Advertisement

Biological Invasions

, Volume 21, Issue 1, pp 217–228 | Cite as

Identifying new associations between invasive aphids and Pinaceae trees using plant sentinels in botanic gardens

  • Sarah Redlich
  • John Clemens
  • Martin K.-F. Bader
  • Dean Pendrigh
  • Anouchka Perret-Gentil
  • William Godsoe
  • David A. J. Teulon
  • Eckehard G. BrockerhoffEmail author
Original Paper

Abstract

Despite progress in prevention and management of biological invasions, challenges remain, including difficulties with assessing future invasion risks. Predicting the identity of potentially damaging invaders is complex because they are often unknown as pests in their natural range. We used a plant sentinel approach to assess host ranges of invasive aphids across 62 conifer species from around the world in Christchurch Botanic Gardens, as a model for risk assessment such as for the ‘International Plant Sentinel Network’. Using standardised sampling, we obtained ca. 600 observations of aphid abundances (4731 individuals), mainly of the pine aphids Eulachnus brevipilosus and Essigella californica and the spruce aphids Cinara pilicornis and Elatobium abietinum. These aphids were highly genus-specific, despite the spatially mixed distribution of genera. A phylogenetic analysis of pine aphid host preferences showed that abundances of species varied among pine subgenera and the geographic origin of trees, with significantly more aphids on pines in the subgenus Pinus than the subgenus Strobus. Essigella californica occurred abundantly on many pines across most subsections in the subgenus Pinus whereas E. brevipilosus was largely restricted to a few species in the subsection Pinus. Our study revealed several new host records (previously unknown aphid-host relationships) including the abundant occurrence of E. brevipilosus on Japanese red pine, P. densiflora, and of E. californica on P. yunnanensis, P. serotina, P. brutia, and P. nigra, among others. Our study identified numerous novel insect-plant interactions that are likely to materialise if these aphids colonise new host plants, confirming the utility of the plant sentinel approach.

Keywords

Abies Alien invasive species Border biosecurity Cedrus Host range Insect-plant interactions Picea Pinus Plant phylogeny 

Notes

Acknowledgements

We thank John Bain, Lindsay Bulman and Stephanie Sopow for information about aphids on conifers in New Zealand, Brooke O’Connor for assistance with aphid sampling, Paul Bradbury for information about New Zealand’s biosecurity surveillance programmes, staff of the Christchurch Botanic Gardens for accommodating the field survey, and Carol Muir and David Voice for assistance with aphid identification. We thank the Friends of the Christchurch Botanic Gardens for co-sponsoring a University of Canterbury Summer Scholarship (to S.R.). Contributions by E.G.B. and M.K.-F.B. were supported by core funding from the New Zealand Government (MBIE contract C04X1104) to Scion via the ‘Better Border Biosecurity’ collaboration.

Supplementary material

10530_2018_1817_MOESM1_ESM.xlsx (15 kb)
Supplementary material 1 (XLSX 14 kb)

References

  1. Appleton C, Gresham B (2003) Monitoring Essigella californica populations in Bay of Plenty forests. N Z Plant Prot 56:45–50Google Scholar
  2. Barham E (2016) The unique role of sentinel trees, botanic gardens and arboreta in safeguarding global plant health. Plant Biosyst 150:377–380CrossRefGoogle Scholar
  3. Barham E, Sharrock S, Lane C, Baker R (2015) An international plant sentinel network. Sibbaldia J Bot Gard Hortic 13:83–97Google Scholar
  4. Bentz BJ, Régnière J, Fettig CJ, Hansen EM, Hayes JL, Hicke JA, Kelsey RG, Negrón JF, Seybold SJ (2010) Climate change and bark beetles of the western United States and Canada: direct and indirect effects. Bioscience 60:602–613CrossRefGoogle Scholar
  5. Bertheau C, Brockerhoff EG, Roux-Morabito G, Lieutier F, Jactel H (2010) Novel insect-tree associations resulting from accidental and intentional biological ‘invasions’: a meta-analysis of effects on insect fitness. Ecol Lett 13:506–515CrossRefGoogle Scholar
  6. BGCI [Botanic Gardens Conservation International] (2014) International Plant Sentinel Network. http://www.bgci.org/ourwork/ipsn/. Accessed 11 Nov 2017
  7. Blackman RL, Eastop VF (1994) Aphids on the world’s trees: an identification and information guide. CAB International, Wallingford, p 987Google Scholar
  8. Blackman RL, Eastop VF (2014) Aphids on the world’s plants: an online identification and information guide. http://www.aphidsonworldsplants.info. Accessed between 23 Oct 2014 and 13 Nov 2017
  9. Branco M, Brockerhoff EG, Castagneyrol B, Orazio C, Jactel H (2015) Host range expansion of native insects to exotic trees increases with area of introduction and the presence of congeneric native trees. J Appl Ecol 52:69–77CrossRefGoogle Scholar
  10. Britton KO, White P, Kramer A, Hudler G (2010) A new approach to stopping the spread of invasive insects and pathogens: early detection and rapid response via a global network of sentinel plantings. N Z J For Sci 40:109–114Google Scholar
  11. Brockerhoff EG, Bulman LS (2014) Biosecurity risks to New Zealand’s forests and the rationale for pathway risk management. N Z J For 59:3–8Google Scholar
  12. Brockerhoff EG, Liebhold AM (2017) Ecology of forest insect invasions. Biol Invasions 19:3141–3159CrossRefGoogle Scholar
  13. Brockerhoff EG, Barratt BI, Beggs JR, Fagan LL, Malcolm K, Phillips CB, Vink CJ (2010) Impacts of exotic invertebrates on New Zealand’s indigenous species and ecosystems. N Z J Ecol 34:158–174Google Scholar
  14. Bulman LS (1990) BUGS and HEALTH—integral part of forest protection strategy. What’s new in Forest Research No. 197. Forest Research Institute, Rotorua, New ZealandGoogle Scholar
  15. Carver M, Kent DS (2000) Essigella californica (Essig) and Eulachnus thunbergii Wilson (Hemiptera: Aphididae: Lachninae) on Pinus in southeastern Australia. Aust J Entomol 39:62–69CrossRefGoogle Scholar
  16. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  17. Dawson J, Lucas R (2011) New Zealand’s native trees. Craig Potton Publishing, NelsonGoogle Scholar
  18. Day KR, McClean SI (1991) Influence of the green spruce aphid on defoliation and radial stem growth of Sitka spruce. Ann Appl Biol 119:415–423CrossRefGoogle Scholar
  19. de Groot P, Turgeon J (2000) Insect-pine interactions. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 354–380Google Scholar
  20. Dodd J, Jones C (2011) Towards a new social purpose: the role of botanic gardens in the 21st century. Roots (Bot Gard Conserv Int Edu Rev) 8:5–8Google Scholar
  21. Edney-Browne E, Brockerhoff EG, Ward D (2018) Establishment patterns of non-native insects in New Zealand. Biol Invasions 20:1657–1669CrossRefGoogle Scholar
  22. Fagan LL, Bithell SL, Dick MA (2008) Systems for identifying invasive threats to New Zealand flora by using overseas plantings of New Zealand native plants. In: Froud KJ, Popay IA, Zydenbos SM (eds) Surveillence for biosecurity: pre-border to pest management. New Zealand Plant Protection Society, Auckland, pp 51–62Google Scholar
  23. Farjon A (2001) World checklist and bibliography of conifers, 2nd edn. Royal Botanic Gardens, Kew, LondonGoogle Scholar
  24. Flynn AR, Teulon DAJ, Stufkens MAW (2003) Distribution and flight activity of the Monterey pine aphid in New Zealand. N Z Plant Prot 56:33–38Google Scholar
  25. Gernandt DS, Geada López G, Ortiz García S, Liston A (2005) Phylogeny and classification of Pinus. Taxon 54:29–42CrossRefGoogle Scholar
  26. Groenteman R, Forgie SA, Hoddle MS, Ward DF, Goeke DF, Anand N (2015) Assessing invasion threats: novel insect-pathogen-natural enemy associations with native New Zealand plants in southern California. Biol Invasions 17:1299–1305CrossRefGoogle Scholar
  27. Holman J (2009) The aphids and their host plants. Host plant catalog of aphids: palaearctic region. Springer, Berlin, pp 7–651CrossRefGoogle Scholar
  28. Jactel H, Barbaro L, Battisti A, Bosc A, Branco M, Brockerhoff E, Castagneyrol B, Dulaurent A-M, Hódar JA, Jacquet J-S, Mateus E, Paiva MR, Roques A, Samalens J-C, Santos H, Schlyter F (2015) Insect—tree interactions in Thaumetopoea pityocampa. In: Roques A (ed) Processionary moths and climate change: an update. Springer, Dordrecht, pp 265–310Google Scholar
  29. Kent D, Carnegie A (2000) Distribution of Essigella californica in New South Wales & ACT. In: Collett NG, Simpson J, Schoenborn C (eds) A review of the current status of the Monterey pine aphid Essigella californica (Essig.), Proceedings of a Workshop. Department of Natural Resources and Environment, Heidelberg, Victoria, Australia, pp 22–29Google Scholar
  30. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204CrossRefGoogle Scholar
  31. Kramer A, Hird A (2011) Building an international sentinel plant network. BGjournal 8:3–6Google Scholar
  32. Lenth R (2018) emmeans: Estimated marginal means, aka least-squares means. R package version 1.2.2Google Scholar
  33. Liebhold AM, Brockerhoff EG, Garrett LJ, Parke JL, Britton KO (2012) Live plant imports: the major pathway for forest insect and pathogen invasions of the US. Front Ecol Environ 10:135–143CrossRefGoogle Scholar
  34. Liebhold AM, Brockerhoff EG, Kalisz S, Nuñez MA, Wardle DA, Wingfield MJ (2017) Biological invasions in forest ecosystems. Biol Invasions 19:3437–3458CrossRefGoogle Scholar
  35. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545CrossRefGoogle Scholar
  36. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  37. Martin NA, Paynter Q (2014) Predicting risk from adventive herbivores to New Zealand indigenous plants. N Z Entomol 37:21–28CrossRefGoogle Scholar
  38. May BM, Carlyle JC (2003) Effect of defoliation associated with Essigella californica on growth of mid-rotation Pinus radiata. For Ecol Manag 183:297–312CrossRefGoogle Scholar
  39. McCracken DP (1997) Gardens of empire: botanical institutions of the Victorian British empire. Leicester University Press, London, p 242Google Scholar
  40. Morin L, Aveyard R, Lidbetter JR, Wilson PG (2012) Investigating the host-range of the rust fungus Puccinia psidii sensu lato across tribes of the family Myrtaceae present in Australia. PLoS ONE 7:e35434CrossRefGoogle Scholar
  41. Nichols JFA (1987) Damage and performance of the green spruce aphid, Elatobium abietinum on twenty spruce species. Entomol Exp Appl 45:211–217CrossRefGoogle Scholar
  42. Ohmart CP (1980) Insect pests of Pinus radiata plantations: present and possible future problems. Austral For 43:226–232CrossRefGoogle Scholar
  43. Paine TD (ed) (2006) Invasive forest insects, introduced forest trees, and altered ecosystems: ecological pest management in global forests of a changing world. Springer, DordrechtGoogle Scholar
  44. Pellizzari G (2010) First record and establishment of Chionaspis wistariae Cooley (Hemiptera, Diaspididae) in Europe. J Entomol Acarol Res 42:147–151CrossRefGoogle Scholar
  45. Poland TM, McCullough DG (2006) Emerald ash borer: invasion of the urban forest and the threat to North America’s ash resource. J For 104:118–124Google Scholar
  46. Roques A, Fan JT, Courtial B, Zhang YZ, Yart A, Auger-Rozenberg MA, Denux O, Kenis M, Baker R, Sun JH (2015) Planting sentinel European trees in Eastern Asia as a novel method to identify potential insect pest invaders. PLoS ONE 10:e0120864CrossRefGoogle Scholar
  47. Seco Fernández MV, Mier Durante MP (1992) Presencia en España del pulgón verde de los pinos americanos: Essigella (Hom., Aphididae: Cinarinae). B Asoc Esp Entomol 16:255–256Google Scholar
  48. Seebens H, Blackburn TM, Dyer EE et al. (2018) Global rise in emerging alien species results from increased accessibility of new source pools. Proc Natl Acad Sci USA.  https://doi.org/10.1073/pnas.1719429115 (in press)Google Scholar
  49. Sorensen JT (1994) A revision of the aphid genus Essigella (Homoptera: Aphididae: Lachninae): its ecological associations with, and evolution on, Pinaceae hosts. Pan-Pacific Entomol 70:1–102Google Scholar
  50. Straw N, Fielding N, Green G, Price J, Williams D (2011) Defoliation and growth relationships for mid-rotation Sitka spruce attacked by the green spruce aphid, Elatobium abietinum (Walker). For Ecol Manag 262:1223–1235CrossRefGoogle Scholar
  51. Teulon DAJ (1999) Multiple-entry key for aphids on forest trees in New Zealand. CropInfo Report No. 619 for Forest Health Research Collaborative, Crop and Food Research, Christchurch, New ZealandGoogle Scholar
  52. Teulon DAJ, Stufkens MAW (2002) Biosecurity and aphids in New Zealand. N Z Plant Prot 55:12–17Google Scholar
  53. Teulon DAJ, Herman TJB, Davidson MM (2003) Monitoring Monterey pine aphid in Hawke’s Bay. N Z Plant Prot 56:39–44Google Scholar
  54. Théry T, Brockerhoff EG, Carnegie AJ, Chen R, Elms SR, Hullé M, Glatz R, Ortego J, Qiao GX, Turpeau É, Favret C (2017) EF-1α DNA sequences indicate multiple origins of introduced populations of Essigella californica (Hemiptera: Aphididae). J Econ Entomol 110:1269–1274CrossRefGoogle Scholar
  55. Turpeau E, Remaudière G (1990) Découverte en France d’un puceron des pins américains du genre Essigella (Hom. Aphididae). Comptes-rendus de l’Académie d’Agriculture de France 76:131–132Google Scholar
  56. Vettraino AM, Li HM, Eschen R, Morales-Rodriguez C, Vannini A (2017) The sentinel tree nursery as an early warning system for pathway risk assessment: fungal pathogens associated with Chinese woody plants commonly shipped to Europe. PLoS ONE 12:e0188800CrossRefGoogle Scholar
  57. Watson MC, Kriticos DJ, Drayton GM, Teulon DAJ, Brockerhoff EG (2008) Assessing the effects of Essigella californica on Pinus radiata at two sites in New Zealand. N Z Plant Prot 61:179–184Google Scholar
  58. Wharton TN, Kriticos DJ (2004) The fundamental and realized niche of the Monterey pine aphid, Essigella californica (Essig) (Hemiptera: Aphididae): implications for managing softwood plantations in Australia. Divers Distrib 10:253–262CrossRefGoogle Scholar
  59. Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in R. J Stat Softw 27:1–25Google Scholar
  60. Zondag R (1983a) Pine aphid. Eulachnus brevipilosus Börner (Hemiptera: Aphididae). Forest and Timber Insects in New Zealand, No. 55. Forest Research Institute, Rotorua, New ZealandGoogle Scholar
  61. Zondag R (1983b) Spruce aphid. Elatobium abietinum (Walker) (Hemiptera: Aphidadae). Forest and Timber Insects in New Zealand, No. 54. Forest Research Institute, Rotorua, New ZealandGoogle Scholar
  62. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Sarah Redlich
    • 1
    • 2
  • John Clemens
    • 1
    • 3
  • Martin K.-F. Bader
    • 4
    • 5
  • Dean Pendrigh
    • 3
  • Anouchka Perret-Gentil
    • 4
  • William Godsoe
    • 6
  • David A. J. Teulon
    • 6
    • 7
    • 8
  • Eckehard G. Brockerhoff
    • 1
    • 4
    • 8
    Email author
  1. 1.School of Biological SciencesUniversity of CanterburyChristchurchNew Zealand
  2. 2.Department of Animal Ecology and Tropical BiologyUniversity of WürzburgWürzburgGermany
  3. 3.Christchurch Botanic Gardens, Christchurch City CouncilChristchurchNew Zealand
  4. 4.Scion (New Zealand Forest Research Institute)ChristchurchNew Zealand
  5. 5.School of ScienceAuckland University of TechnologyAucklandNew Zealand
  6. 6.Bio-Protection Research CentreLincoln UniversityLincolnNew Zealand
  7. 7.Plant and Food ResearchChristchurchNew Zealand
  8. 8.Better Border Biosecurity (B3) Collaboration

Personalised recommendations