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

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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.

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References

  • Appleton C, Gresham B (2003) Monitoring Essigella californica populations in Bay of Plenty forests. N Z Plant Prot 56:45–50

    Google Scholar 

  • 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 

  • Barham E, Sharrock S, Lane C, Baker R (2015) An international plant sentinel network. Sibbaldia J Bot Gard Hortic 13:83–97

    Google Scholar 

  • 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 60:602–613

    Article  Google Scholar 

  • 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 13:506–515

    Article  PubMed  Google Scholar 

  • BGCI [Botanic Gardens Conservation International] (2014) International Plant Sentinel Network. http://www.bgci.org/ourwork/ipsn/. Accessed 11 Nov 2017

  • Blackman RL, Eastop VF (1994) Aphids on the world’s trees: an identification and information guide. CAB International, Wallingford, p 987

    Google Scholar 

  • 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

  • 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 52:69–77

    Article  Google Scholar 

  • 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 40:109–114

    Google Scholar 

  • Brockerhoff EG, Bulman LS (2014) Biosecurity risks to New Zealand’s forests and the rationale for pathway risk management. N Z J For 59:3–8

    Google Scholar 

  • Brockerhoff EG, Liebhold AM (2017) Ecology of forest insect invasions. Biol Invasions 19:3141–3159

    Article  Google Scholar 

  • 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 34:158–174

    Google Scholar 

  • 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 Zealand

  • Carver M, Kent DS (2000) Essigella californica (Essig) and Eulachnus thunbergii Wilson (Hemiptera: Aphididae: Lachninae) on Pinus in southeastern Australia. Aust J Entomol 39:62–69

    Article  Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  • Dawson J, Lucas R (2011) New Zealand’s native trees. Craig Potton Publishing, Nelson

    Google Scholar 

  • Day KR, McClean SI (1991) Influence of the green spruce aphid on defoliation and radial stem growth of Sitka spruce. Ann Appl Biol 119:415–423

    Article  Google Scholar 

  • de Groot P, Turgeon J (2000) Insect-pine interactions. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 354–380

    Google Scholar 

  • 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) 8:5–8

    Google Scholar 

  • Edney-Browne E, Brockerhoff EG, Ward D (2018) Establishment patterns of non-native insects in New Zealand. Biol Invasions 20:1657–1669

    Article  Google Scholar 

  • 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 51–62

    Google Scholar 

  • Farjon A (2001) World checklist and bibliography of conifers, 2nd edn. Royal Botanic Gardens, Kew, London

    Google Scholar 

  • Flynn AR, Teulon DAJ, Stufkens MAW (2003) Distribution and flight activity of the Monterey pine aphid in New Zealand. N Z Plant Prot 56:33–38

    Google Scholar 

  • Gernandt DS, Geada López G, Ortiz García S, Liston A (2005) Phylogeny and classification of Pinus. Taxon 54:29–42

    Article  Google Scholar 

  • 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 17:1299–1305

    Article  Google Scholar 

  • Holman J (2009) The aphids and their host plants. Host plant catalog of aphids: palaearctic region. Springer, Berlin, pp 7–651

    Book  Google Scholar 

  • 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 265–310

    Google Scholar 

  • 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 22–29

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  PubMed  Google Scholar 

  • Kramer A, Hird A (2011) Building an international sentinel plant network. BGjournal 8:3–6

    Google Scholar 

  • Lenth R (2018) emmeans: Estimated marginal means, aka least-squares means. R package version 1.2.2

  • 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 10:135–143

    Article  Google Scholar 

  • Liebhold AM, Brockerhoff EG, Kalisz S, Nuñez MA, Wardle DA, Wingfield MJ (2017) Biological invasions in forest ecosystems. Biol Invasions 19:3437–3458

    Article  Google Scholar 

  • Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Martin NA, Paynter Q (2014) Predicting risk from adventive herbivores to New Zealand indigenous plants. N Z Entomol 37:21–28

    Article  Google Scholar 

  • May BM, Carlyle JC (2003) Effect of defoliation associated with Essigella californica on growth of mid-rotation Pinus radiata. For Ecol Manag 183:297–312

    Article  Google Scholar 

  • McCracken DP (1997) Gardens of empire: botanical institutions of the Victorian British empire. Leicester University Press, London, p 242

    Google Scholar 

  • 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:e35434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nichols JFA (1987) Damage and performance of the green spruce aphid, Elatobium abietinum on twenty spruce species. Entomol Exp Appl 45:211–217

    Article  Google Scholar 

  • Ohmart CP (1980) Insect pests of Pinus radiata plantations: present and possible future problems. Austral For 43:226–232

    Article  Google Scholar 

  • Paine TD (ed) (2006) Invasive forest insects, introduced forest trees, and altered ecosystems: ecological pest management in global forests of a changing world. Springer, Dordrecht

    Google Scholar 

  • Pellizzari G (2010) First record and establishment of Chionaspis wistariae Cooley (Hemiptera, Diaspididae) in Europe. J Entomol Acarol Res 42:147–151

    Article  Google Scholar 

  • 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 

  • 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:e0120864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 16:255–256

    Google Scholar 

  • 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)

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 70:1–102

    Google Scholar 

  • 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 262:1223–1235

    Article  Google Scholar 

  • 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 Zealand

  • Teulon DAJ, Stufkens MAW (2002) Biosecurity and aphids in New Zealand. N Z Plant Prot 55:12–17

    Google Scholar 

  • Teulon DAJ, Herman TJB, Davidson MM (2003) Monitoring Monterey pine aphid in Hawke’s Bay. N Z Plant Prot 56:39–44

    Google Scholar 

  • 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 110:1269–1274

    Article  PubMed  Google Scholar 

  • 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 76:131–132

    Google Scholar 

  • 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:e0188800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 61:179–184

    Google Scholar 

  • 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 10:253–262

    Article  Google Scholar 

  • Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in R. J Stat Softw 27:1–25

    Google Scholar 

  • Zondag R (1983a) Pine aphid. Eulachnus brevipilosus Börner (Hemiptera: Aphididae). Forest and Timber Insects in New Zealand, No. 55. Forest Research Institute, Rotorua, New Zealand

  • Zondag R (1983b) Spruce aphid. Elatobium abietinum (Walker) (Hemiptera: Aphidadae). Forest and Timber Insects in New Zealand, No. 54. Forest Research Institute, Rotorua, New Zealand

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

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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.

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Author notes

  1. Sarah Redlich

    Present address: Department of Animal Ecology and Tropical Biology, University of Würzburg, 97074, Würzburg, Germany

  2. Martin K.-F. Bader

    Present address: School of Science, Auckland University of Technology, Auckland, 1010, New Zealand

Authors and Affiliations

  1. School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, 8140, New Zealand

    Sarah Redlich, John Clemens & Eckehard G. Brockerhoff

  2. Christchurch Botanic Gardens, Christchurch City Council, PO Box 73036, Christchurch, 8154, New Zealand

    John Clemens & Dean Pendrigh

  3. Scion (New Zealand Forest Research Institute), PO Box 29237, Christchurch, 8440, New Zealand

    Martin K.-F. Bader, Anouchka Perret-Gentil & Eckehard G. Brockerhoff

  4. Bio-Protection Research Centre, Lincoln University, PO Box 85084, Lincoln, 7647, New Zealand

    William Godsoe & David A. J. Teulon

  5. Plant and Food Research, Private Bag 4704, Christchurch Mail Centre, Christchurch, 8140, New Zealand

    David A. J. Teulon

  6. Better Border Biosecurity (B3) Collaboration http://b3nz.org

    David A. J. Teulon & Eckehard G. Brockerhoff

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  1. Sarah Redlich
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Correspondence to Eckehard G. Brockerhoff.

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Redlich, S., Clemens, J., Bader, M.KF. et al. Identifying new associations between invasive aphids and Pinaceae trees using plant sentinels in botanic gardens. Biol Invasions 21, 217–228 (2019). https://doi.org/10.1007/s10530-018-1817-x

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