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

Published online by Cambridge University Press:  06 May 2019

Anna Mrazova Open the ORCID record for Anna Mrazova [Opens in a new window]  and
Katerina Sam Open the ORCID record for Katerina Sam [Opens in a new window]
Anna Mrazova
Affiliation:
Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic Biology Centre, CAS, Institute of Entomology, Ceske Budejovice, Czech Republic
Katerina Sam*
Affiliation:
Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic Biology Centre, CAS, Institute of Entomology, Ceske Budejovice, Czech Republic
*
*Email: katerina.sam.cz@gmail.com
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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.

Keywords

Herbivore-induced plant volatileHIPVmethyl jasmonatemultitrophic interactionsplasticine caterpillarspredatorstropical gradient
Type
Research Article
Information
Journal of Tropical Ecology , Volume 35 , Issue 4 , July 2019 , pp. 157 - 164
Copyright
© Cambridge University Press 2019 

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References

Literature cited

Agrawal, AA (1998) Leaf damage and associated cues induce aggressive ant recruitment in a neotropical ant-plant. Ecology 79, 2100–2112.10.1890/0012-9658(1998)079[2100:LDAACI]2.0.CO;2CrossRefGoogle Scholar
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, 1348–1355.10.1111/ele.12177CrossRefGoogle ScholarPubMed
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, 8113–8118.10.1073/pnas.95.14.8113CrossRefGoogle ScholarPubMed
Cipollini, D, Purrington, CB and Bergelson, J (2003) Costs of induced responses in plants. Basic and Applied Ecology 4, 79–89.10.1078/1439-1791-00134CrossRefGoogle Scholar
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, 1009–1022.10.1111/ele.12640CrossRefGoogle ScholarPubMed
De Moraes, CM, Lewis, WJ, Pare, PW, Alborn, HT and Tumlinson, JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393, 570–573.10.1038/31219CrossRefGoogle Scholar
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, 1907–1922.10.1023/A:1020942102181CrossRefGoogle Scholar
Felton, GW and Korth, KL (2000) Trade-offs between pathogen and herbivore resistance. Current Opinion in Plant Biology 3, 309–314.10.1016/S1369-5266(00)00086-8CrossRefGoogle ScholarPubMed
Gill, F and Donsker, D (eds) (2019) IOC World Bird List (v9.1). doi: 10.14344/IOC.ML.9.1. https://www.worldbirdnames.org/.CrossRefGoogle Scholar
Heil, M (2014) Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytologist 204, 297–306.10.1111/nph.12977CrossRefGoogle Scholar
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, 146–150.10.1016/0014-5793(94)00948-1CrossRefGoogle ScholarPubMed
Hothorn, T, Bretz, F and Westfall, P (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.10.1002/bimj.200810425CrossRefGoogle ScholarPubMed
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, 325–329.10.1111/j.1570-7458.2009.00860.xCrossRefGoogle Scholar
Jeanne, RL (1979) A latitudinal gradient in rates of ant predation. Ecology 60, 1211–1224.10.2307/1936968CrossRefGoogle Scholar
Karban, R (2007) Damage to sagebrush attracts predators but this does not reduce herbivory. Entomologia Experimentalis et Applicata 125, 71–80.10.1111/j.1570-7458.2007.00594.xCrossRefGoogle Scholar
Kessler, A and Baldwin, IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141–2144.10.1126/science.291.5511.2141CrossRefGoogle ScholarPubMed
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, 1131–1144.10.1111/eth.12426CrossRefGoogle Scholar
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, 120–126.10.1111/eea.12207CrossRefGoogle Scholar
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, 915–918.10.1111/j.1461-0248.2004.00653.xCrossRefGoogle Scholar
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, 325–330.10.1093/beheco/arm135CrossRefGoogle Scholar
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, 143–153.10.1007/s11829-014-9296-1CrossRefGoogle Scholar
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, 263–271.Google Scholar
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, 1160–1168.10.1104/pp.104.054460CrossRefGoogle ScholarPubMed
Mooney, KA (2007) Tritrophic effects of birds and ants on a canopy food web, tree growth, and phytochemistry. Ecology 88, 2005–2014.10.1890/06-1095.1CrossRefGoogle ScholarPubMed
Mrazova, A and Sam, K (2018) Application of methyl jasmonate to grey willow (Salix cinerea) attracts insectivorous birds in nature. Arthropod–Plant Interactions 12, 1–8.10.1007/s11829-017-9558-9CrossRefGoogle Scholar
Novotny, V and Basset, Y (2005) Host specificity of insect herbivores in tropical forests. Proceedings of the Royal Society B: Biological Sciences 272, 1083–1090.10.1098/rspb.2004.3023CrossRefGoogle ScholarPubMed
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, 27–33.10.1017/S0266467406003671CrossRefGoogle Scholar
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, 679–695.10.1023/A:1010393700918CrossRefGoogle ScholarPubMed
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.2013.00115CrossRefGoogle ScholarPubMed
Romero, GQ and Izzo, TJ (2004) Leaf damage induces ant recruitment in the Amazonian ant-plant Hirtella myrmecophila. Journal of Tropical Ecology 20, 675–682.10.1017/S0266467404001749CrossRefGoogle Scholar
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, 742–744.10.1126/science.aaj1631CrossRefGoogle ScholarPubMed
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, 116–133.Google Scholar
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, 293–300.10.1111/ecog.00979CrossRefGoogle Scholar
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, 317–324.10.1111/eea.12367CrossRefGoogle Scholar
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/srep44018CrossRefGoogle ScholarPubMed
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, 245–269.10.1146/annurev.ecolsys.39.110707.173430CrossRefGoogle Scholar
Schmidt, JO (1990) Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators. Albany, NY: SUNY Press, 502 pp.Google Scholar
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, 512–523.10.1111/jeb.13020CrossRefGoogle Scholar
Takabayashi, J and Dicke, M (1996) Plant–carnivore mutualism through herbivore-induced carnivore attractants. Trends in Plant Science 1, 109–113.10.1016/S1360-1385(96)90004-7CrossRefGoogle Scholar
Thaler, JS (1999) Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature 399, 686–688.10.1038/21420CrossRefGoogle Scholar
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, 1767–1781.10.1007/BF02028503CrossRefGoogle Scholar
Turlings, TC, Humlington, JH and Lewis, WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasite wasps. Science 250, 1251–1253.10.1126/science.250.4985.1251CrossRefGoogle Scholar
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, 331–341.10.1017/S0266467412000235CrossRefGoogle Scholar
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, 8304–8307.10.1073/pnas.1431621100CrossRefGoogle Scholar
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, 928–934.10.1890/06-1976.1CrossRefGoogle ScholarPubMed
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, 301–305.10.1016/j.ejsobi.2009.03.002CrossRefGoogle Scholar
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, 1982–1987.10.1007/BF03183991CrossRefGoogle Scholar
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, 1439–1445.10.1603/022.038.0512CrossRefGoogle ScholarPubMed