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Exogenous application of methyl jasmonate to Ficus hahliana attracts predators of insects along an altitudinal gradient in Papua New Guinea

  • Anna Mrazova (a1) (a2) and Katerina Sam (a1) (a2)

Abstract

In many plants, the defence systems against herbivores are induced, and may be involved in recruiting the natural enemies of herbivores. We used methyl jasmonate, a well-known inducer of plant defence responses, to manipulate the chemistry of Ficus hahliana along a tropical altitudinal gradient in order to test its ability to attract the enemies of herbivores. We examined whether chemical signals from MeJA-treated trees (simulating leaf damage by herbivores) attracted insect enemies in the complex settings of a tropical forest; and how this ability changes with altitude, where the communities of predators differ naturally. We conducted the research at four study sites (200, 700, 1700 and 2700 m asl) of Mt Wilhelm in Papua New Guinea. Using dummy plasticine caterpillars to assess predation on herbivorous insect, we showed that, on average, inducing plant defences with jasmonic acid in this tropical forest increases predation twofold (i.e. caterpillars exposed on MeJA-sprayed trees were attacked twice as often as caterpillars exposed on control trees). The predation rate on control trees decreased with increasing altitude from 20.2% d−1 at 200 m asl to 4.7% d−1 at 2700 m asl. Predation on MeJA-treated trees peaked at 700 m (52.3% d−1) and decreased to 20.8% d−1 at 2700 m asl. Arthropod predators (i.e. ants and wasps) caused relatively more attacks in the lowlands (200–700 m asl), while birds became the dominant predators above 1700 m asl. The predation pressure from birds and arthropods corresponded with their relative abundances, but not with their species richness. Our study found a connection between chemically induced defence in plants and their attractivity to predators of herbivorous insect in the tropics.

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References

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Agrawal, AA (1998) Leaf damage and associated cues induce aggressive ant recruitment in a neotropical ant-plant. Ecology 79, 21002112.10.1890/0012-9658(1998)079[2100:LDAACI]2.0.CO;2
Amo, L, Jansen, JJ, Dam, NM, Dicke, M and Visser, ME (2013) Birds exploit herbivore–induced plant volatiles to locate herbivorous prey. Ecology Letters 16, 13481355.10.1111/ele.12177
Baldwin, IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences USA 95, 81138118.10.1073/pnas.95.14.8113
Cipollini, D, Purrington, CB and Bergelson, J (2003) Costs of induced responses in plants. Basic and Applied Ecology 4, 7989.10.1078/1439-1791-00134
Colwell, RK, Gotelli, NJ, Ashton, LA, Beck, J, Brehm, G, Fayle, TM, Klimes, P, Kluge, J, Longino, JT, Maunsell, SC, McCain, CM, Moses, J, Noben, S, Sam, K, Sam, L, Shapiro, AM, Wang, X and Novotny, V (2016) Midpoint attractors and species richness, modelling the interaction between environmental drivers and geometric constraints. Ecology Letters 19, 10091022.10.1111/ele.12640
De Moraes, CM, Lewis, WJ, Pare, PW, Alborn, HT and Tumlinson, JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393, 570573.10.1038/31219
Dicke, M, Gols, R, Ludeking, D and Posthumus, MA (1999) Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. Journal of Chemical Ecology 25, 19071922.10.1023/A:1020942102181
Felton, GW and Korth, KL (2000) Trade-offs between pathogen and herbivore resistance. Current Opinion in Plant Biology 3, 309314.10.1016/S1369-5266(00)00086-8
Gill, F and Donsker, D (eds) (2019) IOC World Bird List (v9.1). doi: 10.14344/IOC.ML.9.1. https://www.worldbirdnames.org/.
Heil, M (2014) Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytologist 204, 297306.10.1111/nph.12977
Hopke, J, Donath, J, Blechert, S and Boland, W (1994) Herbivore-induced volatiles: the emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a β-glucosidase and jasmonic acid. FEBS Letters 352, 146150.10.1016/0014-5793(94)00948-1
Hothorn, T, Bretz, F and Westfall, P (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346363.10.1002/bimj.200810425
Howe, A, Lövei, GL and Nachman, G (2009) Dummy caterpillars as a simple method to assess predation rates on invertebrates in a tropical agroecosystem. Entomologia Experimentalis et Applicata 131, 325329.10.1111/j.1570-7458.2009.00860.x
Jeanne, RL (1979) A latitudinal gradient in rates of ant predation. Ecology 60, 12111224.10.2307/1936968
Karban, R (2007) Damage to sagebrush attracts predators but this does not reduce herbivory. Entomologia Experimentalis et Applicata 125, 7180.10.1111/j.1570-7458.2007.00594.x
Kessler, A and Baldwin, IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 21412144.10.1126/science.291.5511.2141
Koski, TM, Laaksonen, T, Mäntylä, E, Ruuskanen, S, Li, T, Girón-Calva, PS, Huttunen, L, Blande, JD, Holopainen, JK and Klemola, T (2015) Do insectivorous birds use volatile organic compounds from plants as olfactory foraging cues? Three experimental tests. Ethology 121, 11311144.10.1111/eth.12426
Low, PA, Sam, K, McArthur, C, Posa, MRC and Hochuli, DF (2014) Determining predator identity from attack marks left in model caterpillars: guidelines for best practice. Entomologia Experimentalis et Applicata 152, 120126.10.1111/eea.12207
Mäntylä, E, Klemola, T and Haukioja, E (2004) Attraction of willow warblers to sawfly-damaged mountain birches: novel function of inducible plant defences? Ecology Letters 7, 915918.10.1111/j.1461-0248.2004.00653.x
Mäntylä, E, Klemola, T, Sirkiä, P and Laaksonen, T (2008) Low light reflectance may explain the attraction of birds to defoliated trees. Behavioral Ecology 19, 325330.10.1093/beheco/arm135
Mäntylä, E, Blande, JD and Klemola, T (2014) Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature? Arthropod–Plant Interactions 8, 143153.10.1007/s11829-014-9296-1
Marki, PZ, Sam, K, Koane, B, Kristensen, JB, Kennedy, JD and Jønsson, KA (2016) New and noteworthy bird records from the Mt Wilhelm elevational gradient, Papua New Guinea. Bulletin of the British Ornithologists’ Club 137, 263271.
Mithöfer, A, Wanner, G and Boland, W (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiology 137, 11601168.10.1104/pp.104.054460
Mooney, KA (2007) Tritrophic effects of birds and ants on a canopy food web, tree growth, and phytochemistry. Ecology 88, 20052014.10.1890/06-1095.1
Mrazova, A and Sam, K (2018) Application of methyl jasmonate to grey willow (Salix cinerea) attracts insectivorous birds in nature. Arthropod–Plant Interactions 12, 18.10.1007/s11829-017-9558-9
Novotny, V and Basset, Y (2005) Host specificity of insect herbivores in tropical forests. Proceedings of the Royal Society B: Biological Sciences 272, 10831090.10.1098/rspb.2004.3023
Posa, MRC, Sodhi, NS and Koh, LP (2007) Predation on artificial nests and caterpillar models across a disturbance gradient in Subic Bay, Philippines. Journal of Tropical Ecology 23, 2733.10.1017/S0266467406003671
Rodriguez-Saona, C, Crafts-Brandner, SJ, Paré, PW and Henneberry, TJ (2001) Exogenous methyl jasmonate induces volatile emissions in cotton plants. Journal of Chemical Ecology 27, 679695.10.1023/A:1010393700918
Rodriguez-Saona, CR, Polashock, J and Malo, EA (2013) Jasmonate-mediated induced volatiles in the American cranberry, Vaccinium macrocarpon: from gene expression to organismal interactions. Frontiers in Plant Science 4, 115.10.3389/fpls.2013.00115
Romero, GQ and Izzo, TJ (2004) Leaf damage induces ant recruitment in the Amazonian ant-plant Hirtella myrmecophila. Journal of Tropical Ecology 20, 675682.10.1017/S0266467404001749
Roslin, T, Hardwick, B, Novotny, V, Petry, WK, Andrew, NR, Asmus, A, Barrio, IC, Basset, Y, Boesing, AL and Bonebrake, TC (2017) Higher predation risk for insect prey at low latitudes and elevations. Science 356, 742744.10.1126/science.aaj1631
Sam, K and Koane, B (2014) New avian records along the elevational gradient of Mt Wilhelm, Papua New Guinea. Bulletin of the British Ornithologists’ Club 134, 116133.
Sam, K, Koane, B and Novotny, V (2015a) Herbivore damage increases avian and ant predation of caterpillars on trees along a complete elevational forest gradient in Papua New Guinea. Ecography 38, 293300.10.1111/ecog.00979
Sam, K, Remmel, T and Molleman, F (2015b) Material affects attack rates on dummy caterpillars in tropical forest where arthropod predators dominate: an experiment using clay and dough dummies with green colourants on various plant species. Entomologia Experimentalis et Applicata 157, 317324.10.1111/eea.12367
Sam, K, Koane, B, Jeppy, S, Sykorova, J and Novotny, V (2017) Diet of land birds along an elevational gradient in Papua New Guinea. Scientific Reports 7, 44018.10.1038/srep44018
Schemske, DW, Mittelbach, GG, Cornell, HV, Sobel, JM and Roy, K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annual Review of Ecology, Evolution, and Systematics 40, 245269.10.1146/annurev.ecolsys.39.110707.173430
Schmidt, JO (1990) Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators. Albany, NY: SUNY Press, 502 pp.
Segar, ST, Volf, M, Zima, J Jr, Isua, B, Sisol, M, Sam, L, Sam, K, Souto-Vilarós, D and Novotny, V (2016) Speciation in a keystone plant genus is driven by elevation: a case study in New Guinean Ficus. Journal of Evolutionary Biology 30, 512523.10.1111/jeb.13020
Takabayashi, J and Dicke, M (1996) Plant–carnivore mutualism through herbivore-induced carnivore attractants. Trends in Plant Science 1, 109113.10.1016/S1360-1385(96)90004-7
Thaler, JS (1999) Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature 399, 686688.10.1038/21420
Thaler, JS, Stout, MJ, Karban, R and Duffey, SS (1996) Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. Journal of Chemical Ecology 22, 17671781.10.1007/BF02028503
Turlings, TC, Humlington, JH and Lewis, WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasite wasps. Science 250, 12511253.10.1126/science.250.4985.1251
Tvardikova, K and Novotny, V (2012) Predation on exposed and leaf-rolling artificial caterpillars in tropical forests of Papua New Guinea. Journal of Tropical Ecology 28, 331341.10.1017/S0266467412000235
Van Bael, SA, Brawn, JD and Robinson, SK (2003) Birds defend trees from herbivores in a Neotropical forest canopy. Proceedings of the National Academy of Sciences USA 100, 83048307.10.1073/pnas.1431621100
Van Bael, SA, Philpott, SM, Greenberg, R, Bichier, P, Barber, NA, Mooney, KA and Gruner, DS (2008) Birds as predators in tropical agroforestry systems. Ecology 89, 928934.10.1890/06-1976.1
Véle, A, Holuša, J and Frouz, J (2009) Sampling for ants in different-aged spruce forests: a comparison of methods. European Journal of Soil Biology 45, 301305.10.1016/j.ejsobi.2009.03.002
Xu, T, Zhou, Q, Chen, W, Zhang, G, He, G, Gu, D and Zhang, W (2003) Involvement of jasmonate-signaling pathway in the herbivore-induced rice plant defense. Chinese Science Bulletin 48, 19821987.10.1007/BF03183991
Zhang, Y, Xie, Y, Xue, J, Peng, G and Wang, X (2009) Effect of volatile emissions, especially alpha-pinene, from persimmon trees infested by Japanese wax scales or treated with methyl jasmonate on recruitment of ladybeetle predators. Environmental Entomology 38, 14391445.10.1603/022.038.0512

Keywords

Exogenous application of methyl jasmonate to Ficus hahliana attracts predators of insects along an altitudinal gradient in Papua New Guinea

  • Anna Mrazova (a1) (a2) and Katerina Sam (a1) (a2)

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