Biological Invasions

, Volume 20, Issue 8, pp 1991–2003 | Cite as

Biotic resistance and the spatiotemporal distribution of an invading woodwasp, Sirex noctilio

  • Christopher J. FoelkerEmail author
  • Dylan Parry
  • Melissa K. Fierke
Original Paper


Quantifying the strength of interactions among introduced and native species across space and time is critical in understanding biological invasions as they can attenuate or amplify the magnitude of impact. The European woodwasp, Sirex noctilio F., a global threat to pines, is a recent invader to North America. It attacks and kills primarily Pinus resinosa and Pinus sylvestris, and encounters a diverse assemblage of potential competitors for this resource. We quantified spatial colonization patterns of this woodwasp and resident competitors including scolytine bark beetles, woodboring cerambycid and buprestid beetles, and the fungal root rot diseases Armillaria and Heterobasidion across an 80 year old pine plantation over 4 years. All xylophages were spatially aggregated, but only on a localized scale of 15–20 m. Colonizers occurred non-randomly within trees, with S. noctilio negatively or neutrally associated with all other colonizing agents, whereas all other insect and root rot colonizers were mostly positively co-associated. An autologistic regression with spatially-weighted variables indicated the probability of a dead tree exhibiting symptoms of S. noctilio attack was positively associated with tree density, host species (P. sylvestris), and density of S. noctilio-attacked trees from the current and previous year. Interspecific stand patterns were weaker; probability of attack was negatively associated only with root rot pathogens. Across spatial scales, there were mixed (woodborers) and neutral (bark beetles) associations between S. noctilio and other co-colonizing insects. Our results suggest that competitive interactions with resident species may be contributing to the limited success of S. noctilio in North America, but are unlikely to be driving it by themselves.


Aggregation Auto- and cross-correlation Autologistic regression Non native insect Pinus 



We thank Michael Parisio for field assistance. Bruce Breitmeyer and Chris Nowak provided important logistical support and insight on the history of Pack Demonstration Forest. We thank the NY Department of Environmental Conservation for providing a field vehicle. Comments by Patrick Tobin and an anonymous reviewer greatly improved the quality of this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Aukema BH, Richards GR, Krauth SJ, Raffa KF (2004) Species assemblage arriving at and emerging from trees colonized by Ips pini in the Great Lakes region: partitioning by time since colonization, season, and host species. Ann Entomol Soc Am 97:117–129.[0117:SAAAAE]2.0.CO;2CrossRefGoogle Scholar
  2. Aukema BH, Zhu J, Møller J et al (2010) Predisposition to bark beetle attack by root herbivores and associated pathogens: roles in forest decline, gap formation, and persistence of endemic bark beetle populations. For Ecol Manage 259:374–382. CrossRefGoogle Scholar
  3. Ayres BD, Ayres MP, Abrahamson MD, Teale SA (2001) Resource partitioning and overlap in three sympatric species of Ips bark beetles (Coleoptera: Scolytidae). Oecologia 128:443–453. CrossRefPubMedGoogle Scholar
  4. Ayres MP, Pena R, Lombardo JA, Lombardero MJ (2014) Host use patterns by the European woodwasp, Sirex noctilio, in its native and invaded range. PLoS ONE 9:e90321. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Barbosa P, Cranshaw W, Greenblatt JA (1981) Influence of food quantity and quality on polymorphic dispersal behaviors in the gypsy moth, Lymantria dispar. Can J Zool 59:293–296. CrossRefGoogle Scholar
  6. Bendel M, Rigling D (2008) Signs and symptoms associated with Heterobasidion annosum and Armillaria ostoyae infection in dead and dying mountain pine (Pinus mugo ssp. uncinata). For Pathol 38:61–72. CrossRefGoogle Scholar
  7. Bjørnstad ON, Falck W (2001) Nonparametric spatial covariance functions: estimation and testing. Environ Ecol Stat 8:53–70. CrossRefGoogle Scholar
  8. Böröczky K, Zylstra KE, McCartney NB et al (2012) Volatile profile differences and the associated Sirex noctilio activity in two host tree species in the northeastern United States. J Chem Ecol 38:213–221. CrossRefPubMedGoogle Scholar
  9. Buchner P (1965) Endosymbiosis of animals with plant microorganims. Wiley, HobokenGoogle Scholar
  10. Buxbaum CA, Nowak CA, White EH (2005) Deep subsoil nutrient uptake in potassium-deficient, aggrading Pinus resinosa plantation. Can J For Res 35:1978–1983. CrossRefGoogle Scholar
  11. Capinera JL, Barbosa P (1976) Dispersal of first-instar gypsy moth larvae in relation to population quality. Oecologia 26:53–60. CrossRefPubMedGoogle Scholar
  12. Carlsson NO, Sarnelle O, Strayer DL (2009) Native predators and exotic prey—an acquired taste? Front Ecol Environ 7:525–532. CrossRefGoogle Scholar
  13. Chrystal RN, Myers JG (1928) The Sirex woodwasps and their parasites. Emp For J 7:145–154Google Scholar
  14. Clarke CW, Carnegie AJ, Yousuf F et al (2016) Minimizing the disruptive effect of Ips grandicollis (Coleoptera: Scolytinae) on biocontrol of Sirex noctilio (Hymenoptera: Siricidae). For Ecol Manage 381:134–143. CrossRefGoogle Scholar
  15. Corley JC, Villacide JM (2012) Population dynamics of Sirex noctilio: influence of diapause, spatial aggregation and flight potential on outbreaks and spread. In: Slippers B, de Groot P, Wingfield MJ (eds) The Sirex woodwasp and its fungal symbiont. Springer, Dordrecht, pp 51–64CrossRefGoogle Scholar
  16. Corley JC, Villacide JM, Bruzzone OA (2007) Spatial dynamics of a Sirex noctilio woodwasp population within a pine plantation in Patagonia, Argentina. Entomol Exp Appl 125:231–236. CrossRefGoogle Scholar
  17. Coulson RN, Mayyasi AM, Foltz JL, Hain FP (1976) Interspecific competition between Monochamus titillator and Dendroctonus frontalis. Environ Entomol 5:235–247. CrossRefGoogle Scholar
  18. Coutts MP (1969a) The mechanism of pathogenicity of Sirex noctilio on Pinus radiata L. effects of the symbiotic fungus Amylostereum sp. (Thelophoraceae). Aust J Biol Sci 22:915–924CrossRefGoogle Scholar
  19. Coutts MP (1969b) The mechanism of pathogenicity of Sirex noctilio on Pinus radiata II. Effects of S. noctilio mucus. Aust J Biol Sci 22:1153–1162Google Scholar
  20. Cronin JT, Reeve JD, Wilkens R, Turchin P (2000) The pattern and range of movement of a checkered beetle predator relative to its bark beetle prey. Oikos 90:127–138CrossRefGoogle Scholar
  21. Davis TS, Hofstetter RW (2009) Effects of gallery density and species ratio on the fitness and fecundity of two sympatric bark beetles (Coleoptera: Curculionidae). Environ Entomol 38:639–650. CrossRefPubMedGoogle Scholar
  22. Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331. CrossRefGoogle Scholar
  23. Denno RF, Peterson MA, Gratton C et al (2000) Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores. Ecology 81:1814–1827CrossRefGoogle Scholar
  24. Dodds KJ, de Groot P (2012) Sirex, surveys and management: challenges of having Sirex noctilio in North America. In: Slippers B, de Groot P, Wingfield MJ (eds) The Sirex woodwasp and its fungal symbiont. Springer, Dordrecht, pp 265–286CrossRefGoogle Scholar
  25. Dodds KJ, Graber C, Stephen FM (2001) Facultative intraguild predation by larval Cerambycidae (Coleoptera) on bark beetle larvae (Coleoptera: Scolytidae). Environ Entomol 30:17–22. CrossRefGoogle Scholar
  26. Dodds KJ, de Groot P, Orwig DA (2010) The impact of Sirex noctilio in Pinus resinosa and Pinus sylvestris stands in New York and Ontario. Can J For Res 40:212–223. CrossRefGoogle Scholar
  27. Dodds KJ, Zylstra KE, Dubois GD, Hoebeke ER (2012) Arboreal insects associated with herbicide-stressed Pinus resinosa and Pinus sylvestris used as Sirex noctilio trap trees in New York. Environ Entomol 41:1350–1363. CrossRefPubMedGoogle Scholar
  28. Dunning JB, Danielson BJ, Pulliam HR (1992) Ecological processes that affect populations in complex landscapes. Oikos 65:169–175. CrossRefGoogle Scholar
  29. Eager PT, Allen DC, Frair JL, Fierke MK (2011) Within-tree distributions of the Sirex noctilio Fabricius (Hymenoptera: Siricidae)—parasitoid complex and development of an optimal sampling scheme. Environ Entomol 40:1266–1275. CrossRefPubMedGoogle Scholar
  30. Elton CS (1958) The ecology of invasions by animals and plants. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  31. Erbilgin N, Raffa KF (2000) Effects of host tree species on attractiveness of tunneling pine engravers, Ips pini, to conspecifics and insect predators. J Chem Ecol 26:823–840. CrossRefGoogle Scholar
  32. Erbilgin N, Raffa KF (2002) Association of declining red pine stands with reduced populations of bark beetle predators, seasonal increases in root colonizing insects, and incidence of root pathogens. For Ecol Manage 164:221–236. CrossRefGoogle Scholar
  33. Erbilgin N, Nordheim EV, Aukema BH, Raffa KF (2002) Population dynamics of Ips pini and Ips grandicollis in red pine plantations in Wisconsin: within- and between-year associations with predators, competitors, and habitat quality. Environ Entomol 31:1043–1051. CrossRefGoogle Scholar
  34. Foelker CJ (2016) Beneath the bark: associations among Sirex noctilio development, bluestain fungi, and pine host species in North America. Ecol Entomol 41:676–684. CrossRefGoogle Scholar
  35. Foelker CJ, Standley CR, Fierke MK et al (2016a) Host tissue identification for cryptic hymenopteran parasitoids associated with Sirex noctilio. Agric For Entomol 18:91–94. CrossRefGoogle Scholar
  36. Foelker CJ, Standley CR, Parry D, Fierke MK (2016b) Complex ecological relationships among an assemblage of indigenous hymenopteran parasitoids, the exotic European woodwasp (Sirex noctilio; Hymenoptera: Siricidae), and a native congener. Can Entomol 148:532–542CrossRefGoogle Scholar
  37. Francke-Grosman H (1939) On the symbiosis of woodwasps (Siricinae) with fungi. Z Angew Entomol 25:647–679CrossRefGoogle Scholar
  38. Fukuda H, Hijii N (1996) Host-tree conditions affecting the oviposition activities of the woodwasp, Sirex nitobei Matsumura (Hymenoptera: Siricidae). J For Res 1:177–181CrossRefGoogle Scholar
  39. Garbelotto M, Gonthier P (2013) Biology, epidemiology, and control of Heterobasidion species worldwide. Annu Rev Phytopathol 51:39–59CrossRefPubMedGoogle Scholar
  40. Gelman A (2008) Scaling regression inputs by dividing by two standard deviations. Stat Med 27:2865–2873CrossRefPubMedGoogle Scholar
  41. Graham SA (1925) The felled tree trunk as an ecological unit. Ecology 6:397–411. CrossRefGoogle Scholar
  42. Haavik LJ, Dodds KJ, Allison JD (2015) Do native insects and associated fungi limit non-native woodwasp, Sirex noctilio, survival in a newly invaded environment? PLoS ONE 10:e0138516. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Haavik LJ, Dodds KJ, Ryan K, Allison JD (2016) Evidence that the availability of suitable pine limits non-native Sirex noctilio in Ontario. Agric For Entomol 18:357–366. CrossRefGoogle Scholar
  44. Hanson HS (1939) Ecological notes on the Sirex wood wasps and their parasites. Bull Entomol Res 30:27–65CrossRefGoogle Scholar
  45. Hayes RA, Griffiths MW, Nahrung HF (2015) Electrophysiological activity of the Sirex noctilio ovipositor: you know the drill? J Asia-Pac Entomol 8:165–168. CrossRefGoogle Scholar
  46. Hoebeke ER, Haugen DA, Haack RA (2005) Sirex noctilio: discovery of a Palearctic siricid woodwasp in New York. Newsl Mich Entomol Soc 50:24–25Google Scholar
  47. Hofstetter RW, Cronin JT, Klepzig KD et al (2005) Antagonisms, mutualisms and commensalisms affect outbreak dynamics of the southern pine beetle. Oecologia 147:679–691. CrossRefPubMedGoogle Scholar
  48. Hurley BP, Hatting HJ, Wingfield MJ et al (2012) The influence of Amylostereum areolatum diversity and competitive interactions on the fitness of the Sirex parasitic nematode Deladenus siricidicola. Biol Control 61:207–214. CrossRefGoogle Scholar
  49. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. CrossRefGoogle Scholar
  50. Lantschner MV, Corley JC (2015) Spatial pattern of attacks of the invasive woodwasp Sirex noctilio, at landscape and stand scales. PLoS ONE 10:e0127099. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Levin SA (1992) The problem of pattern and scale in ecology: the Robert H. MacArthur award lecture. Ecology 73:1943–1967CrossRefGoogle Scholar
  52. Light DM, Birch MC, Paine TD (1983) Laboratory study of intraspecific and interspecific competition within and between two sympatric bark beetle species, Ips pini and I. paraconfusus. Z Für Angew Entomol 96:233–241. CrossRefGoogle Scholar
  53. Long SJ, Williams DW, Hajek AE (2009) Sirex species (Hymenoptera: Siricidae) and their parasitoids in Pinus sylvestris in eastern North America. Can Entomol 141:153–157. CrossRefGoogle Scholar
  54. Madden JL (1988) Sirex in Australia. In: Berryman AA (ed) Dynamics of forest insect populations. Springer, New York, pp 407–429CrossRefGoogle Scholar
  55. McClure MS (1984) Influence of cohabitation and resinosis on site selection and survival of Pineus boerneri Annand and P. coloradensis (Gillette) (Homoptera: Adelgidae) on red pine. Environ Entomol 13:657–663CrossRefGoogle Scholar
  56. Miller MC (1986) Within-tree effects of bark beetle insect associates on the emergence of Ips calligraphus (Coleoptera: Scolytidae). Environ Entomol 15:1104–1108. CrossRefGoogle Scholar
  57. Nielson RM, Sugihara RT, Boardman TJ, Engeman RM (2004) Optimization of ordered distance sampling. Environmetrics 15:119–128. CrossRefGoogle Scholar
  58. Niemelä P, Mattson WJ (1996) Invasion of North American forests by European phytophagous insects. Bioscience 46:741–753. CrossRefGoogle Scholar
  59. Omdal DW, Shaw CG III, Jacobi WR (2004) Symptom expression in conifers infected with Armillaria ostoyae and Heterobasidion annosum. Can J For Res 34:1210–1219. CrossRefGoogle Scholar
  60. Paine TD, Birch MC, Švihra P (1981) Niche breadth and resource partitioning by four sympatric species of bark beetles (Coleoptera: Scolytidae). Oecologia 48:1–6CrossRefPubMedGoogle Scholar
  61. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967CrossRefGoogle Scholar
  62. Parkin EA (1941) Symbiosis in larval Siricidæ (Hymenoptera). Nature 147:329. CrossRefGoogle Scholar
  63. Parkin EA (1942) Symbiosis and siricid woodwasps. Ann Appl Biol 29:268–274. CrossRefGoogle Scholar
  64. Price PW, Bouton CE, Gross P et al (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65CrossRefGoogle Scholar
  65. Price PW, Westoby M, Rice B et al (1986) Parasite mediation in ecological interactions. Annu Rev Ecol Syst 17:487–505CrossRefGoogle Scholar
  66. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  67. Raffa KF, Berryman AA (1980) Flight responses and host selection by bark beetles. In: Proceedings of the second IUFRO conference on dispersal of forest insects: evaluation, theory, and management implications. Conference Office, Cooperative Extension Service, Washington State University, Pullman Washington, pp 213–233Google Scholar
  68. Rankin LJ, Borden JH (1991) Competitive interactions between the mountain pine beetle and the pine engraver in lodgepole pine. Can J For Res 21:1029–1036. CrossRefGoogle Scholar
  69. Ripley BD (1976) The second-order analysis of stationary point processes. J Appl Probab 13:255–266. CrossRefGoogle Scholar
  70. Ross-Davis AL, Hanna JW, Kim M-S, Klopfenstein NB (2011) Advances toward DNA-based identification and phylogeny of North American Armillaria species using elongation factor-1 alpha gene. Mycoscience 53:161–165. CrossRefGoogle Scholar
  71. Ryan K, Moncalvo J-M, de Groot P, Smith SM (2011) Interactions between the fungal symbiont of Sirex noctilio (Hymenoptera: Siricidae) and two bark beetle-vectored fungi. Can Entomol 143:224–235. CrossRefGoogle Scholar
  72. Ryan K, de Groot P, Davis C, Smith SM (2012a) Effect of two bark beetle-vectored fungi on the on-host search and oviposition behavior of the introduced woodwasp Sirex noctilio (Hymenoptera: Siricidae) on Pinus sylvestris trees and logs. J Insect Behav 25:453–466. CrossRefGoogle Scholar
  73. Ryan K, De Groot P, Nott RW et al (2012b) Natural enemies associated with Sirex noctilio (Hymenoptera: Siricidae) and S. nigricornis in Ontario, Canada. Environ Entomol 41:289–297. CrossRefPubMedGoogle Scholar
  74. Ryan K, de Groot P, Smith SM (2012c) Evidence of interaction between Sirex noctilio and other species inhabiting the bole of Pinus. Agric For Entomol 14:187–195. CrossRefGoogle Scholar
  75. Safranyik L, Linton DA, Silversides R, McMullen LH (1992) Dispersal of released mountain pine beetles under the canopy of a mature lodgepole pine stand. J Appl Entomol 113:441–450. CrossRefGoogle Scholar
  76. Savely HE (1939) Ecological relations of certain animals in dead pine and oak logs. Ecol Monogr 9:321–385. CrossRefGoogle Scholar
  77. Schlyter F, Anderbrant O (1993) Competition and niche separation between two bark beetles: existence and mechanisms. Oikos 68:437–447. CrossRefGoogle Scholar
  78. Schroeder LM, Weslien J (1994) Reduced offspring production in bark beetle Tomicus piniperda in pine bolts baited with ethanol and α-pinene, which attract antagonistic insects. J Chem Ecol 20:1429–1444. CrossRefPubMedGoogle Scholar
  79. Slippers B, Hurley BP, Wingfield MJ (2015) Sirex woodwasp: a model for evolving management paradigms of invasive forest pests. Annu Rev Entomol 60:601–619. CrossRefPubMedGoogle Scholar
  80. Smith MT, Bancroft J, Li G et al (2001) Dispersal of Anoplophora glabripennis (Cerambycidae). Environ Entomol 30:1036–1040CrossRefGoogle Scholar
  81. Spradbery JP, Kirk AA (1978) Aspects of the ecology of siricid woodwasps (Hymenoptera: Siricidae) in Europe, North Africa and Turkey with special reference to the biological control of Sirex noctilio F. in Australia. Bull Entomol Res 68:341–359. CrossRefGoogle Scholar
  82. Standley CR, Hoebeke ER, Parry D et al (2012) Detection and identification of two new native hymenopteran parasitoids associated with the exotic Sirex noctilio in North America. Proc Entomol Soc Wash 114:238–249. CrossRefGoogle Scholar
  83. Thompson BM (2013) Community ecology and Sirex noctilio: interactions with microbial symbionts and native insects. Ph.D. dissertation, Department of Entomology, The University of Maryland, College Park, MD, USAGoogle Scholar
  84. Thompson BM, Grebenok RJ, Behmer ST, Gruner DS (2012) Microbial symbionts shape the sterol profile of the xylem-feeding woodwasp, Sirex noctilio. J Chem Ecol 39:129–139. CrossRefPubMedGoogle Scholar
  85. Thoss V, O’Reilly-Wapstra J, Iason GR (2007) Assessment and implications of intraspecific and phenological variability in monoterpenes of Scots pine (Pinus sylvestris) foliage. J Chem Ecol 33:477–491. CrossRefPubMedGoogle Scholar
  86. Tribe GD, Cillié JJ (2004) The spread of Sirex noctilio Fabricius (Hymenoptera: Siricidae) in South African pine plantations and the introduction and establishment of its biological control agents. Afr Entomol 12:9–17Google Scholar
  87. Turchin P, Thoeny WT (1993) Quantifying dispersal of southern pine beetles with mark-recapture experiments and a diffusion model. Ecol Appl 3:187–198CrossRefPubMedGoogle Scholar
  88. Villacide JM, Corley JC (2008) Parasitism and dispersal potential of Sirex noctilio: implications for biological control. Agric For Entomol 10:341–345. CrossRefGoogle Scholar
  89. Woodard S, Stenlid J, Karjalainen R, Hüttermann A (1998) Heterobasidion annosum: biology, ecology, impact and control. CAB International, WallingfordGoogle Scholar
  90. Yousuf F, Carnegie AJ, Bashford R et al (2014a) Bark beetle (Ips grandicollis) disruption of woodwasp (Sirex noctilio) biocontrol: direct and indirect mechanisms. For Ecol Manage 323:98–104. CrossRefGoogle Scholar
  91. Yousuf F, Gurr GM, Carnegie AJ et al (2014b) The bark beetle, Ips grandicollis, disrupts biological control of the woodwasp, Sirex noctilio, via fungal symbiont interactions. FEMS Microbiol Ecol 88:38–47. CrossRefPubMedGoogle Scholar
  92. Zylstra KE, Dodds KJ, Francese JA, Mastro V (2010) Sirex noctilio in North America: the effect of stem-injection timing on the attractiveness and suitability of trap trees. Agric For Entomol 12:243–250. CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Christopher J. Foelker
    • 1
    • 2
    Email author
  • Dylan Parry
    • 1
  • Melissa K. Fierke
    • 1
  1. 1.Department of Environmental and Forest BiologyState University of New York-College of Environmental Science and ForestrySyracuseUSA
  2. 2.Wisconsin Department of Agriculture, Trade and Consumer ProtectionMadisonUSA

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