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Gypsy moth herbivory induced volatiles and reduced parasite attachment to cranberry hosts

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Abstract

Interactions between species can have cascading effects that shape subsequent interactions. For example, herbivory can induce plant defenses that affect subsequent interactions with herbivores, pathogens, mycorrhizae, and pollinators. Parasitic plants are present in most ecosystems, and play important roles in structuring communities. However, the effects of host herbivory on parasitic plants, and the potential mechanisms underlying such effects, are not well known. We conducted a greenhouse study to ask whether gypsy moth (Lymantria dispar) damage, host cultivar, and their interaction affected preference of the stem parasite dodder (Cuscuta spp.) on cranberry hosts (Vaccinium macrocarpum). We then assessed the mechanisms that could underlie such effects by measuring induced changes in phytohormones and secondary compounds. We found that damage by gypsy moths delayed dodder attachment by approximately 0.3 days when dodder stems were added 2 days after damage, and reduced attachment by more than 50% when dodder stems were added 1 week after host plant damage. Gypsy moth damage significantly increased jasmonic acid (JA) levels, total volatile emissions, and the flavonol, quercetin aglycone, suggesting possible mechanisms underlying variation in dodder ability to locate or attach to hosts. Dodder preference also differed between cranberry cultivars, with the highest attachment on the cultivar that had significantly lower levels of total volatile emissions and total phenolic acids, suggesting that volatile composition and phenolics may mediate dodder preference. Our results indicate that herbivory can reduce subsequent attachment by a highly damaging parasitic plant, demonstrating the potential importance of early damage for shaping subsequent species interactions.

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References

  • Adler FR, Karban R (1994) Defended fortresses or moving targets? Another model of inducible defenses inspired by military metaphors. Am Nat 144:813–832

    Article  Google Scholar 

  • Adler LS, Karban R, Strauss SY (2001) Direct and indirect effects of alkaloids on plant fitness via herbivory and pollination. Ecology 82:2032–2044

    Article  Google Scholar 

  • Agrawal AA (1999) Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness. Ecology 80:1713–1723

    Article  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. doi:10.1111/j.1442-9993.2001.01070

    Google Scholar 

  • Bell R, Owens C, Shapiro M, Tardif J (1981) Development of mass rearing technology. The gypsy moth: research toward integrated pest management, vol 1584. USDA, Washington, DC, pp 599–633

    Google Scholar 

  • Beninger CW, AbouZaid MM (1997) Flavonol glycosides from four pine species that inhibit early instar gypsy moth (Lepidoptera: Lymantriidae) development. Biochem Syst Ecol 25:505–512. doi:10.1016/s0305-1978(97)00034-3

    Article  CAS  Google Scholar 

  • Chandler FB, Demoranville IE (1958) Cranberry varieties of North America. Bulletin—Massachusetts agricultural experiment station no. 513

  • Dana MN (1983) Cranberry cultivar list (Vaccinium macrocarpon). Fruit Var J 37:88–95

    Google Scholar 

  • Dawson JH, Musselman J, Wolswinkel P, Dorr I (1984) Biology and control of Cuscuta. Weed Sci 6:265–317

    Google Scholar 

  • De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580

    Article  PubMed  Google Scholar 

  • Devlin RM, Deubert KH (1980) Control of swamp dodder (Cuscuta gronovii) on cranberry bogs with butralin. Proc Northeast Weed Sci Soc 11:112–113

    Google Scholar 

  • Dicke M (2016) Plant phenotypic plasticity in the phytobiome: a volatile issue. Curr Opin Plant Biol 32:17–23. doi:10.1016/j.pbi.2016.05.004

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Erb M, Robert CAM, Hibbard BE, Turlings TCJ (2011) Sequence of arrival determines plant-mediated interactions between herbivores. J Ecol 99:7–15. doi:10.1111/j.1365-2745.2010.01757.x

    Article  Google Scholar 

  • Franklin HJ (1950) Cranberry insects in Massachusetts. Bulletin no. 445, Part 1. MA Agricultural Experiment Station, Amherst, MA

  • Gehring C, Bennett A (2009) Mycorrhizal fungal-plant-insect interactions: the importance of a community approach. Environ Entomol 38:93–102. doi:10.1603/022.038.0111

    Article  PubMed  Google Scholar 

  • Ghantous KM, Sandler HA (2012) Mechanical scarification of dodder seeds with a handheld rotary tool. Weed Technol 26:485–489. doi:10.1614/wt-d-11-00077.1

    Article  Google Scholar 

  • Ghantous KM, Stefanovic S, Sandler HA (2012) Initial investigations into dodder species variation in Southeastern Massachusetts. In: Proceedings of northeastern weed science society, vol. 66, Philadelphia, p 60

  • Gilbert L, Johnson D (2015) Plant-mediated ‘apparent effects’ between mycorrhiza and insect herbivores. Curr Opin Plant Biol 26:100–105. doi:10.1016/j.pbi.2015.06.008

    Article  PubMed  Google Scholar 

  • Goldwasser Y, Lanini WT, Wrobel RL (2001) Tolerance of tomato varieties to Lespedeza dodder. Weed Sci 49:520–523

    Article  CAS  Google Scholar 

  • Gouinguene S, Degen T, Turlings TCJ (2001) Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11:9–16. doi:10.1007/pl00001832

    Article  CAS  Google Scholar 

  • Hartley SE, Green JP, Massey FP, Press MCP, Stewart AJA, John EA (2015) Hemiparasitic plant impacts animal and plant communities across four trophic levels. Ecology 96:2408–2416. doi:10.1890/14-1244.1

    Article  CAS  PubMed  Google Scholar 

  • Ihl B, Tutakhil N, Hagen A, Jacob F (1988) Studies on Roxb. 7. defense mechanisms of Lycopersicon esculentum Mill. Flora 181:383–393

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Karban R, Agrawal AA, Thaler JS, Adler LS (1999) Induced plant responses and information content about risk of herbivory. Trends Ecol Evol 14:443–447

    Article  CAS  PubMed  Google Scholar 

  • Karban R, Yang LH, Edwards KF (2014) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17:44–52. doi:10.1111/ele.12205

    Article  PubMed  Google Scholar 

  • Kelly CK (1990) Plant foraging: a marginal value model and coiling response in Cuscuta subinclusa. Ecology 71:1916–1925

    Article  Google Scholar 

  • Kelly CK (1992) Resource choice in Cuscuta europaea. Ecology 89:12194–12197

    CAS  Google Scholar 

  • Lattanzio V, Lattanzio VMT, Cardinali A (2006) Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. Phytochem Adv Res 661:23–67

    Google Scholar 

  • Lucas-Barbosa D (2016) Integrating studies on plant-pollinator and plant-herbivore interactions. Trends Plant Sci 21:125–133. doi:10.1016/j.tplants.2015.10.013

    Article  CAS  PubMed  Google Scholar 

  • Lucas-Barbosa D, van Loon JJA, Dicke M (2011) The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry 72:1647–1654. doi:10.1016/j.phytochem.2011.03.013

    Article  CAS  PubMed  Google Scholar 

  • Matthies D (1996) Interactions between the root hemiparasite Melampyrum arvense and mixtures of host plants: heterotrophic benefit and parasite-mediated competition. Oikos 75:118–124. doi:10.2307/3546328

    Article  Google Scholar 

  • Matthies D (1998) Influence of the host on growth and biomass allocation in the two facultative root hemiparasites Odontites vulgaris and Euphrasia minima. Flora 193:187–193

    Article  Google Scholar 

  • McArt SH, Halitschke R, Salminen J-P, Thaler JS (2013) Leaf herbivory increases plant fitness via induced resistance to seed predators. Ecology 94:966–975. doi:10.1890/12-1664.1

    Article  Google Scholar 

  • Pennings SC, Callaway RM (1996) Impact of a parasitic plant on the structure and dynamics of salt marsh vegetation. Ecology 77:1410–1419

    Article  Google Scholar 

  • Pennings SC, Callaway RM (2002) Parasitic plants: parallels and contrasts with herbivores. Oecologia 131:479–489

    Article  PubMed  Google Scholar 

  • Pennings SC, Simpson JC (2008) Like herbivores, parasitic plants are limited by host nitrogen content. Plant Ecol 196:245–250. doi:10.1007/s11258-007-9348-z

    Article  Google Scholar 

  • Pérez-de-Luque A, Moreno MT, Rubiales D (2008) Host plant resistance against broomrapes (Orobanche spp.): defence reactions and mechanisms of resistance. Ann Appl Biol 152:131–141

    Article  Google Scholar 

  • Poelman EH, Van Loon JJA, Van Dam NM, Vet LEM, Dicke M (2010) Herbivore-induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack. Ecol Entomol 35:240–247. doi:10.1111/j.1365-2311.2010.01179.x

    Article  Google Scholar 

  • Puustinen S, Salonen V (1999) The effect of host defoliation on hemiparasitic-host interactions between Rhinanthus serotinus and two Poa species. Can J Bot Rev Can Bot 77:523–530

    Article  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing R Foundation for Statistical Computing. Austria, Vienna

    Google Scholar 

  • Ren YQ, Guan KY, Li AR, Hu XJ, Zhang L (2010) Host dependence and preference of the root hemiparasite, Pedicularis cephalantha Franch. (Orobanchaceae). Folia Geobot 45:443–455. doi:10.1007/s12224-010-9081-6

    Article  Google Scholar 

  • Rodriguez-Saona CR et al (2011) Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. J Exp Bot 62:2633–2644

    Article  CAS  PubMed  Google Scholar 

  • Rowntree JK, Barham DF, Stewart AJA, Hartley SE (2014) The effect of multiple host species on a keystone parasitic plant and its aphid herbivores. Funct Ecol 28:829–836. doi:10.1111/1365-2435.12281

    Article  Google Scholar 

  • Runyon JB, Mescher MC, De Moraes CM (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–1967

    Article  CAS  PubMed  Google Scholar 

  • Runyon JB, Mescher MC, Felton GW, De Moraes CM (2010) Parasitism by Cuscuta pentagona sequentially induces JA and SA defense pathways in tomato. Plant Cell Environ 33:290–303

    Article  CAS  PubMed  Google Scholar 

  • Seel WE, Cooper RE, Press MC (1993) Growth, gas-exchange and water-use efficiency of the facultative hemiparasite rhinanthus-minor associated with hosts differing in foliar nitrogen concentration. Physiol Plant 89:64–70

    Article  CAS  Google Scholar 

  • Stam JM et al (2014) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65(65):689–713. doi:10.1146/annurev-arplant-050213-035937

    Article  CAS  PubMed  Google Scholar 

  • Theis N, Kesler KE, Adler LS (2009) Leaf herbivory increases floral fragrance in male but not female Cucurbita pepo subsp. texana (Cucurbitaceae) flowers. Am J Bot. 95(5):897-903

    Article  Google Scholar 

  • Tjiurutue MC, Sandler HA, Kersch-Becker MF, Theis N, Adler LS (2016) Cranberry resistance to dodder parasitism: induced chemical defenses and behavior of a parasitic plant. J Chem Ecol 42:95–106. doi:10.1007/s10886-016-0671-5

    Article  CAS  PubMed  Google Scholar 

  • Uesugi A, Poelman E, Kessler A (2013) A test of genotypic variation in specificity of herbivore-induced responses in Solidago altissima L. (Asteraceae). Oecologia 173:1387–1396

    Article  PubMed  Google Scholar 

  • Van Zandt PA, Agrawal AA (2004) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629

    Article  Google Scholar 

  • Vorsa N (2010) Cranberry, in register of new fruit and nut cultivars, (List 45). In: Clark JR, Finn CE (Eds) HortScience 45:536–562

  • Vvedenskaya IO, Rosen RT, Guido JE, Russell DJ, Mills KA, Vorsa N (2004) Characterization of flavonols in cranberry (Vaccinium macrocarpon) powder. J Agric Food Chem 52:188–195. doi:10.1021/jf034970s

    Article  CAS  PubMed  Google Scholar 

  • Walling L (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195

    CAS  PubMed  Google Scholar 

  • Yoder JI, Scholes JD (2010) Host plant resistance to parasitic weeds; recent progress and bottlenecks. Curr Opin Plant Biol 13:478–484

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank S. Sha and N. Vorsa for conducting the phenolic profile analysis, J. Normanly for the use of lab space and GC–MS for volatile analysis, V. Tumasyan for help with volatile analysis, R. Halitschke for his assistance in the phytohormone analyses, former and present Adler lab members for comments on the manuscript, M. Kinyota and E. Palmer-Young for help with data collection, the UMass Cranberry Station (especially J. O’Connell and K. Ghantous) for cranberry cultivation and supply of dodder seed, and the UMass greenhouse stuff, C. Joyner and colleagues. We also thank U.S. Department of Agriculture-APHIS for providing gypsy moth larvae.

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Contributions

MCT, HAS, and LSA conceived and designed the experiments. MCT, MFK, and NT performed the experiments. MCT and NT analyzed the data. MCT and LSA wrote the manuscript; all authors provided editorial advice.

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Correspondence to Lynn S. Adler.

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Funding

The study was funded by Fulbright Fellowship (MCT), Faculty for the Future Fellowship (MCT), Plant Biology Graduate program (MCT), the United States Department of Agriculture/Cooperative Research and Extension Services (Hatch) MAS000411 (LSA) and United States Department of Agriculture National Research Initiative 2008-02346 (LSA).

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The authors declare that they have no conflict of interest.

Data availability

The data for this article are publicly available in Dryad: doi:10.5061/dryad.bj3tt.

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Communicated by Evan H DeLucia.

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Tjiurutue, M.C., Sandler, H.A., Kersch-Becker, M.F. et al. Gypsy moth herbivory induced volatiles and reduced parasite attachment to cranberry hosts. Oecologia 185, 133–145 (2017). https://doi.org/10.1007/s00442-017-3915-3

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