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Replacement of a dominant viral pathogen by a fungal pathogen does not alter the collapse of a regional forest insect outbreak

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Abstract

Natural enemies and environmental factors likely both influence the population cycles of many forest-defoliating insect species. Previous work suggests precipitation influences the spatiotemporal patterns of gypsy moth outbreaks in North America, and it has been hypothesized that precipitation could act indirectly through effects on pathogens. We investigated the potential role of climatic and environmental factors in driving pathogen epizootics and parasitism at 57 sites over an area of ≈72,300 km2 in four US mid-Atlantic states during the final year (2009) of a gypsy moth outbreak. Prior work has largely reported that the Lymantria dispar nucleopolyhedrovirus (LdNPV) was the principal mortality agent responsible for regional collapses of gypsy moth outbreaks. However, in the gypsy moth outbreak-prone US mid-Atlantic region, the fungal pathogen Entomophaga maimaiga has replaced the virus as the dominant source of mortality in dense host populations. The severity of the gypsy moth population crash, measured as the decline in egg mass densities from 2009 to 2010, tended to increase with the prevalence of E. maimaiga and larval parasitoids, but not LdNPV. A significantly negative spatial association was detected between rates of fungal mortality and parasitism, potentially indicating displacement of parasitoids by E. maimaiga. Fungal, viral, and parasitoid mortality agents differed in their associations with local abiotic and biotic conditions, but precipitation significantly influenced both fungal and viral prevalence. This study provides the first spatially robust evidence of the dominance of E. maimaiga during the collapse of a gypsy moth outbreak and highlights the important role played by microclimatic conditions.

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References

  • Agrios G (2005) Plant pathology. Elsevier/Academic, San Diego

  • Alalouni U, Schädler M, Brandl R (2013) Natural enemies and environmental factors affecting the population dynamics of the gypsy moth. J Appl Entomol 137:721–738. doi:10.1111/jen.12072

  • Andreadis TG, Weseloh RM (1990) Discovery of Entomophaga maimaiga in North American gypsy moth, Lymantria dispar. Proc Natl Acad Sci USA 87:2461–2465

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Anselin L (1988) Spatial econometrics: methods and models. Kluwer, Dordrecht

  • Bell RA, Owens CD, Shapiro M, Tardiff JR (1981) Mass rearing and virus production. In: Doane CC, McManus ML (eds) The gypsy moth: research towards integrated pest management. USDA For Serv Tech Bull 1584:599–655

  • Berryman AA (1999) Principles of population dynamics and their application. Stanley Thornes, Cheltenham

    Google Scholar 

  • Bjørnstad O, Falck W (2001) Nonparametric spatial covariance functions: estimating and testing. Environ Ecol Stat 8:53–70

    Article  Google Scholar 

  • Brown JH, Whitham TG, Ernest MSK, Gehring CA (2001) Complex species interactions and the dynamics of ecological systems: long-term experiments. Science 293:643–650

    Article  CAS  PubMed  Google Scholar 

  • Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci USA 108:662–667

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Campbell RW (1963) The role of disease and desiccation in the population dynamics of the gypsy moth Porthetria dispar (L.) (Lepidoptera: Lymantriidae). Can Entomol 95:426–434

    Article  Google Scholar 

  • Campbell RW, Podgwaite JD (1971) The disease complex of the gypsy moth: I. Major components. J Invertebr Pathol 18:101–107

    Article  CAS  PubMed  Google Scholar 

  • Collins JP (2013) History, novelty, and emergence of an infectious amphibian disease. Proc Natl Acad Sci USA 110:9193–9194

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cunningham JC (1982) Field trials with baculoviruses: control of forest insect pests. In: Kurstak E (ed) Microbial and viral pesticides. Marcel Dekker, New York, pp 335–386

    Google Scholar 

  • Cushman JH, Meentemeyer RK (2008) Multi-scale patterns of human activity and the incidence of an exotic forest pathogen. J Ecol 96:766–776

    Article  Google Scholar 

  • D’Amico V, Elkinton JS (1995) Rainfall effects on transmission of gypsy moth (Lepidoptera: Lymantriidae) nuclear polyhedrosis virus. Environ Entomol 24:1144–1149

    Article  Google Scholar 

  • Doane CC (1970) Primary pathogens and their role in the development of an epizootic in the gypsy moth. J Invertebr Pathol 15:21–33

    Article  Google Scholar 

  • Dwyer G (1994) Density dependence and spatial structure in the dynamics of insect pathogens. Am Nat 143:533–562

    Article  Google Scholar 

  • Dwyer G, Elkinton JS (1995) Host dispersal and the spatial spread of insect pathogens. Ecology 76:1262–1275

    Article  Google Scholar 

  • Dwyer G, Elkinton JS, Hajek AE (1998) Spatial scale and the spread of a fungal pathogen of gypsy moth. Am Nat 152:485–494

    Article  CAS  PubMed  Google Scholar 

  • Dwyer G, Dushoff J, Yee SH (2004) The combined effects of pathogens and predators on insect outbreaks. Nature 430:341–345

    Article  CAS  PubMed  Google Scholar 

  • Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Chapman and Hall, London

    Book  Google Scholar 

  • Elkinton JS, Liebhold AM (1990) Population dynamics of gypsy moth in North America. Annu Rev Entomol 35:571–596

    Article  Google Scholar 

  • Elkinton JS, Hajek AE, Boettner GH, Simons EE (1991) Distribution and apparent spread of Entomophaga maimaiga (Zygomycetes: Entomophthorales) in gypsy moth (Lepidoptera: Lymantriidae) populations in North America. Environ Entomol 20:1601–1605

    Article  Google Scholar 

  • Elkinton JS, Healy WM, Buonaccorsi JP, Boettner GH, Hazzard AM, Smith HR, Liebhold AM (1996) Interactions among gypsy moths, white-footed mice, and acorns. Ecology 77:2332–2342

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GG, Butchkoski CM, Kunz TH (2010) An emerging disease causes regional population collapse of a common North American bat species. Science 329:679–682

    Article  CAS  PubMed  Google Scholar 

  • Fuester R, Hajek AE, Schaefer P, Elkinton JS (2013) Biological control of Lymantria dispar. In: Van Driesche RG, Reardon R (eds) The use of classical biological control to preserve forests in North America. FHTET-2013-02. USDA Forest Service, Forest Health Technology Enterprise Team, Morgantown, West Virginia, pp 49–82

  • Fuxa JR (2004) Ecology of insect nucleopolyhedroviruses. Agric Ecosys Environ 103:27–43

    Article  Google Scholar 

  • Georgiev G, Hubenov Z, Georgieva M, Mirchev P, Matova M, Solter LF, Pilarska D, Pilarski P (2013) Interactions between the introduced fungal pathogen Entomophaga maimaiga and indigenous tachinid parasitoids of gypsy moth Lymantria dispar in Bulgaria. Phytoparasitica 41:125–131

    Article  Google Scholar 

  • Gesch DB (2007) The national elevation dataset. In: Maune D (ed) Digital elevation model technologies and applications: the DEM user’s manual, 2nd edn. American Society for Photogrammetry and Remote Sensing, Bethesda, pp 99–118

    Google Scholar 

  • Gesch D, Oimoen M, Greenlee S, Nelson C, Steuck M, Tyler D (2002) The National Elevation Dataset. Photogramm Eng Remote Sens 68:5–11

  • Hajek AE (1999) Pathology and epizootiology of the Lepidoptera-specific mycopathogen Entomophaga maimaiga. Microbiol Molec Biol Rev 63:814–835

    CAS  Google Scholar 

  • Hajek AE, Tobin PC (2011) Introduced pathogens follow the invasion front of a spreading alien host. J Anim Ecol 80:1217–1226

    Article  PubMed  Google Scholar 

  • Hajek AE, Humber RA, Elkinton JS, May B, Walsh SRA, Silver JC (1990) Allozyme and RFLP analyses confirm Entomophaga maimaiga responsible for 1989 epizootics in North American gypsy moth populations. Proc Natl Acad Sci USA 87:6979–6982

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hajek AE, Humber RA, Elkinton JS (1995) The mysterious origin of Entomophaga maimaiga in North America. Am Entomol 41:31–42

    Article  Google Scholar 

  • Hajek AE, Elkinton JS, Witcosky JJ (1996) Introduction and spread of the fungal pathogen Entomophaga maimaiga along the leading edge of gypsy moth spread. Environ Entomol 25:1235–1247

    Article  Google Scholar 

  • Hajek AE, Olsen C, Elkinton JS (1999) Dynamics of airborne conidia of the gypsy moth (Lepidoptera: Lymantriidae) fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales). Biol Control 16:111–117

    Article  Google Scholar 

  • Hajek AE, Shimazu M, Knoblauch B (2000) Isolating Entomophaga maimaiga using resting spore-bearing soil. J Invertebr Pathol 75:298–300

    Article  CAS  PubMed  Google Scholar 

  • Hajek AE, Plymale RC, Reilly JR (2012) Comparing two methods for quantifying soil-borne Entomophaga maimaiga resting spores. J Invertebr Pathol 111:193–195

    Article  PubMed  Google Scholar 

  • Haynes KJ, Liebhold AM, Johnson DM (2009) Spatial analysis of harmonic oscillation of gypsy moth outbreak intensity. Oecologia 159:249–256

    Article  PubMed  Google Scholar 

  • Haynes KJ, Bjørnstad ON, Allstadt AJ, Liebhold AM (2013) Geographical variation in the spatial synchrony of a forest-defoliating insect: isolation of environmental and spatial drivers. Proc R Soc B 280:20130112. doi:10.1098/rspb.2012.2373

    Article  PubMed Central  Google Scholar 

  • Holt RD, Dobson AP (2006) Extending the principles of community ecology to address the epidemiology of host–pathogen systems. In: Collinge SK, Ray C (eds) Disease ecology: community structure and pathogen dynamics. Oxford University Press, Oxford, pp 6–27

  • Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993

    Article  CAS  PubMed  Google Scholar 

  • Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652

    Article  CAS  PubMed  Google Scholar 

  • Lafferty KD (2009) The ecology of climate change and infectious diseases. Ecology 90:888–900

    Article  PubMed  Google Scholar 

  • Liebhold AM, Thorpe K, Ghent J, Lyons DB (1994) Gypsy moth egg mass sampling for decision-making: a user’s guide. Publication NA-TP-04-94. USDA Forest Service, Morgantown

  • Liebhold AM, Gottschalk KW, Muzika RM, Montgomery ME, Young R, O’Day K, Kelley B (1995) Suitability of North American tree species to the gypsy moth: a summary of field and laboratory tests. Gen Tech Rpt NE-211. USDA Forest Service, Washington, DC

  • Liebhold AM, Gottschalk KW, Luzader ER, Mason DA, Bush R, Twardus DB (1997) Gypsy moth in the United States: an atlas. Gen Tech Rpt NE-233. USDA Forest Service, Washington, DC

  • Liebhold AM, Koenig WD, Bjørnstad ON (2004) Spatial synchrony in population dynamics. Annu Rev Ecol Evol Syst 35:467–490

    Article  Google Scholar 

  • Liebhold AM, Haynes KJ, Bjørnstad ON (2012) Spatial synchrony of insect outbreaks. In: Barbosa P, Letourneau DK, Agrawal AA (eds) Insect outbreaks revisited. Wiley, Chichester, pp 113–125

    Chapter  Google Scholar 

  • Liebhold AM, Plymale R, Elkinton JS, Hajek AE (2013) Emergent fungal entomopathogen does not alter density dependence in a viral competitor. Ecology 94:1217–1222

    Article  PubMed  Google Scholar 

  • Malakar R, Elkinton JS, Hajek AE, Burand JP (1999) Within-host interactions of Lymantria dispar L. (Lepidoptera: Lymantriidae) nucleopolyhedrosis virus (LdNPV) and Entomophaga maimaiga (Zygomycetes: Entomophthorales). J Invertebr Pathol 73:91–100

    Article  PubMed  Google Scholar 

  • McManus M, Csóka G (2007) History and impact of gypsy moth in North America and comparison to recent outbreaks in Europe. Acta Silvat Lignar Hungar 3:47–64

    Google Scholar 

  • McNab WH, Cleland DT, Freeouf JA, Keys Jr JE, Nowacki GJ, Carpenter CA (2007) Description of ecological subregions: sections of the conterminous United States. Gen Tech Rpt WO-76B. USDA Forest Service, Washington, DC

  • Morin Jr RS, Liebhold AM, Luzader ER, Lister AJ, Gottschalk KW, Twardus DB (2005) Mapping host-species abundance of three major exotic forest pests. Res Pap NE-726. USDA Forest Service, Washington, DC

  • Murray K, Elkinton J (1989) Environmental contamination of egg masses as a major component of transgenerational transmission of gypsy moth nuclear polyhedrosis virus (LdMNPV). J Invertebr Pathol 19:662–665

    Google Scholar 

  • Myers JH, Corey JS (2013) Population cycles in forest Lepidoptera revisited. Annu Rev Ecol Evol Syst 44:565–592

    Article  Google Scholar 

  • Myers JH, Malakar R, Cory JS (2000) Sublethal nucleopolyhedrovirus infection effects on female pupal weight, egg mass size, and vertical transmission in gypsy moth (Lepidoptera: Lymantriidae). Environ Entomol 29:1268–1272

    Article  Google Scholar 

  • Nielsen C, Milgroom MG, Hajek AE (2005) Genetic diversity in the gypsy moth fungal pathogen Entomophaga maimaiga from founder populations in North America and source populations in Asia. Mycol Res 109:941–950

    Article  CAS  PubMed  Google Scholar 

  • Peltonen M, Liebhold AM, Bjørnstad ON, Williams DW (2002) Spatial synchrony in forest insect outbreaks: roles of regional stochasticity and dispersal. Ecology 83:3120–3129

    Article  Google Scholar 

  • PRISM Climate Group (2011) PRISM climate data. PRISM Climate Group, Oregon State University, Corvallis. http://prism.oregonstate.edu, created 10 October 2011

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reilly JR, Hajek AE, Liebhold AM, Plymale R (2014) The impact of Entomophaga maimaiga on outbreak gypsy moth populations: the role of weather. Environ Entomol 43:632–641

    Article  PubMed  Google Scholar 

  • Rothman LD, Darling DC (1991) Spatial density dependence: effects of scale, host spatial pattern and parasitoid reproductive strategy. Oikos 62:221–230

    Article  Google Scholar 

  • Royama T (1992) Analytical population dynamics, 1st edn. Chapman and Hall, London

    Book  Google Scholar 

  • Sacks BN, Woodward DL, Colwell AE (2003) A long-term study of non-native-heartworm transmission among coyotes in a Mediterranean ecosystem. Oikos 102:478–490

    Article  Google Scholar 

  • Shapiro-Ilan DI, Bruck DJ, Lacey LA (2012) Principles of epizootiology and microbial control. In: Vega FE, Kaya HK (eds) Insect pathology, 2nd edn. Elsevier, Amsterdam, pp 29–72

    Chapter  Google Scholar 

  • Simons EE, Reardon RC, Ticehurst M (1974) Selected parasites and hyperparasites of the gypsy moth, with keys to adults and immatures. Handbook 540. USDA, Washington, DC

  • Tobin PC, Hajek AE (2012) Release, establishment, and initial spread of the fungal pathogen Entomophaga maimaiga in island populations of Lymantria dispar. Biol Control 63:31–39

    Article  Google Scholar 

  • Tobin PC, Bai BB, Eggen DA, Leonard DS (2012) The ecology, geopolitics, and economics of managing Lymantria dispar in the United States. Int J Pest Manag 53:195–210

    Article  Google Scholar 

  • Tobin PC, Gray DR, Liebhold AM (2014) Supraoptimal temperatures influence the range dynamics of a non-native insect. Divers Distrib 20:813–823

    Article  Google Scholar 

  • Turchin P (2003) Complex population dynamics: a theoretical/empirical synthesis. Princeton University Press, Princeton

    Google Scholar 

  • USDA Forest Service (2013a) Gypsy moth digest. http://na.fs.fed.us/fhp/gm/. Accessed 28 May 2010

  • USDA Forest Service (2013b) Insect and disease detection surveys. http://www.fs.fed.us/foresthealth/technology/adsm.shtml. Accessed 28 September 2010

  • USDA Natural Resources Conservation Service (2012) Soil survey geographic (SSURGO) database. http://soildatamart.nrcs.usda.gov. Accessed 28 May 2010

  • Walde SJ, Murdoch WW (1988) Spatial density dependence in parasitoids. Annu Rev Entomol 33:441–466

    Article  Google Scholar 

  • Weseloh RM (2003) Short and long range dispersal in the gypsy moth (Lepidoptera: Lymantriidae) fungal pathogen, Entomophaga maimaiga (Zygomycetes: Entomophthorales). Environ Entomol 32:111–122

    Article  Google Scholar 

  • Weseloh RM (2004) Effect of conidial dispersal of the fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) on survival of its gypsy moth (Lepidoptera: Lymantriidae) host. Biol Control 29:138–144

    Article  Google Scholar 

  • Weseloh RM, Andreadis TG (1992) Epizootiology of the fungus Entomophaga maimaiga and its impact on gypsy moth populations. J Invertebr Pathol 59:133–141

    Article  Google Scholar 

  • Woods SA, Elkinton JS, Murray KD, Liebhold AM, Gould JR, Podgwaite JD (1991) Transmission dynamics of a nuclear polyhedrosis virus and predicting mortality in gypsy moth (Lepidoptera: Lymantriidae) populations. J Econ Entomol 84:423–430

    Article  Google Scholar 

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Acknowledgments

We thank R. Rabaglia and R. Reardon (USDA Forest Service) for helping to conceive, assist, and design this study. This study was only possible due to extensive assistance from R. Tatman (MD Department of Agriculture), T. Marasco (PA Bureau of Forestry), C. Asaro (VA Department of Forestry), and R. Turcotte (USDA Forest Service, Morgantown, WV) and their teams. At Cornell, samples were diagnosed and data were collated by R. Plymale, S. Long, K. Ciccaglione, C. Fritzen, M. Garvey, M. Grambor, T. James, A. Navarro, and J. Tyvoll, and J. Nix counted resting spore densities in soil samples. We thank L. Blackburn (USDA Forest Service) and J. Walter (University of Virginia) for technical assistance, and A. Liebhold and two anonymous reviewers for comments on the manuscript. This study was funded by USDA Forest Service, Forest Health Protection USDA Forest Service grant #07-CA-11420004-152.

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Correspondence to Ann E. Hajek.

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Communicated by Wolf M. Mooij.

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Hajek, A.E., Tobin, P.C. & Haynes, K.J. Replacement of a dominant viral pathogen by a fungal pathogen does not alter the collapse of a regional forest insect outbreak. Oecologia 177, 785–797 (2015). https://doi.org/10.1007/s00442-014-3164-7

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