Toxicity of Monoterpene Structure, Diversity and Concentration to Mountain Pine Beetles, Dendroctonus ponderosae: Beetle Traits Matter More

Abstract

A high diversity of plant defenses may be a response to herbivore diversity or may be collectively more toxic than single compounds, either of which may be important for understanding insect-plant associations. Monoterpenes in conifers are particularly diverse. We tested the fumigant toxicity of four monoterpenes, alone and in combination, to mountain pine beetles, Dendroctonus ponderosae, in the context of the beetles' individual body traits. Chemical structures of tested monoterpene hydrocarbons had modest effects on beetle survival, mass loss, water content and fat content, with (R)-(+)-limonene tending to be more toxic than (−)-α-pinene, (−)-β-pinene, and (+)-3-carene. Monoterpene diversity (all qualitative combinations of one to four monoterpenes) did not affect toxicity. Concentration (0 to 1200 ppm) of individual monoterpenes was a strong determinant of toxicity. Beetle body size and body condition index strongly and positively affected survival during monoterpene treatments. Larger beetles in better condition lost proportionally less mass during exposure, where proportion mass loss negatively affected survivorship. Toxicity was much more associated with water loss than with fat loss, suggesting that a main cost of detoxification is excretion, a process that has received little attention. These results provide insight into the determinants of beetle success in historic and novel hosts that differ in monoterpene composition and concentration. We also suggest that water availability will affect beetle success directly through their ability to tolerate detoxification as well as indirectly through host responses to drought.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Adams AS, Boone CK, Bohlmann J, Raffa KF (2011) Responses of bark beetle-associated bacteria to host monoterpenes and their relationship to insect life histories. J Chem Ecol 37:808–817

    CAS  Article  PubMed  Google Scholar 

  2. Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432

    Article  Google Scholar 

  3. Allen CD et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684

    Article  Google Scholar 

  4. Appel HM, Martin MM (1992) Significance of metabolic load in the evolution of host specificity of Manduca sexta. Ecology 73:216–228

    Article  Google Scholar 

  5. Bentz BJ et al (2010) Climate change and bark beetles of the western United States and Canada: direct and indirect effects. Bioscience 60:602–613

    Article  Google Scholar 

  6. Bentz BJ, Boone C, Raffa KF (2015) Tree response and mountain pine beetle attack preference, reproduction and emergence timing in mixed whitebark and lodgepole pine stands. Agric For Entomol 17:421–432

    Article  Google Scholar 

  7. Berenbaum MR (1995) The chemistry of defense: theory and practice. Proc Natl Acad Sci 92:2–8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Berenbaum MR, Nitao JK, Zangerl AR (1991) Adaptive significance of furanocoumarin diversity in Pastinaca sativa (Apiaceae). J Chem Ecol 17:207–215

    CAS  Article  PubMed  Google Scholar 

  9. Boone CK, Aukema BH, Bohlmann J, Carroll AL, Raffa KF (2011) Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species. Can J For Res/Rev Can Rech For 41:1174–1188

    Article  Google Scholar 

  10. Boone CK, Keefover-Ring K, Mapes AC, Adams AS, Bohlmann J, Raffa KF (2013) Bacteria associated with a tree-killing insect reduce concentrations of plant defense compounds. J Chem Ecol 39:1003–1006

    CAS  Article  PubMed  Google Scholar 

  11. Burke JL, Carroll AL (2016) The influence of variation in host tree monoterpene composition on secondary attraction by an invasive bark beetle: implications for range expansion and potential host shift by the mountain pine beetle. For Ecol Manag 359:59–64

    Article  Google Scholar 

  12. Byers JA (1995) Host-tree chemistry affecting colonization in bark beetles. In: Cardé RT, Bell WJ (eds) Chemical ecology of insects, 2nd edn. Chapman and Hall, New York, pp 156–213

    Google Scholar 

  13. Calow P (1990) A physiological basis of population processes: ecotoxicological implications. Funct Ecol 4:283–288

    Article  Google Scholar 

  14. Cano-Ramirez C, Lopez MF, Cesar-Ayala AK, Pineda-Martinez V, Sullivan BT, Zuniga G (2013) Isolation and expression of cytochrome P450 genes in the antennae and gut of pine beetle Dendroctonus rhizophagus (Curculionidae: Scolytinae) following exposure to host monoterpenes. Gene 520:47–63

    CAS  Article  PubMed  Google Scholar 

  15. Carmona D, Lajeunesse MJ, Johnson MTJ (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367

    Article  Google Scholar 

  16. Castañeda LE et al (2011) Evaluating reproductive fitness and metabolic costs for insecticide resistance in Myzus persicae from Chile. Physiol Entomol 36:253–260

    Article  Google Scholar 

  17. Cates RG (1996) The role of mixtures and variation in the production of terpenoids in conifer-insect-pathogen interactions. In: Romeo JT, Saunders JA, Barbosa P (eds) Phytochemical diversity and redundancy in ecological interactions, vol 30. Plenum Press, New York, pp 179–216

    Google Scholar 

  18. Cerezke HF (1995) Egg gallery, brood production, and adult characteristics of mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae), in three pine hosts. Can Entomol 127:955–965

    Article  Google Scholar 

  19. Chown SL (2002) Respiratory water loss in insects. Comp Biochem Physiol A 133:791–804

    CAS  Article  Google Scholar 

  20. Chown SL, Sorensen JG, Terblanche JS (2011) Water loss in insects: an environmental change perspective. J Insect Physiol 57:1070–1084

    CAS  Article  PubMed  Google Scholar 

  21. Clark EL, Pitt C, Carroll AL, Lindgren BS, Huber DP (2014) Comparison of lodgepole and jack pine resin chemistry: implications for range expansion by the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae). PeerJ 2:e240

    Article  PubMed  PubMed Central  Google Scholar 

  22. Cook SP, Hain FP (1988) Toxicity of host monoterpenes to Dendroctonus frontalis and Ips calligraphus (Coleoptera: Scolytidae). J Entomol Sci 23:287–292

    CAS  Google Scholar 

  23. Dai L, Ma M, Wang C, Shi Q, Zhang R, Chen H (2015) Cytochrome P450s from the Chinese white pine beetle, Dendroctonus armandi (Curculionidae: Scolytinae): expression profiles of different stages and responses to host allelochemicals. Insect Biochem Mol Biol 65:35–46

    CAS  Article  PubMed  Google Scholar 

  24. David J-P, Boyer S, Mesneau A, Ball A, Ranson H, Dauphin-Villemant C (2006) Involvement of cytochrome P450 monooxygenases in the response of mosquito larvae to dietary plant xenobiotics. Insect Biochem Mol Biol 36:410–420

    CAS  Article  PubMed  Google Scholar 

  25. Elkin CM, Reid ML (2005) Low energy reserves and energy allocation decisions affect reproduction by mountain pine beetles (Dendroctonus ponderosae). Funct Ecol 19:102–109

    Article  Google Scholar 

  26. Elkin CM, Reid ML (2010) Shifts in breeding habitat selection behaviour in response to population density. Oikos 119:1070–1080

    Article  Google Scholar 

  27. Erbilgin N, Colgan LJ (2012) Differential effects of plant ontogeny and damage type on phloem and foliage monoterpenes in jack pine (Pinus banksiana). Tree Physiol 32:946–957

    CAS  Article  PubMed  Google Scholar 

  28. Erbilgin N, Ma C, Whitehouse C, Shan B, Najar A, Evenden M (2013) Chemical similarity between historical and novel host plants promotes range and host expansion of the mountain pine beetle in a naive host ecosystem. New Phytol 201:940–950

    Article  PubMed  Google Scholar 

  29. Evenden ML, Whitehouse CM, Sykes J (2014) Factors influencing flight capacity of the mountain pine beetle (Coleoptera: Curculionidae: Scolytinae). Environ Entomol 43:187–196

    CAS  Article  PubMed  Google Scholar 

  30. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414

    CAS  Article  PubMed  Google Scholar 

  31. Gershenzon J, Fontana A, Burow M, Wittstock U, Degenhardt J (2012) Mixtures of plant secondary metabolites: metabolic origins and ecological benefits. In: Iason GR, Dicke M, Hartley S (eds) The ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, Cambridge, pp 56–77

    Google Scholar 

  32. Geyer HJ, Scheunert I, Rapp K, Gebefugi I, Steinberg C, Kettrup A (1993) The relevance of fat content in toxicity of lipophilic chemicals to terrestrial animals with special reference to dieldrin and 2,3,7,8-tetrachlorodibeno-p-dioxin (TCDD). Ecotoxicol Environ Saf 26:45–60

    CAS  Article  PubMed  Google Scholar 

  33. Gibbs AG (2003) Evolution of water conservation mechanisms in Drosophila. J Exp Biol 206:1183–1192

    Article  PubMed  Google Scholar 

  34. Gray CA, Runyon JB, Jenkins MJ, Giunta AD (2015) Mountain pine beetles use volatile cues to locate host limber pine and avoid non-host Great Basin bristlecone pine. PLoS One 10:e0135752

    Article  PubMed  PubMed Central  Google Scholar 

  35. Holmstrup M et al (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762

    CAS  Article  PubMed  Google Scholar 

  36. Iason GR, O'Reilly-Wapstra JM, Brewer MJ, Summers RW, Moore BD (2011) Do multiple herbivores maintain chemical diversity of scots pine monoterpenes? Philos Trans R Soc Lond Ser B Biol Sci 366:1337–1345

    Article  Google Scholar 

  37. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  38. Karise R, Mänd M (2015) Recent insights into sublethal effects of pesticides on insect respiratory physiology. Open Access Insect Physiology 31

  39. Keeling CI (2016) Bark beetle research in the postgenomic era. In: Tittiger C, Blomquist GJ (eds) Advances in insect physiology: pine bark beetles, vol 50. Elsevier Ltd, London, pp 265–293

    Google Scholar 

  40. Keeling CI, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:657–675

    CAS  Article  PubMed  Google Scholar 

  41. Larsen EH, Deaton LE, Onken H, O’Donnell M, Grosell M, Dantzler WH, Weihrauch D (2014) Osmoregulation and excretion. Comprehensive Physiology 4:405–573

    Article  PubMed  Google Scholar 

  42. Latty TM, Reid ML (2010) Who goes first? Condition and danger dependent pioneering in a group-living beetle (Dendroctonus ponderosae). Behav Ecol Sociobiol 64:639–646

    Article  Google Scholar 

  43. Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–353

    Article  PubMed  Google Scholar 

  44. Lopez MF, Cano-Ramirez C, Cesar-Ayala AK, Ruiz EA, Zuniga G (2013) Diversity and expression of P450 genes from Dendroctonus valens LeConte (Curculionidae: Scolytinae) in response to different kairomones. Insect Biochem Mol Biol 43:417–432

    CAS  Article  PubMed  Google Scholar 

  45. Lyon RL (1958) A useful secondary characteristic in Dendroctonus bark beetles. Can Entomol 60:582–584

    Article  Google Scholar 

  46. Manning CG, Reid ML (2013) Sub-lethal effects of monoterpenes on reproduction by mountain pine beetles. Agric For Entomol 15:262–271

    Article  Google Scholar 

  47. Marsh KJ, Wallis IR, McLean S, Sorensen JS, Foley WJ (2006) Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets. Ecology 87:2103–2112

    Article  PubMed  Google Scholar 

  48. Mason PA, Singer MS, Biere A (2015) Defensive mixology: combining acquired chemicals towards defence. Funct Ecol 29:441–450

    Article  Google Scholar 

  49. Miller DR, Borden JH (2000) Dose-dependent and species-specific responses of pine bark beetles (Coleoptera: Scolytidae) to monoterpenes in association with pheromones. Can Entomol 132:183–195

    Article  Google Scholar 

  50. Moore BD, Andrew RL, Kulheim C, Foley WJ (2013) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol 201:733–750

    Article  PubMed  Google Scholar 

  51. Newton EL, Bullock JM, Hodgson DJ (2009) Glucosinolate polymorphism in wild cabbage (Brassica oleracea) influences the structure of herbivore communities. Oecologia 160:63–76

    Article  PubMed  Google Scholar 

  52. Raffa KF, Berryman AA (1983) The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae). Ecol Monogr 53:27–49

    Article  Google Scholar 

  53. Raffa KF, Berryman AA (1987) Interacting selective pressures in conifer-bark beetle systems: a basis for reciprocal adaptations. Am Nat 129:234–262

    Article  Google Scholar 

  54. Raffa KF, Smalley EB (1995) Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle-fungal complexes. Oecologia 102:285–295

    Article  PubMed  Google Scholar 

  55. Raffa KF, Powell EN, Townsend PA (2013) Temperature-driven range expansion of an irruptive insect heightened by weakly coevolved plant defenses. Proc Natl Acad Sci 110:2193–2198

    CAS  Article  PubMed  Google Scholar 

  56. Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Annu Rev Entomol 57:405–424

    CAS  Article  PubMed  Google Scholar 

  57. Reid ML, Purcell JRC (2011) Condition-dependent tolerance of monoterpenes in an insect herbivore. Arthropod Plant Interact 5:331–337

    Article  Google Scholar 

  58. Reid TG, Reid ML (2008) Fluorescent powder marking reduces condition but not survivorship in adult mountain pine beetles. Can Entomol 140:582–588

    Article  Google Scholar 

  59. Robert JA, Pitt C, Bonnett TR, Yuen MM, Keeling CI, Bohlmann J, Huber DP (2013) Disentangling detoxification: gene expression analysis of feeding mountain pine beetle illuminates molecular-level host chemical defense detoxification mechanisms. PLoS One 8:e77777

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. Romeo JT, Saunders JA, Barbosa P (eds) (1996) Phytochemical diversity and redundancy in ecological interactions, vol 30. Recent Advances in Phytochemistry. Plenum Press, New York

    Google Scholar 

  61. Ruiz-Sanchez E, O’Donnell MJ (2015) The insect excretory system as a target for novel pest control strategies. Current Opinion Insect Sci 11:14–20

    Article  Google Scholar 

  62. Safranyik L, Carroll AL (2006) The biology and epidemiology of the mountain pine beetle in lodgepole pine forests. In: Safranyik L, Wilson B (eds) The mountain pine beetle: a synthesis of its biology and Management in Lodgepole Pine. Natural Resources Canada, Canadian Forest Service

  63. Safranyik L et al (2010) Potential for range expansion of mountain pine beetle into the boreal forest of North America. Can Entomol 142:415–442

    Article  Google Scholar 

  64. SAS Institute Inc. (2015). JMP 12.0. Cary, North Carolina

  65. Seybold SJ, Huber DPW, Lee JC, Graves AD, Bohlmann J (2006) Pine monoterpenes and pine bark beetles: a marriage of convenience for defense and chemical communication. Phytochem Rev 5:143–178

    CAS  Article  Google Scholar 

  66. Taft S, Najar A, Godbout J, Bousquet J, Erbilgin N (2015) Variations in foliar monoterpenes across the range of jack pine reveal three widespread chemotypes: implications to host expansion of invasive mountain pine beetle. Front Plant Sci 6:342

    Article  PubMed  PubMed Central  Google Scholar 

  67. Thoss V, Byers JA (2006) Monoterpene chemodiversity of ponderosa pine in relation to herbivory and bark beetle colonization. Chemecology 16:51–58

    CAS  Article  Google Scholar 

  68. Trowbridge AM (2014) Evolutionary ecology of chemically mediated plant-insect interactions. In: Monson RK (ed) Ecology and the environment, the plant sciences, vol 8. Springer, New York, pp 143–176. doi:10.1007/978-1-4614-7501-9_11

    Google Scholar 

  69. Wallin KF, Raffa KF (2000) Influences of host chemicals and internal physiology on the multiple steps of postlanding host acceptance behavior of Ips pini (Coleoptera: Scolytidae). Environ Entomol 29:442–453

    CAS  Article  Google Scholar 

  70. Wallin KF, Raffa KF (2004) Feedback between individual host selection behavior and population dynamics in an eruptive herbivore. Ecol Monogr 74:101–116

    Article  Google Scholar 

  71. Whitehead SR, Jeffrey CS, Leonard MD, Dodson CD, Dyer LA, Bowers MD (2013) Patterns of secondary metabolite allocation to fruits and seeds in Piper reticulatum. J Chem Ecol 39:1373–1384

    CAS  Article  PubMed  Google Scholar 

  72. Whitehead SR, Bowers MD, McArthur C (2014) Chemical ecology of fruit defence: synergistic and antagonistic interactions among amides from Piper. Funct Ecol 28:1094–1106

    Article  Google Scholar 

Download references

Acknowledgements

Funding for this study was provided by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to MLR. We thank H. Peralta-Vázquez, M. Fenton, T. Rajabi and J. Zawalykut for their assistance in the lab. K. Raffa, W. Francke and an anonymous reviewer provided helpful comments.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mary L. Reid.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Reid, M.L., Sekhon, J.K. & LaFramboise, L.M. Toxicity of Monoterpene Structure, Diversity and Concentration to Mountain Pine Beetles, Dendroctonus ponderosae: Beetle Traits Matter More. J Chem Ecol 43, 351–361 (2017). https://doi.org/10.1007/s10886-017-0824-1

Download citation

Keywords

  • Plant defences
  • Monoterpenes
  • Pinus
  • Scolytinae
  • Fumigant toxicity
  • Body size