No rest for the laurels: symbiotic invaders cause unprecedented damage to southern USA forests

Abstract

Laurel wilt is an extraordinarily destructive exotic tree disease in the southeastern United States that involves new-encounter hosts in the Lauraceae, an introduced vector (Xyleborus glabratus) and pathogen symbiont (Raffaelea lauricola). USDA Forest Service Forest Inventory and Analysis data were used to estimate that over 300 million trees of redbay (Persea borbonia sensu lato) have succumbed to the disease since the early 2000s (ca 1/3 of the pre-invasion population). In addition, numerous native shrub and tree species in the family are susceptible and  threatened in the Western Hemisphere. Genetic markers were used to test the hypothesis that the vector and pathogen entered North America as a single introduction. With a portion of the cytochrome oxidase I gene, a single X. glabratus haplotype was detected in the USA. Similarly, Amplified Fragment Length Polymorphisms indicated that 95% (54 of 57) of the isolates of R. lauricola that were examined were of a single clonal genotype; only minor variation was detected in three polymorphic isolates. Similar levels of disease developed after swamp bay (P. palustris) was inoculated with each of the four genotypes of R. lauricola. It is proposed that a single founding event is responsible for the laurel wilt epidemic in the United States.

This is a preview of subscription content, log in to check access.

Fig. 1

Photos by: a Chip Bates, Georgia Forestry Commission. b Jiri Hulcr, University of Florida

Fig. 2
Fig. 3

References

  1. Anagostakis SL (1987) Chestnut blight: the classical problem of an introduced pathogen. Mycologia 79:22–37

    Google Scholar 

  2. Anderson PK, Cuningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19:535–544

    Article  PubMed  Google Scholar 

  3. Bates CA, Fraedrich S, Harrington T, Cameron RS, Menard RD, Best GS (2013) First report of laurel wilt, caused by Raffaelea lauricola, on sassafras (Sassafras albidum) in Alabama. Plant Dis 97:668

    Article  Google Scholar 

  4. Bechtold WA, Scott CT (2005) The Forest Inventory and Analysis plot design. In: Bechtold WA, Patterson PL (eds) The enhanced Forest Inventory and Analysis program—national sampling design and estimation procedures. General Technical Report SRS-80. USDA, Forest Service, Southern Research Station. http://www.srs.fs.usda.gov/pubs/gtr/gtr_srs080/gtr_srs080.pdf. Accessed 28 Sep 2016

  5. Boyd LL, Freer-Smith Ph, Gilligan CA, Godfray HCJ (2013) The consequences of tree pests and diseases for ecosystem services. Science 342:1235773

    CAS  Article  PubMed  Google Scholar 

  6. Brasier CM (2001) Rapid evolution of introduced plant pathogens via interspecific hybridization. Hybridization is leading to rapid evolution of the Dutch elm disease and other fungal plant pathogens. Bioscience 51:123–133

    Article  Google Scholar 

  7. Cameron RS, Hanula J, Fraedrich SW, Bates C (2015) Progression of laurel wilt disease within redbay and sassafras populations in southeast Georgia. Southeast Nat 14:650–674

    Article  Google Scholar 

  8. Campbell L, Madden LV (1990) Introduction to Plant Disease Epidemiology. Wiley, NY

    Google Scholar 

  9. Campbell AS, Ploetz RC, Dreaden TJ, Kendra PE, Montgomery WS (2017) Geographic variation in mycangial communities of Xyleborus glabratus. Mycologia 108:657–667

    Article  Google Scholar 

  10. Carrillo D, Duncan RE, Ploetz JN, Campbell AF, Ploetz RC, Peña JE (2014) Lateral transfer of a phytopathogenic symbiont among native and exotic ambrosia beetles. Plant Pathol 63:54–62

    Article  Google Scholar 

  11. Chupp AD, Battaglia LL (2014) Potential for host shifting in Papilio palamedes following invasion of laurel wilt disease. Biol Invasions 16:2639–2651

    Article  Google Scholar 

  12. Chupp AD, Battaglia LL, Schauber EM, Sipes SD (2015) Orchid-pollinator interactions and potential vulnerability to potential biological invasions. AoB Plants 7:plv099

    Article  PubMed  PubMed Central  Google Scholar 

  13. Cognato AI, Hulcr J, Dole SA, Jordal BH (2011a) Phylogeny of haplo–diploid, fungus-growing ambrosia beetles (Curculionidae: Scolytinae: Xyleborini) inferred from molecular and morphological data. Zool Scr 40:174–186

    Google Scholar 

  14. Cognato AI, Olson RO, Rabaglia RJ (2011b) An Asian ambrosia beetle, Xylosandrus amputatus (Blandford) (Curculionidae: Scolytinae: Xyleborini), discovered in Florida, USA. Coleops Bull 65:43–45

    Article  Google Scholar 

  15. Cognato AI, Hoebeke ER, Kajimura H, Smith S (2015) History of the exotic ambrosia beetles Euwallacea interjectus (Blandford) and E. validus (Eichhoff) (Coleoptera: Curculionidae: Xyleborini) in the United States of America. J Econ Entomol 108:129–1135

    Article  Google Scholar 

  16. Dole SA, Jordal BH, Cognato AI (2010) Polyphyly of Xylosandrus Reitter inferred from nuclear and mitochondrial genes. Mol Phylogenet Evol 53:773–782

    Article  Google Scholar 

  17. Drake JM, Lodge DM (2006) Allee effects, propagule pressure and the probability of establishment: risk analysis for biological invasions. Biol Invasions 8:65–375

    Google Scholar 

  18. Dreaden TJ, Davis JM, Harmon CL, Ploetz RC, Palmateer AJ, Soltis PS, Smith JA (2014) Development of multilocus PCR assays for Raffaelea lauricola, causal agent of laurel wilt disease. Plant Dis 98:379–383

    CAS  Article  Google Scholar 

  19. Dreaden TJ, Campbell AS, Gonzalez-Benecke CA, Ploetz RC, Smith JA (2017) Response of swamp bay, Persea palustris, and redbay, P. borbonia, to Raffaelea lauricola spp. isolated from Xyleborus glabratus. For Pathol 47:e12288

    Article  Google Scholar 

  20. Duncan RP (2016) How propagule size and environmental suitability jointly determine establishment success: a test using dung beetle introductions. Biol Invasions 18:985–996

    Article  Google Scholar 

  21. Duran A, Gryzenhout M, Drenth A, Slippers B, Ahumada R, Wingfield BD, Wingfield MJ (2010) AFLP analysis reveals a clonal population of Phytophthora pinifolia in Chile. Fungal Biol 114:746–752

    Article  PubMed  Google Scholar 

  22. Engering A, Hogerwerf L, Slingenbergh J (2013) Pathogen-host-environment interplay and disease emergence. Emerg Microbe Infect 2:e5

    CAS  Article  Google Scholar 

  23. Evans JP, Scheffers BR, Hess M (2013) Effect of laurel wilt invasion on redbay populations in a maritime forest community. Biol Invasions 16:1581–1588

    Article  Google Scholar 

  24. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194

    CAS  Article  PubMed  Google Scholar 

  25. Formby JP, Krishnan N, Riggins JJ (2013) Supercooling in the redbay ambrosia beetle (Coleoptera: Curculionidae). Fla Entomol 96:1530–1540

    Article  Google Scholar 

  26. Fraedrich SW, Harrington TC, Rabaglia RJ, Ulyshen MD, Hanula JL, Eickwort JM, Miller DR (2008) A fungal symbiont of the redbay ambrosia beetle causes a lethal wilt in redbay and other Lauraceae in the southeastern United States. Plant Dis 92:215–224

    Article  Google Scholar 

  27. Fraedrich SW, Harrington TC, Bates CA, Johnson J, Reid LS, Best GS, Leininger TD, Hawkins TS (2011) Susceptibility to laurel wilt and disease incidence in two rare plant species, pondberry and pondspice. Plant Dis 95:1056–1062

    Article  Google Scholar 

  28. Fraedrich SW, Harrington TC, Best GS (2015) Xyleborus glabratus attacks and systemic colonization by Raffaelea lauricola associated with dieback of Cinnamomum camphora in the southeastern United States. For Pathol 45:60–70

    Article  Google Scholar 

  29. Germain-Aubrey CC, Nelson C, Soltis DE, Soltis PA, Gitzendanner MA (2016) Are microsatellite fragment lengths useful for population-level studies? The case of Polygala lewtonii (Polygalaceae). Appl Plant Sci 4:1500115

    Article  Google Scholar 

  30. Grosholz ED (2005) Recent biological invasion may hasten invasional meltdown by accelerating historical introductions. Proc Nat Acad Sci USA 102:1088–1091

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Grünwald NJ, Garbelotto M, Goss EM, Heungens K, Prospero S (2012) Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends Microbiol 20:131–138

    Article  PubMed  Google Scholar 

  32. Hanula JL, Sullivan B (2008) Manuka oil and phoebe oil are attractive baits for Xyleborus glabratus (Coleoptera: Scolytinae), the vector of laurel wilt. Environ Entomol 37:1403–1409

    CAS  Article  PubMed  Google Scholar 

  33. Harrington TC (1981) Cycloheximide sensitivity as a taxonomic character in Ceratocystis. Mycologia 73:1123–1129

    CAS  Article  Google Scholar 

  34. Harrington TC, Fraedrich SW (2010) Quantification of propagules of the laurel wilt fungus and other mycangial fungi from the redbay ambrosia beetle, Xyleborus glabratus. Phytopathology 100:118–1123

    Article  Google Scholar 

  35. Harrington TC, Fraedrich SW, Aghayeva DN (2008) Raffaelea lauricola, a new ambrosia beetle symbiont and pathogen on the Lauraceae. Mycotaxon 104:399–404

    Google Scholar 

  36. Harrington TC, Yun HY, Lu SS, Goto H, Fraedrich SW (2011) Isolations from the redbay ambrosia beetle, Xyleborus glabratus, confirm that the laurel wilt pathogen, Raffalea lauricola, originated in Asia. Mycologia 103:1028–1036

    Article  PubMed  Google Scholar 

  37. 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 

  38. Hicke JA, Jenkins JC, Ojima DS, Ducey M (2007) Spatial patterns of forest characteristics in the western United States derived from inventories. Ecol Appl 17:2387–2402

    Article  PubMed  Google Scholar 

  39. Hoegger PJ, Rigling D, Holdenrieder O, Heiniger U (2000) Genetic structure of newly established Cryphonectria parasitica. Mycol Res 104:1108–1116

    CAS  Article  Google Scholar 

  40. Hughes MA, Smith JA, Ploetz RC, Kendra PE, Mayfield AE III, Hanula JL, Hulcr J, Stelinski LL, Cameron S, Riggins JJ, Carrillo D, Rabaglia R, Eickwort J, Pernas T (2015a) Recovery plan for laurel wilt on redbay and other forest species caused by Raffaelea lauricola and disseminated by Xyleborus glabratus. Plant Health Prog. doi:10.1094/PHP-RP-15-0017

    Google Scholar 

  41. Hughes MA, Inch SA, Ploetz RC, Er HL, van Bruggen AHC, Smith JA (2015b) Responses of swamp bay, Persea palustris, and avocado, Persea americana, to various concentrations of the laurel wilt pathogen, Raffaelea lauricola. For Pathol 45:111–119

    Article  Google Scholar 

  42. Hulcr J, Dunn RR (2011) The sudden emergence of pathogenicity in insect-fungus symbioses threatens naive forest ecosystems. Proc R Soc B 278:2866–2873

    Article  PubMed  PubMed Central  Google Scholar 

  43. Hulcr J, Lou QZ (2013) The redbay ambrosia beetle (Coleoptera: Curculionidae) prefers Lauraceae in its native range: records from the Chinese National Insect Collection. Fla Entomol. 96:1595–1596

    Article  Google Scholar 

  44. Ivors KL, Hayden KJ, Bonants PJM, Rizzo DM, Garbelotto M (2004) AFLP and phylogenetic analysis of North American and European populations of Phytophthora ramorum. Mycol Res 108:378–392

    CAS  Article  PubMed  Google Scholar 

  45. Jackson MC (2015) Interactions among multiple invasive animals. Ecology 96:2035–2041

    CAS  Article  PubMed  Google Scholar 

  46. Kim M-S, Klopfenstein NB, Hanna JW, McDonald GI (2006) Characterization of North American Armillaria species: genetic relationships determined by ribosomal DNA sequences and AFLP markers. For. Pathol 36:145–164

    Article  Google Scholar 

  47. Kirkendal LR, Biedermann PHW, Jordal BJ (2015) Evolution and diversity of bark and ambrosia beetles. In: Vega FE, Hofstetter RW (eds) Bark beetles: biology and ecology of native and invasive species, 1st edn. Elsevier, San Diego, pp 85–156

    Google Scholar 

  48. Koch FH, Smith WD (2008) Spatio-temporal analysis of Xyleborus glabratus (Coleoptera: Circulionidae: Scolytinae) invasion in eastern US forests. Environ Entomol 37:442–452

    CAS  Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  50. Kubisiak TL, Anderson CL, Amerson ML, Smith JA, Davis JM, Nelson CD (2011) A genomic map enriched for markers linked to Avr1 in Cronartium quercum f.sp. fusiforme. Fungal Genet Biol 48:266–274

    CAS  Article  PubMed  Google Scholar 

  51. Liebhold AM, Tobin PC (2008) Population ecology of insect invasions and their management. Annu Rev Entomol 53:387–408

    CAS  Article  PubMed  Google Scholar 

  52. 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 

  53. Mayfield AE III, Smith JA, Hughes MA, Dreaden TJ (2008) First report of laurel wilt disease caused by a Raffaelea sp. on avocado in Florida. Plant Dis 92:976

    Article  Google Scholar 

  54. McDonald BA (1997) The population genetics of fungi: tools and techniques. Phytopathology 87:448–453

    CAS  Article  PubMed  Google Scholar 

  55. McRoberts RE (2005) The enhanced Forest Inventory and Analysis program. In: Bechtold WA, Patterson PL (eds) The enhanced Forest Inventory and Analysis program—national sampling design and estimation procedures General Technical Report SRS-80. USDA, Forest Service, Southern Research Station. http://www.srs.fs.usda.gov/pubs/gtr/gtr_srs080/gtr_srs080.pdf. Accessed 28 Sep 2016

  56. Meudt HM, Clarke AC (2007) Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends Plant Sci 12:106–117

    CAS  Article  PubMed  Google Scholar 

  57. Mosquera M, Evans EA, Ploetz R (2015) Assessing the profitability of avocado production in south Florida in the presence of laurel wilt. Theor Econ Lett 5:343–356

    Article  Google Scholar 

  58. Noss RF, Platt WJ, Sorrie BA, Weakley AS, Means DB, Costanza J, Peet RK (2015) How global biodiversity hotspots many go unrecognized: lessons from the North American Coastal Plain. Divers Distrib 21:236–244

    Article  Google Scholar 

  59. Pautasso M, Aas G, Queloz V, Holdenrieder O (2013) European ash (Fraxinus excelsior) dieback—a conservation biology challenge. Biol Conserv 158:37–49

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  61. Ploetz RC, Konkol J (2013) First report of gulf licaria, Licaria triandra, as a suscept of laurel wilt. Plant Dis 97:1248

    Article  Google Scholar 

  62. Ploetz RC, Hulcr J, Wingfield MJ, de Beer ZW (2013) Destructive tree diseases associated with ambrosia and bark beetles: black swan events in tree pathology? Plant Dis 95:856–872

    Article  Google Scholar 

  63. Ploetz RC, Thant YY, Hughes MA, Dreaden TJ, Konkol JL, Kyaw AT, Smith JA, Harmon CL (2016) Laurel wilt, caused by Raffaelea lauricola, is detected for the first time outside of the southeastern United States. Plant Dis 100:2166

    Article  Google Scholar 

  64. Ploetz RC, Konkol JL, Pérez-Martínez JM, Fernandez R (2017a) Management of laurel wilt of avocado, caused by Raffaelea lauricola. Eur J Plant Pathol. doi:10.1007/s10658-017-1173-1

    Google Scholar 

  65. Ploetz RC, Kendra PE, Choudhury RA, Rollins JA, Campbell A, Garrett K, Hughes M, Dreaden T (2017b) Laurel wilt in natural and agricultural ecosystems: understanding the drivers and scales of complex pathosystems. Forests 8:48. doi:10.3390/f8020048

    Article  Google Scholar 

  66. Rabaglia RJ, Dole SA, Cognato AI (2006) Review of American Xyleborina (Coleoptera: Curculionidae: Scolytinae) occurring north of Mexico, an illustrated key. Ann Entomol Soc Am 99:1034–1056

    Article  Google Scholar 

  67. Rassati D, Faccoli M, Haack RA, Rabaglia RJ, Toffolo EP, Battisti A, Marini L (2016) Bark and ambrosia beetles show different invasions patterns in the USA. PLoS ONE 11(7):e0158519

    Article  PubMed  PubMed Central  Google Scholar 

  68. Robertson JL, Wyatt R (1990) Evidence for pollination ecotypes in the yellow-fringed orchid, Platanthera ciliaris. Evolution 44:121–133

    Article  PubMed  Google Scholar 

  69. Rodgers L, Derksen A, Pernas T (2014) Expansion and impact of laurel wilt in the Florida Everglades. Fla Entomol 97:1247–1250

    Article  Google Scholar 

  70. Roman J, Darling J (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    Article  PubMed  Google Scholar 

  71. Rossetto M, McNally J, Henry RJ (2002) Evaluating the potential of ssr flaking regions for examining taxonomic relationships in the Vitaceae. Theor Appl Genet 104:61–66

    CAS  Article  PubMed  Google Scholar 

  72. Scott CT, Bechtold WA, Reams GA, Smith WD, Westfall JA, Hansen MH, Moisen GG (2005) Sample-based estimators used by the Forest Inventory and Analysis national information management system. In: Bechtold WA, Patterson PL (eds) The enhanced Forest Inventory and Analysis program—national sampling design and estimation procedures. General Technical Report SRS-80. USDA, Forest Service, Southern Research Station. http://www.srs.fs.usda.gov/pubs/gtr/gtr_srs080/gtr_srs080.pdf. Accessed 17 Jan 2017

  73. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629

    Article  PubMed  Google Scholar 

  74. Shaw JD, Steed BE, DeBlander LT (2005) Forest Inventory and Analysis (FIA) annual inventory answers the question: what is happening to pinyon-juniper woodlands? J For 103:280–285

    Google Scholar 

  75. Shearman TM, Wang GG, Bridges WC (2015) Population dynamics of redbay (Persea borbonia) after laurel wilt disease: an assessment based on forest inventory and analysis data. Biol Invasions 17:1371–1382

    Article  Google Scholar 

  76. Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919

    Article  PubMed  Google Scholar 

  77. Smith JA, Mount L, Mayfield AE III, Bates BA, Lamborn WA, Fraedrich SW (2009) First report of laurel wilt disease caused by Raffaelea lauricola on camphor in Florida and Georgia. Plant Dis 93:198

    Article  Google Scholar 

  78. Smith JA, O’Donnell K, Mount LL, Peacock K, Trulock A, Spector T, Cruse-Sanders J, Determann R (2011) A novel Fusarium species causes a canker disease of the critically endangered conifer, Torreya taxifolia. Plant Dis 95:633–639

    Article  Google Scholar 

  79. Spiegel KS, Leege LM (2013) Impacts of laurel wilt disease on redbay (Persea borbonia (L.) Spreng.) population structure and forest communities in the coastal plain of Georgia, USA. Biol Invasions 15:2467–2487

    Article  Google Scholar 

  80. Trumbore S, Brando P, Hartmann H (2015) Forest health and global change. Science 349:814–818

    CAS  Article  PubMed  Google Scholar 

  81. Vose JM, Wear DN, Mayfield AE III, Nelson CD (2013) Hemlock wooly adelgid in the southern Appalachians: control strategies, ecological impacts, and potential management response. For Eco Manag 291:209–219

    Article  Google Scholar 

  82. Wingfield MJ, Garnas JR, Hajek A, Hurley BP, de Beer ZW, Taerum SJ (2016) Novel and co-evolved associations between insects and microorganisms as drivers of forest pestilence. Biol Invasions 18:1045–1056

    Article  Google Scholar 

  83. Wuest CE, Harrington TC, Fraedrich SW, Yun H-Y, Lu S-S (2017) Genetic variation in native populations of the laurel wilt pathogen, Raffaelea lauricola, in Taiwan and Japan and the introduced population in the United States. Plant Dis 101:619–628

    Article  Google Scholar 

Download references

Acknowledgements

We thank John Coulston (USDA Forest Service) and Bill Smith (USDA Forest Service, ret.) for assistance with FIA data analyses, Stephen Fraedrich (USDA Forest Service) for donating fungal isolates, Kathy Smith (USDA Forest Service) for assistance with molecular techniques, and our three anonymous pre-submission manuscript reviewers. Funding was provided by the USDA Forest Service Region 8 Forest Health Protection and STDP programs.

Author information

Affiliations

Authors

Corresponding author

Correspondence to M. A. Hughes.

Additional information

M. A. Hughes and J. J. Riggins have contributed equally to this manuscript.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 20 kb)

Supplementary material 2 (DOCX 15 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hughes, M.A., Riggins, J.J., Koch, F.H. et al. No rest for the laurels: symbiotic invaders cause unprecedented damage to southern USA forests. Biol Invasions 19, 2143–2157 (2017). https://doi.org/10.1007/s10530-017-1427-z

Download citation

Keywords

  • Laurel wilt
  • Redbay ambrosia beetle
  • Xyleborus glabratus
  • Raffaelea lauricola
  • Persea borbonia
  • Invasive species
  • Forest disease
  • Forest Inventory and Analysis