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The consequence of leaf life span to virus infection of herbivorous insects

  • Plant-microbe-animal interactions – original research
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Abstract

Many herbivorous insects die of pathogen infections, though the role of plant traits in promoting the persistence of these pathogens as an indirect interaction is poorly understood. We tested whether winter leaf retention of bush lupines (Lupinus arboreus) promotes the persistence of a nucleopolyhedroviruses, thereby increasing the infection risk of caterpillars (Arctia virginalis) feeding on the foliage during spring. We also investigated whether winter leaf retention reduces viral exposure of younger caterpillars that live on the ground, as leaf retention prevents contaminated leaves from reaching the ground. We surveyed winter leaf retention of 248 lupine bush canopies across twelve sites and examined how it related to caterpillar infection risk, herbivory, and inflorescence density. We also manipulated the amount of lupine litter available to young caterpillars in a feeding experiment to emulate litterfall exposure in the field. Greater retention of contaminated leaves from the previous season increased infection rates of caterpillars in early spring. Higher infection rates reduced herbivory and increased plant inflorescence density by summer. Young caterpillars exposed to less litterfall were more likely to starve to death but less likely to die from infection, further suggesting foliage mediated exposure to viruses. We speculate that longer leaf life span may be an unrecognized trait that indirectly mediates top-down control of herbivores by facilitating epizootics.

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Data availability

The data and code are deposited on Dryad and Zenodo respectively. Pan, Vincent; Pepi, Adam; LoPresti, Eric; Karban, Richard (2023), The Consequence of Leaf Life Span to Virus Infection of Herbivorous Insects, Dryad, Dataset, https://doi.org/10.25338/B8PD2K.

References

  • Anderson RM, May RM (1978) Regulation and Stability of Host-Parasite Population Interactions: I. Regulat Proces J Anim Ecol 47:219–247

    Article  Google Scholar 

  • Anderson RM, May RM (1980) Infectious diseases and population cycles of forest insects. Science 210(4470):658–661

    Article  CAS  PubMed  Google Scholar 

  • Barrett JW, Brownwright AJ, Primavera MJ, Palli SR (1998) Studies of the Nucleopolyhedrovirus infection process in insects by using the green fluorescence protein as a reporter. J Virol 72(4):3377–3382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biever KD, Hostetter DL (1985) Field persistence of Trichoplusia ni (Lepidoptera: Noctuidae) single-embedded nuclear polyhedrosis virus on cabbage foliage. Environ Entomol 14(5):579–581

    Article  Google Scholar 

  • Bolnick DI, Amarasekare P, Araújo MS et al (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192

    Article  PubMed  PubMed Central  Google Scholar 

  • Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A et al (2017) GlmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9(2):378–400

    Article  Google Scholar 

  • Bürkner PC (2017) brms: An R package for bayesian multilevel models using Stan. J Stat Softw 80(1):1–28

    Article  Google Scholar 

  • Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Annu Rev Ecol Syst 13(1):229–259

    Article  Google Scholar 

  • Christensen, R. H. B. (2019). ordinal: Regression models for ordinal data (Version 2019.4–25). Retrieved from https://CRAN.R-project.org/package=ordinal

  • Cortesero AM, Stapel JO, Lewis WJ (2000) Understanding and manipulating plant attributes to enhance biological control. Biol Control 17(1):35–49

    Article  Google Scholar 

  • Cory JS, Hoover K (2006) Plant-mediated effects in insect–pathogen interactions. Trends Ecol Evol 21(5):278–286

    Article  PubMed  Google Scholar 

  • Cory JS, Myers JH (2003) The ecology and evolution of insect baculoviruses. Annu Rev Ecol Evol Syst 34:239–272

    Article  Google Scholar 

  • D’Amico V, Elkinton JS (1995) Rainfall effects on transmission of gypsy moth (Lepidoptera: Lymantriidae) nuclear polyhedrosis virus. Environ Entomol 24(5):1144–1149

    Article  Google Scholar 

  • Elliot SL, Sabelis MW, Janssen A, van der Geest LPS, Beerling EAM, Fransen J (2000) Can plants use entomopathogens as bodyguards? Ecol Lett 3(3):228–235

    Article  Google Scholar 

  • Faeth SH, Connor EF, Simberloff D (1981) Early leaf abscission: a neglected source of mortality for folivores. Am Nat 117(3):409–415

    Article  Google Scholar 

  • Gange AC, Koricheva J, Currie AF, Jaber LR, Vidal S (2019) Meta-analysis of the role of entomopathogenic and unspecialized fungal endophytes as plant bodyguards. New Phytol 223(4):2002–2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gasmi L, Martínez-Solís M, Frattini A, Ye M, Collado MC, Turlings TCJ et al (2019) Can herbivore-induced volatiles protect plants by increasing the herbivores’ susceptibility to natural pathogens? Appl Environ Microbiol 85(1):e01468-e1518

    Article  CAS  PubMed  Google Scholar 

  • Grace JB, Johnson DJ, Lefcheck JS, Byrnes JEK (2018) Quantifying relative importance: computing standardized effects in models with binary outcomes. Ecosphere 9(6):e02283

    Article  Google Scholar 

  • Harrison S, Maron JL (1995) Impacts of defoliation by tussock moths (Orgyia vetusta) on the growth and reproduction of bush lupine (Lupinus arboreus). Ecol Entomol 20(3):223–229

    Article  Google Scholar 

  • Hay WT, Behle RW, Berhow MA, Miller AC, Selling GW (2020) Biopesticide synergy when combining plant flavonoids and entomopathogenic baculovirus. Sci Rep 10:6806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hodgson DJ, Vanbergen AJ, Hartley SE, Hails RS, Cory JS (2002) Differential selection of baculovirus genotypes mediated by different species of host food plant. Ecol Lett 5(4):512–518

    Article  Google Scholar 

  • Hoover K, Washburn JO, Volkman LE (2000) Midgut-based resistance of Heliothis virescens to baculovirus infection mediated by phytochemicals in cotton. J Insect Physiol 46(6):999–1007

    Article  CAS  PubMed  Google Scholar 

  • Hountondji FCC, Sabelis MW, Hanna R, Janssen A (2005) Herbivore-induced plant volatiles trigger sporulation in entomopathogenic fungi: the case of Neozygites tanajoae infecting the cassava green mite. J Chem Ecol 31(5):1003–1021

    Article  CAS  PubMed  Google Scholar 

  • Hsieh Y-L, Linsenmair KE (2012) Seasonal dynamics of arboreal spider diversity in a temperate forest. Ecol Evol 2(4):768–777

    Article  PubMed  PubMed Central  Google Scholar 

  • Inglis GD, Goettel MS, Johnson DL (1993) Persistence of the entomopathogenic fungus Beauveria bassiana, on phylloplanes of crested wheatgrass and alfalfa. Biol Control 3:258–270

    Article  Google Scholar 

  • Inglis GD, Johnson DL, Goettel MS (1995) Effects of simulated rain on the persistence of Beauveria bassiana conidia on leaves of alfalfa and wheat. Biocontrol Sci Technol 5(3):365–370

    Article  Google Scholar 

  • Inyang EN, Butt TM, Beckett A, Archer S (1999) The effect of crucifer epicuticular waxes and leaf extracts on the germination and virulence of Metarhizium anisopliae conidia. Mycol Res 103(4):419–426

    Article  CAS  Google Scholar 

  • Kahn DM, Cornell HV (1989) Leafminers, early leaf abscission, and parasitoids: a yritrophic interaction. Ecology 70(5):1219–1226

    Article  Google Scholar 

  • Karban R, Grof-Tisza P, Maron JL, Holyoak M (2012) The importance of host plant limitation for caterpillars of an arctiid moth (Platyprepia virginalis) varies spatially. Ecology 93(10):2216–2226

    Article  PubMed  Google Scholar 

  • Karban R, Grof-Tisza P, Holyoak M (2017) Wet years have more caterpillars: Interacting roles of plant litter and predation by ants. Ecology 98(9):2370–2378

    Article  PubMed  Google Scholar 

  • Keathley CP, Harrison RL, Potter DA (2012) Baculovirus infection of the armyworm (Lepidoptera: Noctuidae) feeding on spiny- or smooth-edged grass (Festuca spp.) leaf blades. Biol Control 61:147–154

    Article  Google Scholar 

  • Lacey LA, Solter LF (2012) Initial handling and diagnosis of diseased invertebrates. In: Lacey LA (ed) Manual of Techniques in Invertebrate Pathology. Academic press, London

    Google Scholar 

  • Lefcheck JS (2016) piecewiseSEM: Piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol Evol 7(5):573–579

    Article  Google Scholar 

  • Lev-Yadun S, Halpern M (2008) External and internal spines in plants insert pathogenic microorganisms into herbivore’s tissues for defense. In: Trends MER (ed) T, vol Dijk. Nova Biomedical Books, New York, pp 155–168

    Google Scholar 

  • Lynch RE, Lewis LC, Berry EC (1980) Application efficacy and field persistence of Bacillus thuringiensis when applied to corn for European corn borer control. J Econ Entomol 73(1):4–7

    Article  Google Scholar 

  • Marquis RJ (1996) Plant architecture, sectoriality and plant tolerance to herbivores. Vegetatio 127:85–97

    Article  Google Scholar 

  • McGuire MR, Shasha BS, Lewis LC, Nelsen TC (1994) Residual activity of granular starch-encapsulated Bacillus thuringiensis. J Econ Entomol 87(3):631–637

    Article  Google Scholar 

  • Mooney HA, Dunn EL (1970) Photosynthetic systems of mediterranean-climate shrubs and trees of California and Chile. Am Nat 104(939):447–453

    Article  Google Scholar 

  • Myers JH, Cory JS (2013) Population cycles in forest Lepidoptera revisited. Annu Rev Ecol Evol Syst 44(1):565–592

    Article  Google Scholar 

  • Myers JH, Cory JS (2016) Ecology and evolution of pathogens in natural populations of Lepidoptera. Evol Appl 9(1):231–247

    Article  PubMed  Google Scholar 

  • Nilsson SG (1983) Evolution of leaf abscission times: alternative hypotheses. Oikos 40:318

    Article  Google Scholar 

  • Orrock J, Connolly B, Kitchen A (2017) Induced defences in plants reduce herbivory by increasing cannibalism. Nat Ecol Evol 1(8):1205–1207

    Article  PubMed  Google Scholar 

  • Otto C, Nilsson LM (1981) Why do beech and oak trees retain leaves until spring? Oikos 37(3):387

    Article  CAS  Google Scholar 

  • Pearse IS, LoPresti E, Schaeffer RN, Wetzel WC, Mooney KA, Ali JG et al (2020) Generalising indirect defence and resistance of plants. Ecol Lett 23(7):1137–1152

    Article  PubMed  Google Scholar 

  • Pepi A, Holyoak M, Karban R (2021) Altered precipitation dynamics lead to a shift in herbivore dynamical regime. Ecol Lett 24(7):1400–1407

    Article  PubMed  Google Scholar 

  • Pepi A, Pan V, Rutkowski D, Mase V, Karban R (2022) Influence of delayed density and ultraviolet radiation on caterpillar baculovirus infection and mortality. J Anim Ecol 91(11):2192–2202

    Article  PubMed  Google Scholar 

  • Pritchard IM, James R (1984) Leaf fall as a source of leaf miner mortality. Oecologia 64(1):140–141

    Article  CAS  PubMed  Google Scholar 

  • Pritzkow S, Morales R, Moda F, Khan U, Telling GC, Hoover E et al (2015) Grass plants bind, retain, uptake and transport infectious prions. Cell Rep 11(8):1168–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team. (2020). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.r-project.org/

  • Raymond B, Hartley SE, Cory JS, Hails RS (2005) The role of food plant and pathogen-induced behaviour in the persistence of a nucleopolyhedrovirus. J Invertebr Pathol 88(1):49–57

    Article  PubMed  Google Scholar 

  • Rosa E, Woestmann L, Biere A, Saastamoinen M (2018) A plant pathogen modulates the effects of secondary metabolites on the performance and immune function of an insect herbivore. Oikos 127(10):1539–1549

    Article  CAS  Google Scholar 

  • Shikano I (2017) Evolutionary ecology of multitrophic interactions between plants, insect herbivores and entomopathogens. J Chem Ecol 43(6):586–598

    Article  CAS  PubMed  Google Scholar 

  • Shikano I, Shumaker KL, Peiffer M, Felton GW, Hoover K (2017) Plant-mediated effects on an insect–pathogen interaction vary with intraspecific genetic variation in plant defences. Oecologia 183(4):1121–1134

    Article  PubMed  Google Scholar 

  • Shikano I, McCarthy E, Hayes-Plazolles N, Slavicek JM, Hoover K (2018) Jasmonic acid-induced plant defenses delay caterpillar developmental resistance to a baculovirus: Slow-growth, high-mortality hypothesis in plant–insect–pathogen interactions. J Invertebr Pathol 158:16–23

    Article  CAS  PubMed  Google Scholar 

  • Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90(2):363–368

    Article  PubMed  Google Scholar 

  • Stiling P, Simberloff D (1989) Leaf Abscission: Induced Defense against Pests or Response to Damage? Oikos 55(1):43–49

    Article  Google Scholar 

  • Therneau, T. M. (2020). survival: Survival Analysis (Version 3.2–7). Retrieved from https://CRAN.R-project.org/package=survival

  • Vega F, Kaya H (2012) Insect Pathology, 2nd edn. Academic Press, San Diego, CA

    Google Scholar 

  • Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92(1):3–10

    Article  PubMed  Google Scholar 

  • Williams T, Virto C, Murillo R, Caballero P (2017) Covert Infection of Insects by Baculoviruses. Front Microbiol 8:1337

    Article  PubMed  PubMed Central  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F et al (2004) The worldwide leaf economics spectrum. Nature 428(6985):821

    Article  CAS  PubMed  Google Scholar 

  • Yamazaki K, Sugiura S (2008) Deer predation on leaf miners via leaf abscission. Sci Nat 95(3):263–268

    Article  CAS  Google Scholar 

  • Zhao X, Lynch JG Jr, Chen Q (2010) Reconsidering baron and kenny: myths and truths about mediation analysis. J Consum Res 37:197–206

    Article  Google Scholar 

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Acknowledgements

We thank Harry Kaya, Danielle Rutkowski, Vinay Mase, Michael Turelli, and Jenny Cory for helping with the identification of the virus, Neal Williams for sharing microscope equipment and freezer, Jay Rosenheim for sharing incubators and lab space, Claire Beck and Jasmine Daragahi for help with rearing caterpillars, Jackie Sones for aiding access to the Bodega Marine Reserve, the joint-insect ecology lab group at UC Davis for providing feedback, Hanna Kahl and Emily Meineke for commenting on our manuscript, and the anonymous reviewers for providing constructive comments.

Funding

VSP, AP, and RK were funded by NSF-LTREB (1456225) and an NSF-REU supplement (DEB-2018169). EFL was funded by start-up funds from Oklahoma State University.

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Authors and Affiliations

  1. Department of Integrative Biology, Michigan State University, 288 Farm Lane, East Lansing, MI, 48824, USA

    Vincent S. Pan

  2. Department of Entomology and Nematology, University of California-Davis, Briggs Hall, One Shields Avenue, Davis, CA, 95616, USA

    Adam Pepi & Richard Karban

  3. Department of Biological Sciences, University of South Carolina, 700 Sumter St #401, Columbia, SC, 29208, USA

    Eric F. LoPresti

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  1. Vincent S. Pan
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  2. Adam Pepi
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Contributions

VSP, AP, and RK conceived the study and collected the data. VSP and AP conducted the analysis. VSP wrote the manuscript. AP, EFL, and RK provided editorial support. All authors contributed critically to the drafts and approved final publication.

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Correspondence to Vincent S. Pan.

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Communicated by Caroline Müller.

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Pan, V.S., Pepi, A., LoPresti, E.F. et al. The consequence of leaf life span to virus infection of herbivorous insects. Oecologia 201, 449–459 (2023). https://doi.org/10.1007/s00442-023-05325-w

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