The combined effects of pathogens and predators on insect outbreaks

Abstract

The economic damage caused by episodic outbreaks of forest-defoliating insects has spurred much research1, yet why such outbreaks occur remains unclear2. Theoretical biologists argue that outbreaks are driven by specialist pathogens or parasitoids, because host–pathogen and host–parasitoid models show large-amplitude, long-period cycles resembling time series of outbreaks3,4. Field biologists counter that outbreaks occur when generalist predators fail, because predation in low-density defoliator populations is usually high enough to prevent outbreaks5,6,7,8. Neither explanation is sufficient, however, because the time between outbreaks in the data is far more variable than in host–pathogen and host–parasitoid models1,2, and far shorter than in generalist-predator models9,10,11. Here we show that insect outbreaks can be explained by a model that includes both a generalist predator and a specialist pathogen. In this host–pathogen–predator model, stochasticity causes defoliator densities to fluctuate erratically between an equilibrium maintained by the predator, and cycles driven by the pathogen12,13. Outbreaks in this model occur at long but irregular intervals, matching the data. Our results suggest that explanations of insect outbreaks must go beyond classical models to consider interactions among multiple species.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Comparison of model output with data for an outbreaking insect.
Figure 2: Graphical representation of the combined model's equilibria.
Figure 3: Phase portraits of the combined model, with time proceeding anticlockwise.
Figure 4: Effects of stochasticity on time between outbreaks.

References

  1. 1

    Myers, J. H. Can a general hypothesis explain population cycles of forest Lepidoptera? Adv. Ecol. Res. 18, 179–242 (1988)

    Article  Google Scholar 

  2. 2

    Liebhold, A. & Kamata, N. Are population cycles and spatial synchrony a universal characteristic of forest insect populations? Popul. Ecol. 42, 205–209 (2000)

    Article  Google Scholar 

  3. 3

    Varley, G. C., Gradwell, G. R. & Hassell, M. P. Insect Population Ecology: An Analytical Approach 135–153 (Blackwell Scientific, Oxford, 1973)

    Google Scholar 

  4. 4

    Anderson, R. M. & May, R. M. The population-dynamics of micro-parasites and their invertebrate hosts. Phil. Trans. R. Soc. Lond. B 291, 451–524 (1981)

    ADS  Article  Google Scholar 

  5. 5

    Mason, R. R., Torgerson, T. R., Wickman, B. E. & Paul, H. G. Natural regulation of a Douglas-fir tussock moth (Lepidoptera: Lymantriidae) population in the Sierra Nevada. Environ. Entomol. 12, 587–594 (1983)

    Article  Google Scholar 

  6. 6

    Elkinton, J. S. et al. Interactions among gypsy moths, white-footed mice, and acorns. Ecology 77, 2332–2342 (1996)

    Article  Google Scholar 

  7. 7

    Parry, D., Spence, J. R. & Volney, W. J. A. Response of natural enemies to experimentally increased populations of the forest tent caterpillar, Malacosoma disstria. Ecol. Entomol. 22, 97–108 (1997)

    Article  Google Scholar 

  8. 8

    Klemola, T., Tanhuanpää, M., Korpimäki, E. & Ruohomäki, K. Specialist and generalist natural enemies as an explanation for geographical gradients in population cycles of northern herbivores. Oikos 99, 83–94 (2002)

    Article  Google Scholar 

  9. 9

    Southwood, T. R. E. & Comins, H. N. A synoptic population model. J. Anim. Ecol. 45, 949–965 (1976)

    Article  Google Scholar 

  10. 10

    May, R. M. Thresholds and breakpoints in ecosystems with a multiplicity of stable states. Nature 269, 471–477 (1977)

    ADS  Article  Google Scholar 

  11. 11

    Ludwig, D., Jones, D. D. & Holling, C. S. Qualitative analysis of insect outbreak systems: the spruce budworm and forest. J. Anim. Ecol. 47, 315–332 (1978)

    Article  Google Scholar 

  12. 12

    Rand, D. & Wilson, H. B. Chaotic stochasticity: a ubiquitous source of unpredictability in epidemics. Proc. R. Soc. Lond. B 246, 179–184 (1991)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Dennis, B., Desharnais, R. A., Cushing, J. M., Henson, S. M. & Constantino, R. F. Estimating chaos and complex dynamics in an insect population. Ecol. Monogr. 71, 277–303 (2001)

    Article  Google Scholar 

  14. 14

    Cory, J. S., Hails, R. S. & Sait, S. M. in The Baculoviruses (ed. Miller, L. K.) 301–339 (Plenum, New York, 1997)

    Google Scholar 

  15. 15

    Woods, S. & Elkinton, J. S. Bimodal patterns of mortality from nuclear polyhedrosis virus in gypsy moth (Lymantria dispar) populations. J. Invertebr. Pathol. 50, 151–157 (1987)

    Article  Google Scholar 

  16. 16

    Shepherd, R. F. Evidence of synchronized cycles in outbreak patterns of Douglas-fir tussock moth, Orgyia pseudotsugata (McDunnough) (Lepidoptera: Lymantriidae). Mem. Entomol. Soc. Can. 146, 107–121 (1988)

    Article  Google Scholar 

  17. 17

    Murray, K. D. & Elkinton, J. S. Environmental contamination of egg masses as a major component of transgenerational transmission of gypsy-moth nuclear polyhedrosis virus (LdMNPV). J. Invertebr. Pathol. 53, 324–334 (1989)

    Article  Google Scholar 

  18. 18

    Dwyer, G., Elkinton, J. S. & Buonaccorsi, J. P. Host heterogeneity in susceptibility and disease dynamics: tests of a mathematical model. Am. Nat. 150, 685–707 (1997)

    CAS  Article  Google Scholar 

  19. 19

    Dwyer, G., Dushoff, J., Elkinton, J. S. & Levin, S. A. Pathogen-driven outbreaks in forest defoliators revisited: building models from experimental data. Am. Nat. 156, 105–120 (2000)

    PubMed  Google Scholar 

  20. 20

    Hunter, A. F. in Population Dynamics: New Approaches and Synthesis (eds Cappuccino, N. & Price, P. W.) 41–64 (Academic, New York, 1995)

    Google Scholar 

  21. 21

    Gould, J. R., Elkinton, J. S. & Wallner, W. E. Density-dependent suppression of experimentally created gypsy moth Lymantria dispar (Lepidoptera: Lymantriidae) populations by natural enemies. J. Anim. Ecol. 59, 213–233 (1990)

    Article  Google Scholar 

  22. 22

    Holling, C. S. Some characteristics of simple types of predation and parasitism. Can. Entomol. 91, 293–320 (1959)

    Article  Google Scholar 

  23. 23

    Kendall, B. E. et al. Why do populations cycle? A synthesis of statistical and mechanistic modeling approaches. Ecology 80, 1789–1805 (1999)

    Article  Google Scholar 

  24. 24

    Bjornstad, O. N. Cycles and synchrony: two historical experiments and one ‘experience’. J. Anim. Ecol. 69, 869–873 (2000)

    Article  Google Scholar 

  25. 25

    Scheffer, S., Carpenter, S., Foley, J. A., Folkes, C. & Walker, B. Catastrophic shifts in ecosystems. Nature 413, 591–596 (2001)

    ADS  CAS  Article  Google Scholar 

  26. 26

    Williams, D. W. et al. Oak defoliation and population density relationships for the Gypsy Moth (Lepidoptera: Lymantriidae). J. Econ. Entomol. 84, 1508–1514 (1991)

    Article  Google Scholar 

  27. 27

    Williams, D. W. & Liebhold, A. M. Influence of weather on the synchrony of gypsy moth (Lepidoptera: Lymantriidae) outbreaks in New England. Environ. Entomol. 24, 987–995 (1995)

    Article  Google Scholar 

  28. 28

    Schwerdtfeger, R. Über die ursachen des massenwechsels der insekten. Z. Angew. Entomol. 28, 254–303 (1941)

    Article  Google Scholar 

  29. 29

    Ruohomäki, K. et al. Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice. Popul. Ecol. 42, 211–223 (2000)

    Article  Google Scholar 

  30. 30

    Liebhold, A., Kamata, N. & Jacobs, T. Cyclicity and synchrony of historical outbreaks of the beech caterpillar, Quadricalcarifera punctatella (Motschulsky) in Japan. Res. Popul. Ecol. 38, 87–94 (1996)

    Article  Google Scholar 

Download references

Acknowledgements

We thank O. Bjornstad, P. Turchin and A. Hunter for comments. G.D. and J.D. were supported by grants from the US National Science Foundation. J.D. was also supported by the Andrew W. Mellon Foundation.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Greg Dwyer.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Information 1

Results for the combined model when a term for long-term pathogen survival is added to the pathogen equation. The file includes figures showing the model's multiple equilibria and stochastically-induced complex dynamics. (PDF 112 kb)

Supplementary Information 2

Equations and results for a host-parasitoid-predator model analogous to the combined host-pathogen-predator model in the main text. The file includes figures showing the model's multiple equilibria, and stochastically-induced complex dynamics. (PDF 96 kb)

Supplementary Information 3

Results for a spatial version of the combined model. The file includes a figure showing a realization of the model, as an example of how this version of the model usually allows for high levels of synchrony (correlation greater than 0.8) among sub-populations. (PDF 75 kb)

Supplementary Information 4

Figures showing that changes in the parameter values have only a modest effect on the upper bound of the CV of the time between outbreaks in the combined model. (PDF 295 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dwyer, G., Dushoff, J. & Yee, S. The combined effects of pathogens and predators on insect outbreaks. Nature 430, 341–345 (2004). https://doi.org/10.1038/nature02569

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Sign up for the Nature Briefing newsletter for a daily update on COVID-19 science.
Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing