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Role of insect vectors in epidemiology and invasion risk of Fusarium circinatum, and risk assessment of biological control of invasive Pinus contorta

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Abstract

Pitch canker, caused by the pathogen Fusarium circinatum, is a serious disease of pines, Pinus species. It is a threat to natural and planted pine forests, and to date it has invaded countries across five continents. Pine-feeding insects can play a key role in the epidemiology of the disease, as wounding agents allowing pathogen access or as vectors transmitting the pathogen from infected to healthy trees. We reviewed the role of insects in the epidemiology of pitch canker worldwide and assessed which insects are present in New Zealand that may act as wounding agents or vectors to determine whether pathogen invasion could adversely affect Pinus radiata plantation forests and urban trees. We also evaluated whether cone or seed insects of pines could be introduced as biological control agents of invasive Pinus contorta and how this may affect the impact of a potential F. circinatum invasion. As there are no native pines or other Pinaceae in New Zealand, there are only a few pine insects, mainly accidental introductions. None of the insects recorded on pines in New Zealand is likely to be a vector, suggesting low disease risk. Of six potentially suitable biocontrol candidates, the European pine cone weevil Pissodes validirostris is the most promising regarding host specificity and impact on seed production, but there is uncertainty about its ability to act as a vector of F. circinatum. Our methodology to review and evaluate the vector potential of pine associates can be used as a generic framework to assess the potential impacts of F. circinatum invasion.

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References

  • Adams DH, Frankel SJ, Tidwell TE (1999) Chronicle of pitch canker in California. In: Devey ME, Matheson AC, Gordon TR (eds) Current and potential impacts of pitch canker in radiata pine, Proceedings of the IMPACT Monterey workshop, California, USA, 30 Nov to 3 Dec 1998. CSIRO Forestry and Forest Products Report No. 112, CSIRO, Canberra, pp 49–53

  • Annila E (1975) The biology of Pissodes validirostris Gyll. (Col. Curculionidae) and its harmfulness, especially in Scots pine seed orchards. Commun Inst For Fenn 85:1–95

    Google Scholar 

  • Annila E, Hiltunen R (1977) Damage by Pissodes validirostris (Coleoptera, Curculionidae) studied in relation to the monoterpene composition in Scots pine and Lodgepole pine. Ann Entomol Fenn 43:87–92

    CAS  Google Scholar 

  • Bachiller P (1966) Estudio sobre la biologia y tratamientos del Pissodes validirostris Gyll. Boll Serv Plagas For 9:133–136

    Google Scholar 

  • Bain J, Sopow SL, Bulman LS (2011) The sirex woodwasp in New Zealand: history and current status. In: Slippers B, de Groot P, Wingfield MJ (eds) The sirex woodwasp and its fungal symbiont. Research and management of a worldwide invasive pest. Springer, Dordrecht, pp 167–173

    Google Scholar 

  • Berndt LA, Brockerhoff EG, Jactel H, Weis T, Beaton J (2004) Biology and rearing of Pseudocoremia suavis, an endemic looper (Lepidoptera: Geometridae) with a history of outbreaks on exotic conifers. N Z Entomol 27:73–82

    Article  Google Scholar 

  • Blakeslee GM, Foltz JL (1981) The deodar weevil, a vector and wounding agent associated with pitch canker of slash pine. Phytopathology 71:861

    Google Scholar 

  • Blakeslee GM, Oak SW, Gregory W, Moses CS (1978) Natural association of Fusarium moniliforme var. subglutinans with Pissodes nemorensis. Phytopathol News 12:208

    Google Scholar 

  • Brockerhoff EG, Hosking GP (2001) Arhopalus tristis (F.) (Coleoptera: Cerambycidae), burnt pine longhorn beetle. Forest and timber insects in New Zealand 27 (revised). Forest Research Institute (Scion), Rotorua, pp 1–7

  • Brockerhoff EG, Kay M (1998) Prospects and risks of biological control of wilding Pinus contorta in New Zealand. In: Proceedings of the 51st New Zealand plant protection conference. New Zealand Plant Protection Society, pp 216–223

  • Brockerhoff EG, Hoffmann J, Roques A (2004) Is biological control an option for the management of wilding pines (Pinus spp.) in New Zealand? In: Hill RL, Zydenbos SM, Bezar CM (eds) Managing wilding conifers in New Zealand: present and future. New Zealand Plant Protection Society, Christchurch, pp 65–78

    Google Scholar 

  • Brockerhoff EG, Jones DC, Kimberley MO, Suckling DM, Donaldson T (2006) Nation-wide survey for invasive wood boring and bark beetles (Coleoptera) using traps baited with pheromones and kairomones. For Ecol Manag 228:234–240

    Article  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

    Google Scholar 

  • Carlucci A, Colatruglio L, Frisullo S (2007) First report of pitch canker caused by Fusarium circinatum on Pinus halepensis and P. pinea in Apulia (Southern Italy). Plant Dis 91:1683

    Article  Google Scholar 

  • Correll JC, Gordon TR, McCain AH, Fox JW, Koehler CS, Wood DL, Schultz ME (1991) Pitch canker in California: pathogenicity, distribution and canker development on Monterey pine (Pinus radiata). Plant Dis 75:676–682

    Article  Google Scholar 

  • Coutinho TA, Steenkamp ET, Mongwaketsi K, Wilmot M, Wingfield MJ (2007) First outbreak of pitch canker in a South African pine plantation. Australas Plant Path 36(3):256–261

    Article  Google Scholar 

  • Dallara PL (1997) Studies on the distribution, interspecific relationships, host range, and chemical ecology of Pityophthorus spp. (Coleoptera: Scolytidae) and selected insectan associates, and their associations with Fusarium subglutinans f. sp. pini in central coastal California. Dissertation, University of California, Berkeley

  • de Groot P, Turgeon JJ (1998) Insect–pine interactions. In: Richardson DA (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 354–380

    Google Scholar 

  • Delplanque A, Giovanini JP, Roques A, Augustin S (1988) Primeros problemas entomologicas consecutivos a la introduccion de Pinus contorta Douglas en Francia. Plagas Forestales 16:123–132

    Google Scholar 

  • Dick MA (1998) Pine pitch canker—the threat to New Zealand. N Z J For 42:30–34

    Google Scholar 

  • Dick M, Bain J (2004) Biocontrol of wildings—Could it be trouble? N Z Tree Grow 25(1):32

    Google Scholar 

  • Dormont L, Roques A (1999) A survey of insects attacking seed cones of Pinus cembra in the Alps, the Pyrenees and Massif Central. J Appl Entomol 123:65–72

    Article  Google Scholar 

  • Dormont L, Roques A (2001) Why are seed cones of Swiss stone pine (Pinus cembra) not attacked by the specialized pine cone weevil, Pissodes validirostris ? A case of host selection vs. host suitability. Entomol Exp Appl 99:157–163

    Article  Google Scholar 

  • Dwinell LD (1999) Global distribution of the pitch canker fungus. In: Devey ME, Matheson AC, Gordon TR (eds) Current and potential impacts of pitch canker in radiata pine, proceedings of the IMPACT Monterey workshop, California, USA, 30 Nov to 3 Dec 1998. CSIRO Forestry and Forest Products Report No. 112. CSIRO, Canberra, pp 54–57

  • Dwinell LD, Barrows-Broaddus J, Kuhlman EG (1985) Pitch canker: a disease complex of southern pines. Plant Dis 69:270–276

    Article  Google Scholar 

  • Erbilgin N, Storer AJ, Wood DL, Gordon TR (2005) Colonization of cut branches of five coniferous hosts of the pitch canker fungus by Pityophthorus spp. (Coleoptera: Scolytidae) in central, coastal California. Can Entomol 137:337–349

    Article  Google Scholar 

  • Erbilgin N, Ritokova G, Gordon TR, Wood DL, Storer AJ (2008) Temporal variation in contamination of pine engraver beetles with Fusarium circinatum in native Monterey pine forests in California. Plant Path 57:1103–1108

    Article  Google Scholar 

  • Erbilgin N, Gordon TR, Wood DL, Storer AJ (2009) Bark beetle (Coleoptera: Scolytidae)-mediated fungal infections of susceptible trees induce resistance to subsequent infections in a dose dependent manner. Agric For Entomol 11:255–263

    Article  Google Scholar 

  • Fourrier C, Antoine S, Piou D, Ioos R (2015) Rapid detection of Fusarium circinatum propagules on trapped pine beetles. Forest Pathol 45:324–330

    Article  Google Scholar 

  • Fowler SV, Syrett P, Hill RL (2000) Success and safety in the biological control of environmental weeds in New Zealand. Austral Ecol 25:553–562

    Article  Google Scholar 

  • Fox JW, Wood DL, Koehler CS (1990) Distribution and abundance of engraver beetles (Scolytidae: Ips species) on Monterey pines infected with pitch canker. Can Entomol 122:1157–1166

    Article  Google Scholar 

  • Fox JW, Wood DL, Koehler CS, O’Keefe ST (1991) Engraver beetles (Scolytidae: Ips species) as vectors of the pitch canker fungus, Fusarium subglutinans. Can Entomol 123:1355–1367

    Article  Google Scholar 

  • Gadgil P, Dick M, Simpson J, Bejakovich D, Ross M, Bain J, Wylie R, Horgan G (2003) Management plan for response to an incursion of pine pitch canker for Australia and for New Zealand. Unpublished report, Forest Research, Rotorua

  • Ganley R (2007) Pitch canker—risk of establishment in New Zealand based on a global perspective. N Z J For 52(2):26–30

    Google Scholar 

  • Ganley RJ, Watt MS, Manning L, Iturritxa E (2009) A global climatic risk assessment of pitch canker disease. Can J For Res 39:2246–2256

    Article  Google Scholar 

  • Gernandt DS, López GG, García SO, Liston A (2005) Phylogeny and classification of Pinus. Taxon 54:29–42

    Article  Google Scholar 

  • Gordon TR, Storer AJ, Wood DL (2001) The pitch canker epidemic in California. Plant Dis 85:1128–1139

    Article  Google Scholar 

  • Hedlin AF, Yates III HO, Cibrian-Tovar D, Ebel BH, Koerber TW, Merkel EP (1980) Cone and seed insects of North American conifers. Environment Canada, Canadian Forest Service, Ottawa; USDA Forest Service, Washington DC; Secr. Agric. Recur. Hidraul., Mexico, pp 1–122

  • Hoffmann JH, Moran VC, Van Wilgen BW (2011) Prospects for the biological control of invasive Pinus species (Pinaceae) in South Africa. Afr Entomol 19(2):393–401

    Article  Google Scholar 

  • Hoover K, Wood DL, Fox JW, Bros WE (1995) Quantitative and seasonal association of the pitch canker fungus, Fusarium subglutinans f. sp. pini, with Conophthorus radiatae (Coleoptera: Scolytidae) and Ernobius punctulatus (Coleoptera: Anobiidae) which infest Pinus radiata. Can Entomol 127:79–91

    Article  Google Scholar 

  • Hoover K, Wood DL, Storer AJ, Fox JW, Bros WE (1996) Transmission of the pitch canker fungus, Fusarium subglutinans f. sp. pini to Monterey pine, Pinus radiata, by cone- and twig-infesting beetles. Can Entomol 128:981–994

    Article  Google Scholar 

  • Hosking GP (1978) Oemona hirta (Fabricius) (Coleoptera: Cerambycidae), lemon tree borer. Forest and timber insects in New Zealand 31. Forest Research Institute, Rotorua, pp 1–4

    Google Scholar 

  • Hurley BP, Slippers B, Coutinho TA, Wingfield BD, Govender P, Wingfield MJ (2007) Molecular detection of fungi carried by Bradysia difformis (Sciaridae: Diptera) in South African forestry nurseries. South Hemisphere For J 69(2):103–109

    Article  CAS  Google Scholar 

  • Iturritxa E, Ganley RJ, Wright J, Heppe E, Steenkamp ET, Gordon TR, Wingfield MJ (2011) A genetically homogenous population of Fusarium circinatum causes pitch canker of Pinus radiata in the Basque Country, Spain. Fungal Biol 115(3):288–295

    Article  PubMed  Google Scholar 

  • Keen FP (1958) Cone and seed insects of western forest trees. US Dept Agric Tech Bull 1169:1–168

    Google Scholar 

  • Leach JB (1940) Insect transmission of plant diseases. McGraw-Hill, New York

    Google Scholar 

  • Ledgard NJ (1998) The spread of lodgepole pine (Pinus contorta, Dougl.) in New Zealand. For Ecol Manag 141:43–57

    Article  Google Scholar 

  • Lennox CL, Hoffmann JH, Coutinho TA, Roques A (2009) A threat of exacerbating the spread of pitch canker precludes further consideration of a cone weevil, Pissodes validirostris, for biological control of invasive pines in South Africa. Biol Control 50:179–184

    Article  Google Scholar 

  • Matthews FR (1962) Pitch canker-tip moth damage association on slash pine seedlings. J For 60:825–826

    Google Scholar 

  • McCain AH, Koehler CS, Tjosvold SA (1987) Pitch canker threatens California pines. Calif Agric 41:22–23

    Google Scholar 

  • Pfenning LH, Costa SDS, Melo MPD, Costa H, Ventura JA, Auer CG, Santos ÁFD (2014) First report and characterization of Fusarium circinatum, the causal agent of pitch canker in Brazil. Trop Plant Pathol 39(3):210–216

    Article  Google Scholar 

  • 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 34:1203–1221

    Article  Google Scholar 

  • Richardson DM, Higgins SI (1998) Pines as invaders in the southern hemisphere. In: Richardson DA (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 450–473

    Google Scholar 

  • Romón P, Iturrondobeitia JC, Gibson K, Lindgren BS, Goldarazena A (2007) Quantitative association of bark beetles with pitch canker fungus and effects of verbenone on their semiochemical communication in Monterey pine forests in northern Spain. Environ Entomol 36:743–750

    Article  PubMed  Google Scholar 

  • Romón P, Troya M, de Gamarra ME, Eguzkitza A, Iturrondobeitia J, Goldarazena A (2008) Fungal communities associated with pitch canker disease of Pinus radiata caused by Fusarium circinatum in northern Spain: association with insects and pathogen-saprophyte antagonistic interactions. Can J Plant Pathol 30:241–253

    Article  Google Scholar 

  • Roques A (1976) Observations sur la biologie et l’écologie de Pissodes validirostris Gyll. (Coléoptère, Curculionidae) en forêt de Fontainebleau. Ann Zool Ecol Anim 8:533–542

    Google Scholar 

  • Roques A (1977) Etude du complexe entomologique lié aux cônes de pin sylvestre en forêt de Fontainebleau. B Ecol 8:415–434

    Google Scholar 

  • Roques A (1983) Les insectes ravageurs des cônes et graines de conifères en France. INRA, Service des Publications, Versailles, France

    Google Scholar 

  • Roques A, El Alaoui El Fels MA (2002) Overview of the arthropod fauna exploiting seed cones in the Mediterranean Basin. In: Lieutier F, Ghaioule D (eds) Entomological research in Mediterrannean forest ecosystems, INRA Editions. Versailles, France, pp 59–78

    Google Scholar 

  • Roques A, Raimbault JP, Goussard F (1983) L’impact des insectes ravageurs des cônes et graines sur la régénération naturelle du Pin à crochets (Pinus uncinata Ram.) dans quelques forêts de montagne des Alpes du Sud et des Pyrénées Orientales. Acta Biol Montana 2:331–347

    Google Scholar 

  • Roques A, Roux-Morabito G, Hoffmann JH, Kleinhentz M, Gourov A (2004) Determining the suitability of a European cone weevil, Pissodes validirostris, for biological control of invasive pines in South Africa. In: Cullen JM, Briese DT, Kritikos DJ, Lonsdale WM, Morin L, Scott JK (eds) Proceedings of the XI international symposium on biological control of weeds, 27 April–2 May 2003, Canberra, Australia. CSIRO Entomology, Canberra, pp 315–321

    Google Scholar 

  • Rundel PW, Dickie IA, Richardson DM (2014) Tree invasions into treeless areas: mechanisms and ecosystem processes. Biol Invasions 16:663–675

    Article  Google Scholar 

  • Sakamoto JM, Gordon TR, Storer AJ, Wood DL (2007) The role of Pityophthorus spp. as vectors of pitch canker affecting Pinus radiata. Can Entomol 139:864–871

    Article  Google Scholar 

  • Six DL, Wingfield MJ (2011) The role of phytopathogenicity in bark beetle-fungus symbioses: a challenge to the classic paradigm. Annu Rev Entomol 56:255–272

    Article  CAS  PubMed  Google Scholar 

  • Storer AJ, Gordon TR, Wood DL, Bonello P (1997) Pitch canker disease of pines: current and future impacts. J For 95:21–26

    Google Scholar 

  • Storer AJ, Wood DL, Wikler KR, Gordon TR (1998) Association between a native spittlebug (Homoptera: Cercopidae) on Monterey pine and an introduced tree pathogen which causes pitch canker disease. Can Entomol 130:783–792

    Article  Google Scholar 

  • Storer AJ, Wood DL, Gordon TR (2002) The epidemiology of pitch canker of Monterey pine in California. Forest Sci 48:694–700

    Google Scholar 

  • Storer AJ, Wood DL, Gordon TR (2004a) Twig beetles, Pityophthorus spp. (Coleoptera: Scolytidae), as vectors of the pitch canker pathogen in California. Can Entomol 136:685–693

    Article  Google Scholar 

  • Storer AJ, Wood DL, Gordon TR (2004b) Could biological control of wilding pines increase the potential for damage by the pitch canker pathogen? In: Hill RL, Zydenbos SM, Bezar CM (eds) Managing wilding conifers in New Zealand: present and future. New Zealand Plant Protection Society, Christchurch, pp 97–111

    Google Scholar 

  • Suckling DM (2013) Benefits from biological control of weeds in New Zealand range from negligible to massive: a retrospective analysis. Biol Control 66:27–32

    Article  Google Scholar 

  • Turgeon JJ, Roques A, de Groot P (1994) Insect fauna of coniferous seed cones: diversity, host plant interactions, and management. Annu Rev Entomol 39:179–212

    Article  Google Scholar 

  • Van Wyk SJP, Boutigny A-L, Coutinho TA, Viljoen A (2012) Sanitation of a South African forestry nursery contaminated with Fusarium circinatum using hydrogen peroxide at specific oxidation reduction potentials. Plant Dis 96:875–880

    Article  Google Scholar 

  • Viljoen A, Wingfield MJ, Marasas WFO (1994) First report of Fusarium subglutinans f. sp. pini on seedlings in South Africa. Plant Dis 78:309–312

    Article  Google Scholar 

  • Viljoen A, Wingfield MJ, Marasas WFO, Coutinho TA (1997) Pitch canker of pines: a contemporary review. S Afr J Sci 93(9):411–413

    Google Scholar 

  • Wingfield MJ, Jacobs A, Coutinho TA, Ahumada R, Wingfield BD (2002) First report of the pitch canker fungus, Fusarium circinatum, on pines in Chile. Plant Pathol 51:397

    Article  Google Scholar 

  • Wingfield MJ, Hammerbacher A, Ganley RJ, Steenkamp ET, Gordon TR, Wingfield BD, Coutinho TA (2008) Pitch canker caused by Fusarium circinatum—a growing threat to pine plantations and forests worldwide. Australas Plant Path 37:319–334

    Article  Google Scholar 

  • Yamoah E, Jones EE, Suckling DM, Bourdôt GW, Walter M, Stewart A (2011) Using insects as potential vectors of Fusarium tumidum to control gorse. N Z Entomol 34:5–11

    Article  Google Scholar 

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Acknowledgments

We thank John Bain for reviewing an earlier version of the manuscript. Funding for this review was obtained from the New Zealand Government (FRST contract C04X0302 and Better Border Biosecurity via MBIE core funding to Scion, contract C04X1104).

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Authors and Affiliations

  1. Scion (New Zealand Forest Research Institute), Christchurch, New Zealand

    Eckehard G. Brockerhoff

  2. Scion (New Zealand Forest Research Institute), Rotorua, New Zealand

    Margaret Dick & Rebecca Ganley

  3. INRA – UR0633, Zoologie Forestière, 2163 Av. Pomme de pin, CS 40001, 45075, Orléans, France

    Alain Roques

  4. School of Forest Resources and Environmental Science, Michigan Technological University, 1400 Townsend Drive, Houghton, MI, 49931, USA

    Andrew J. Storer

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  1. Eckehard G. Brockerhoff
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  2. Margaret Dick
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  3. Rebecca Ganley
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  4. Alain Roques
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  5. Andrew J. Storer
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Correspondence to Eckehard G. Brockerhoff.

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Brockerhoff, E.G., Dick, M., Ganley, R. et al. Role of insect vectors in epidemiology and invasion risk of Fusarium circinatum, and risk assessment of biological control of invasive Pinus contorta . Biol Invasions 18, 1177–1190 (2016). https://doi.org/10.1007/s10530-016-1059-8

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