre and early spread of emerald ash borer in North America. Divers Distrib 20:847–858

    Article  Google Scholar 

  86. Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102

    Article  Google Scholar 

  87. Stagoll K, Lindenmayer DB, Knight E et al (2012) Large trees are keystone structures in urban parks. Conserv Lett 5:115–122

    Article  Google Scholar 

  88. Stenlid J, Oliva J, Boberg JB et al (2011) Emerging diseases in European forest ecosystems and responses in society. Forests 2:486

    Article  Google Scholar 

  89. Tomoshevich M, Kirichenko N, Holmes K et al (2013) Foliar fungal pathogens of European woody plants in Siberia: an early warning of potential threats? For Pathol 43:345–359

    Google Scholar 

  90. Tubby KV, Webber JF (2010) Pests and diseases threatening urban trees under a changing climate. Forestry 83:451–459

    Article  Google Scholar 

  91. Vettraino A, Roques A, Yart A et al (2015) Sentinel trees as a tool to forecast invasions of alien plant pathogens. PLoS ONE 10:15

    Article  Google Scholar 

  92. Webber JF, Mullettm M, Brasier CM (2010) Dieback and mortality of plantation Japanese larch (Larix kaempferi) associated with infection by Phytophthora ramorum. New Dis Rep 22:19

    Article  Google Scholar 

  93. Wingfield MJ, Coetzee MPA, Crous PW et al (2010) Fungal phoenix rising from the ashes? IMA Fungus 1:149–153

    Article  PubMed  PubMed Central  Google Scholar 

  94. Wingfield MJ, Brockerhoff EG, Wingfield BD et al (2015) Planted forest health: the need for a global strategy. Science 349:832–836

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

This paper had its origins at a workshop on ‘Non-native species in urban environments’ hosted and funded by the DST-NRF Centre of Excellence for Invasion Biology (CIB) in Stellenbosch, South Africa, in November 2016. We thank Duccio Migliorini for useful discussion on the movement of pathogens through nursery stock. This work was funded by the South African National Department of Environmental Affairs.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Trudy Paap.

Additional information

Guest Editors: Mirijam Gaertner, John R. U. Wilson, Marc W. Cadotte, J. Scott MacIvor, Rafael D. Zenni and David M. Richardson/Urban Invasions

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Paap, T., Burgess, T.I. & Wingfield, M.J. Urban trees: bridge-heads for forest pest invasions and sentinels for early detection. Biol Invasions 19, 3515–3526 (2017). https://doi.org/10.1007/s10530-017-1595-x

Download citation

Keywords

  • Biological invasions
  • Biosecurity
  • Invasion pathways
  • Pathogens
  • Pests
  • Sentinel plants
  • Urban trees