THE POTENTIAL OF PLANTS TO MEDIATE THE INTERACTION BETWEEN HERBIVORY AND POLLINATION
DOI:
https://doi.org/10.4257/oeco.2018.2204.01Palavras-chave:
floral traits, herbivory costs, induced responses, pollinator attraction, trait-mediated indirect interactionsResumo
Herbivory may affect important plant traits that mediate the interaction with floral visitors and potential pollinators with consequences to fruit and seed production. These may occur through varied mechanisms, ranging from a trade-off in resource allocation for defense and reproduction, to pleiotropic effects in the biosynthesis of secondary compounds for plant defense and floral attractiveness. The subject has been receiving attention and is leading to new perspectives in the study of ecology and evolution of insect-plant interactions. Here our main goal is to briefly review the scientific literature and discuss theoretical aspects of plant mediation of interactions between herbivores and pollinators. We conducted an extensive but non-systematic search for literature on the main theme “effects of herbivory on floral visitors and pollination”. We found experimental studies and reviews reporting that foliar and floral herbivory usually change floral traits that mediate plant-pollinator interactions. The effect of herbivores on floral visitation tend to be neutral or negative, and does not always lead to negative impacts on seed production. These results open a path for new hypotheses on how plants may avoid or compensate for possible ecological costs of herbivory. We suggest that future studies should explore finer mechanisms through which herbivory affects pollination by considering natural history, pollination effectiveness, and the chemical background upon which flowers are presented to pollinators. Such studies will improve our understanding of how indirect effects structure ecological communities and their role in the evolution of plant-animal interactions.
Referências
Abrams, P. A., Menge, B. A., Mittelbach, G. G., Spiller, D. A., & Yodzis, P. 1996. The role of indirect effects in food webs. In: G. A. Polis & K. O. Winemiller (Eds.), Food webs: integration of patterns and dynamics. pp 371–395. US: Springer.
Adler, L. S., & Irwin, R. E. 2005. Ecological costs and benefits of defenses in nectar. Ecology, 86(11), 2968–2978. DOI: 10.1890/05-0118
Adler, L. S. 2008. Selection by pollinators and herbivores on attraction and defense. In: K. J. Tilmon (Ed.), Specialization, speciation, and radiation: The Evolutionary Biology of Herbivores Insects. pp 162–173. US: University of California Press.
Adler, L. S., Wink, M., Distl, M., & Lentz, A. J. 2006. Leaf herbivory and nutrients increase nectar alkaloids. Ecology Letters, 9(8), 960–967. DOI: 10.1111/j.1461-0248.2006.00944.x
Agrawal, A. A., & Karban, R. 1999. Why induced defenses may be favored over constitutive strategies in plants. In: R. Tollrian & C. D. Harvell (Eds.), The Ecology and Evolution of Inducible Defenses. pp. 5–61. US: Princeton University Press.
Agrawal, A. A., & Rutter, M. T. 1998. Dynamic anti-herbivore defense in ant-plants: the role of induced responses. Oikos, 83(2), 227–236. DOI: 10.2307/3546834
Aizen, M. A., & Raffaele, E. 1996. Nectar production and pollination in Alstroemeria aurea: responses to level and pattern of flowering shoot defoliation. Oikos, 76(2), 312–322. DOI: 10.2307/3546203
Almeida-Soares, S., Polatto, L. P., Dutra, J., & Torezan-Silingardi, H. M. 2010. Pollination of Adenocalymma bracteatum (Bignoniaceae): floral biology and visitors. Neotropical Entomology, 39(6), 941–948. DOI: 10.1590/S1519-566X2010000600015
Althoff, D. M., & Segraves, K. A. 2016. Mutualism, the evolutionary ecology of. In: Encyclopedia of evolutionary biology. pp. 87–93. Elsevier.
Armbruster, W. S. 1997. Exaptations link evolution of plant-herbivore and plant-pollinator interactions: a phylogenetic inquiry. Ecology, 78(6), 1661–1672. DOI: 10.2307/2266091
Armbruster, W. S., Howard, J. J., Clausen, T. P., Debevec, E. M., Loquvam, J. C., Matsuki, M., Cerendolo, B., & Andel, F. 1997. Do biochemical expectation link evolution of plant defense and pollination systems? Historical hypotheses and experimental tests with Dalechampia vines. The American Naturalist, 149(3), 461–484. DOI: 10.1086/286000
Begon, M., Harpper, J. L., & Townsend, C. R (Eds.). 2007. Ecologia: de indivíduos a ecossistemas. 4 ed. Porto Alegre, RS: Artmed: p. 752.
Beker, R., Dafni, A., Eisikowitch, D., & Ravid, U. 1989. Volatiles of two chemotypes of Majorana syriaca L.(Labiatae) as olfactory cues for the honeybee. Oecologia, 79(4), 446–451. DOI: 10.1007/BF00378659
Belsky, A. J. 1986. Does herbivory benefit plants? A review of the evidence. The American Naturalist, 127(6), 870–892. DOI: 10.1086/284531
Bergelson, J., & Purrington, C. B. 1996. Surveying patterns in the cost of resistance in plants. The American Naturalist, 148(3), 536–558. DOI: 10.1086/285938
Bertness, M. D., Wise, C., & Ellison, A. M. 1987. Consumer pressure and seed set in a salt marsh perennial plant community. Oecologia 71(2), 190–200. DOI: 10.1007/BF00377284
Boege, K., & Marquis, R. J. 2005. Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology & Evolution, 20(8), 441–448. DOI: 10.1016/j.tree.2005.05.001
Bostock, R. M. 2005. Signal Crosstalk and induced resistance: straddling the line between cost and benefit. Annual Review of Phytopathology, 43(1), 545–580. DOI: 10.1146/annurev.phyto.41.05200
095505
Bronstein, J. D., Huxman, T. E., & Davidowitz, G. 2007. Plant-mediated effects linking herbivory and pollination. In: T. Ohgushi, T. P. Craig & P. W. Price (Eds.). Ecological communities: plant mediation in indirect interaction webs. pp. 75–103. UK: Cambridge University Press.
Bruce, T. J. A., & Pickett, J. A. 2011. Perception of plant volatile blends by herbivorous insects: finding the right mix. Phytochemistry, 72(13), 1605–1611. DOI: 10.1016/j.phytochem.2011.04.011
Buchanan, A. L., & Underwood, N. 2013. Attracting pollinators and avoiding herbivores: insects influence plant traits within and across years. Oecologia, 173(2), 473–482. DOI: 10.1007/s00442-013-2629-4
Caissard, J.-C., Meekijjironenroj, A., Baudino, S., & Anstett, M.-C. 2004. Localization of production and emission of pollinator attractant on whole leaves of Chamaerops humilis (Arecaceae). American Journal of Botany, 91(8), 1190–1199. DOI: 10.3732/ajb.91.8.1190
Cardel, Y. J., & Koptur, S. 2010. Effects of florivory on the pollination of flowers: an experimental field study with a perennial plant. International Journal of Plant Sciences, 171(3), 283–292. DOI: 10.1086/650154
Castro, S., Loureiro, J., Ferrero, V., Silveira, P., & Navarro, L. 2013. So many visitors and so few pollinators: variation in insect frequency and effectiveness governs the reproductive success of an endemic milkwort. Plant Ecology, 214(10), 1233–1245. DOI: 10.1007/s11258-013-0247-1
Cook, J. M., Rasplus, J. Y. 2003. Mutualisms with attitude: coevolving fig wasps and figs. Trends in Ecology and Evolution 18(5), 241–248. DOI: 10.1016/S0169-5347(03)00062-4
Cozzolino, S., Fineschi, S., Litto, M., Scopece, G., Trunschke, J., & Schiestl, F. P. 2015. Herbivory increases fruit set in Silene latifolia: a consequence of induced pollinator-attracting floral volatiles? Journal of Chemical Ecology, 41(7), 622–630. DOI: 10.1007/s10886-015-0597-3
Crawley, M. J. 1993. Herbivory: the dynamics of animal-plant intercations. Oxford, UK: Blackwell Scientific Publications: p. 437.
Danell, K., & Bergström, R. 2002. Mammalian herbivory in terrestrial environments. In: C. M. Herrera & O. Pellmyr (Eds.), Plant animal interactions: an evolutionary approach. pp. 328. US: Wiley-Blackwell.
Del-Claro, K., & Torezan-Silingardi, H. M. 2009. Insect-plant interactions: new pathways to a better comprehension of ecological communi-ties in Neotropical savannas. Neotropical Entomology, 38(2), 159–164. DOI: 10.1590/S1519-566X200900020000
Denno, R. F., McClure, M. S., & Ott, J. R. 1995. Interspecific interactions in phytophagous insects: competition reexamined and resur-rected. Annual Review of Entomology, 40(1), 297–331. DOI: 10.1146/annurev.en.40.010195.001501
Denno, R. F. & Kaplan, I. 2007. Plant-mediated interactions in herbivorous insects: mechanisms, symmetry, and challenging the paradigms of competition past. In: T. Ohgushi, T. P. & Craig, P. W. Price (Eds.). Ecological communities: plant mediation in indirect interaction webs. pp. 19–50. UK: Cambridge University Press.
Dicke, M., & Baldwin, I. T. 2010. The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help.’ Trends in Plant Science, 15(3), 167–175. DOI: 10.1016/j.tplants.2009.12.002
Dicke, M. 2016. Induced plant volatiles: plant body odours structuring ecological networks. New Phytologist, 210(1), 10–12. DOI: 10.1111/nph.13896
Dufaÿ, M., Hossaert-McKey, M., & Anstett, M. C. 2003. When leaves act like flowers: how dwarf palms attract their pollinators. Ecology Letters, 6(1), 28–34. DOI: 10.1046/j.1461-0248.2003.00382.x
Effmert, U., Dinse, C., & Piechulla, B. 2008. Influence of green leaf herbivory by Manduca sexta on floral volatile emission by Nicotiana suaveolens. Plant Physiology, 146(4), 1996–2007. DOI: 10.1104/pp.107.112326
Fatouros, N. E., Lucas-Barbosa, D., Weldegergis, B. T., Pashalidou, F. G., van Loon, J. J. A., Dicke, M., Harvey, J. A., Gols, R., & Huigens, M. E. 2012. Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS ONE, 7(8), e43607. DOI: 10.1371/journal.pone.0043607
Ferreira, C. A., & Torezan-Silingardi, H. M. 2013. Implications of the floral herbivory on Malpighiacea plant fitness: visual aspect of the flower affects the attractiveness to pollinators. Sociobiology, 60(3). DOI: 10.13102/sociobiology.v60i3.323-328
Fineblum, W. L., & Rausher, M. D. 1997. Do floral pigmentation genes also influence resistance to enemies? The W locus in Ipomoea purpurea. Ecology, 78(6), 1646. DOI: 10.2307/2266089
Fornoni, J., Núñez-Farfán, J., & Valverde, P. L. 2003. Evolutionary ecology of tolerance to herbivory: advances and perspectives. Comments on Theoretical Biology, 8(6), 643–663. DOI: 10.1080/713713331
Foster, K. R., & Wenseleers, T. 2006. A general model for the evolution of mutualisms. Journal of Evolutionary Biology, 19(4), 1283–1293. DOI: 10.1111/j.1420-9101.2005.01073.x
Freeman, R. S., Brody, A. K., & Neefus, C. D. 2003. Flowering phenology and compensation for herbivory in Ipomopsis aggregata. Oecologia, 136(3), 394–401. DOI: 10.1007/s00442-003-1276-6
Hairston, N. G., Smith, F. E., & Slobodkin, L. B. 1960. Community structure, population control, and competition. The American Naturalist, 94 (879), 421–425. DOI: 10.1086/282146
Heil, M. 2011. Plant-mediated interactions between above- and below-ground communi-ties at multiple trophic levels. Journal of Ecology, 99(1), 3–6. DOI: 10.1111/j.1365-2745.2010.01773.x
Herms, D. A., & Mattson, W. J. 1992. The dilemma of plants: to grow or defend. The Quarterly Review of Biology, 67(3), 283–335. DOI: 10.1086/417659
Hoffmeister, M., Wittköpper, N., & Junker, R. R. 2016. Herbivore-induced changes in flower scent and morphology affect the structure of flower–visitor networks but not plant repro-duction. Oikos, 125(9), 1241–1249. DOI: 10.1111/oik.02988
Holst, B. P. 1909. The teachers' and pupils' cyclopaedia. Kansas City: The Bufton Book Company: p. 404.
Howe, G. A., & Jander, G. 2008. Plant immunity to insect herbivores. Annual Review of Plant Biology, 59(1), 41–66. DOI: 10.1146/annurev.arplant.59.032607.092825
Irwin, R. E., Adler, L. S., & Brody, A. K. 2004. The dual role of floral traits: pollinator attraction and plant defense. Ecology, 85(6), 1503–1511. DOI: 10.1890/03-0390
Johnson, M. T. J., Campbell, S. A., & Barrett, S. C. H. 2015. Evolutionary interactions between plant reproduction and defense against herbivores. Annual Review of Ecology, Evolution, and Systematics, 46(1), 191–213. DOI: 10.1146/annu
rev-ecolsys-112414-054215
Junker, R. R., Blüthgen, N., Brehm, T., Binkenstein, J., Paulus, J., Martin Schaefer, H., & Stang, M. 2013. Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Functional Ecology, 27(2), 329–341. DOI: 10.1111/1365-2435.12005
Karban, R., & Baldwin, I. T. 1997. Induced responses to herbivory. Chicago: The University of Chicago Press: p. 330.
Karban, R., & Strauss, S. Y. 1993. Effects of herbivores on growth and reproduction of their perennial host, Erigeron glaucus. Ecology, 74(1), 39–46. DOI: 10.2307/1939499
Karban, R. 2011. The ecology and evolution of induced resistance against herbivores: Induced resistance against herbivores. Functional Ecology, 25(2), 339–347. DOI: 10.1111/j.1365-2435.2010.01789.x
Karban, R. 2015. Plant sensing and communi-cation. Chicago: The University of Chicago Press: p. 240.
Kessler, D., Gase, K., & Baldwin, I. T. 2008. Field experiments with transformed plants reveal the sense of floral scents. Science 29, 321(5893), 1200–1202. DOI: 10.1126/science.1160072
Kessler, A., & Halitschke, R. 2009. Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study. Functional Ecology, 23(5), 901–912. DOI: 10.1111/j.1365-2435.2009.01639.x
Kessler, D., Diezel, C., & Baldwin, I. T. 2010. Changing pollinators as a means of escaping herbivores. Current Biology, 20(3), 237–242. DOI: 10.1016/j.cub.2009.11.071
Kessler, A., & Heil, M. 2011. The multiple faces of indirect defenses and their agents of natural selection. Functional Ecology, 25(2), 348–357. DOI: 10.1111/j.1365-2435.2010.01818.x
Kessler, A., Halitschke, R., & Poveda, K. 2011. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant–pollinator interactions. Ecology, 92(9), 1769–1780. DOI: 10.1890/10-1945.1
Krupnick, G. A., Weis, A. E., & Campbell, D. R. 1999. The consequences of floral herbivory for pollinator service to Isomeris arborea. Ecology, 80(1), 125–134. DOI: 10.2307/176984
Lehtilä, K., & Strauss, S. Y. 1997. Leaf damage by herbivores affects attractiveness to pollinators in wild radish, Raphanus raphanistrum. Oecologia, 111(3), 396–403. DOI: 10.1007/s004420050251
Lemaitre, A. B., Pinto, C. F., & Niemeyer, H. M. 2014. Generalized pollination system: are floral traits adapted to different pollinators? Arthro-pod-Plant Interactions, 8(4), 261–272. DOI: 10.1007/s11829-014-9308-1
Lennartsson, T., Nilsson, P., & Tuomi, J. 1998. Induction of overcompensation in the field gentian, Gentianella campestris. Ecology, 79(3), 1061–1072. DOI: 10.1890/0012-9658(1998)079[1061:IOOITF]2.0.CO;2
Levin, D. A., & Anderson, W. W. 1970. Competition for pollinators between simultaneously flowering species. The American Naturalist, 104(939), 455–467. DOI: 10.1086/282680
Lohman, D. J., Zangerl, A. R., & Berenbaum, M. R. 1996. Impact of floral herbivory by parsnip webworm (Oecophoridae: Depressaria pastinacella Duponchel) on pollination and fitness of wild parsnip (Apiaceae: Pastinaca sativa L.). American Midland Naturalist, 136(2), 407–412. DOI: 10.2307/2426744
Lucas-Barbosa, D., van Loon, J. J. A., & Dicke, M. 2011. The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry, 72(13), 1647–1654. DOI: 10.1016/j.phytochem.2011.03.013
Lucas-Barbosa, D. 2016. Integrating studies on plant–pollinator and plant–herbivore interac-tions. Trends in Plant Science, 21(2), 125–133. DOI: 10.1016/j.tplants.2015.10.013
Mathews. F. S. 1902. Field book of American wild flowers. New York, New York: G. P. Putnam's Sons: p. 601
McCall, A. C., & Irwin, R. E. 2006. Florivory: the intersection of pollination and herbivory. Ecology Letters, 9(12), 1351–1365. DOI: 10.1111/j.1461-0248.2006.00975.x
Mothershead, K., & Marquis, R. J. 2000. Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology, 81(1), 30–40. DOI: 10.2307/177131
Mutikainen, P., & Delph, L. F. 1996. Effects of herbivory on male reproductive success in plants. Oikos, 75(3), 353–358. DOI: 10.2307/3545874
Ohgushi, T., Craig, T. P., & Price, P. W (Eds.). 2007. Ecological communities: plant mediation in indirect interaction webs. Cambridge, UK: Cambridge University Press: p. 444.
Ollerton, J., Winfree, R., & Tarrant, S. 2011. How many flowering plants are pollinated by animals? Oikos, 120(3), 321–326. DOI: 10.1111/j.1600-0706.2010.18644.x
Olsen, K. M. 1997. Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia, 109(1), 114–121. DOI: 10.1007/PL00008811
Padyšáková, E., Bartoš, M., Tropek, R., & Janeček, Š. 2013. Generalization versus specialization in pollination systems: visitors, thieves, and pollinators of Hypoestes aristata (Acanthaceae). PLoS ONE, 8(4), e59299. DOI: 10.1371/journal.pone.0059299
Paige, K. N., & Whitham, T. G. 1987. Overcompensation in the response to mammalian herbivory: the advantage of being eaten. The American Naturalist, 129(3), 407–416. DOI: 10.1086/284645
Paine, R., T. 1980. Food webs: linkage, interaction strength and community infrastructure. The Journal of Animal Ecology, 49(3), 666–685. DOI: 10.2307/4220
Pareja, M., Qvarfordt, E., Webster, B., Mayon, P., Pickett, J., Birkett, M., & Glinwood, R. 2012. Herbivory by a phloem-feeding insect inhibits floral volatile production. PLoS ONE, 7(2), e31971. DOI: 10.1371/journal.pone.0031971
Pellmyr, O., & Thien, L. B. 1986. Insect reproduction and floral fragrances: keys to the evolution of the angiosperms? Taxon, 35(1), 76–85. DOI: 10.2307/1221036
Pellmyr, O. 2003. Yuccas, yucca moths, and coevolution: a review. Annals of the Missouri Botanical Garden, 90(1), 35–55. DOI: 10.2307/3298524
Poveda, K., Steffan-Dewenter, I., Scheu, S., & Tscharntke, T. 2003. Effects of below- and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia, 135(4), 601–605. DOI: 10.1007/s00442-003-1228-1
Poveda, K., Steffan-Dewenter, I., Scheu, S., & Tscharntke, T. 2005. Effects of decomposers and herbivores on plant performance and above-ground plant-insect interactions. Oikos, 108(3), 503–510. DOI: 10.1111/j.0030-1299.2005.13664.x
Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N., Weis, A. E. 1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics, 11(1), 41–65. DOI: 10.1146/annurev.es.11.110180.000353
Quesada, M., Bollman, K., & Stephenson, A. G. 1995. Leaf damage decreases pollen production and hinders pollen performance in Cucurbita texana. Ecology, 76(2), 437–443. DOI: 10.2307/1941202
Raguso, R. A. 2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annual Review of Ecology, Evolution, and Systematics, 39(1), 549–569. DOI: 10.1146/annurev.ecolsys.38.091206.095601
Raguso, R. A. 2009. Floral scent in a whole-plant context: moving beyond pollinator attraction. Functional Ecology, 23(5), 837–840. DOI: 10.1111/j.1365-2435.2009.01643.x
Ramirez, R. A., & Eubanks, M. D. 2016. Herbivore density mediates the indirect effect of herbivores on plants via induced resistance and apparent competition. Ecosphere, 7(2), 1–11. DOI: 10.1002/ecs2.1218
Rech, A. R., & Brito, V. L. G. de. 2012. Mutualismos extremos de polinização: história natural e tenências evolutivas. Oecologia Australis, 16(02), 297–310. DOI: 10.4257/oeco.2012.1602.08
Rech, A. D., Agostini, K., Oliveira, P. E., & Machado, I. C (Eds.). 2014. Biologia da Polinização. Rio de Janeiro, Rio de Janeiro: Editora Projeto Cultural: p. 524.
Richardson, S. C. 2004. Are nectar-robbers mutualists or antagonists? Oecologia, 139(2), 246–254. DOI: 10.1007/s00442-004-1504-8
Schmidt-Büsser, D., von Arx, M., & Guerin, P. M. 2009. Host plant volatiles serve to increase the response of male european grape berry moths, Eupoecilia ambiguella, to their sex pheromone. Journal of Comparative Physiology A, 195(9), 853–864. DOI: 10.1007/s00359-009-0464-1
Schmitz, O. J. 2009. Indirect effects in communi-ties and ecosystems: the role of trophic and nontrophic interactions. In: S. A. Levin. (Ed.). The Princeton Guide to Ecology. pp. 298–295. New Jersey: Princeton University Press.
Schoonhoven L. M, van Loon J. J. A, & Dicke, M. 2005. Insect-plant biology. 2nd. ed. Oxford: Oxford University Press: p. 421.
Simms, E. L., & Bucher, M. A. 1996. Pleiotropic effects of flower-color intensity on herbivore performance on Ipomoea purpurea. Evolution, 50(2), 957–963. DOI: 10.2307/2410871
Srinivasan, M. V. 2010. Honey bees as a model for vision, perception, and cognition. Annual Review of Entomology, 55(1), 267–284. DOI: 10.1146/annurev.ento.010908.164537
Stanton, M. L. 2003. Interacting guilds: moving beyond the pairwise perspective on mutualisms. The American Naturalist, 162(S4), S10–S23. DOI: 10.1086/378646
Strauss, S. Y. 1991. Indirect effects in community ecology: their definition, study and importance. Trends in Ecology and Evolution 6(7), 206–2010. DOI: 10.1016/0169-5347(91)90023-Q
Strauss, S. Y. 1997. Floral characters link herbivores, pollinators, and plant fitness. Ecology, 78(6), 1640–1645. DOI: 10.2307/2266088
Strauss, S. Y., Conner, J. K., & Rush, S. L. 1996. Foliar herbivory affects floral characters and plant attractiveness to pollinators: implications for male and female plant fitness. American Naturalist 147, 1098–1107. DOI: 10.1086/285896
Strauss, S. Y., Siemens, D. H., Decher, M. B., & Mitchell-Olds, T. 1999. Ecological costs of plant resistance to herbivores in the currency of pollination. Evolution, 53(4), 1105–1113. DOI: 10.2307/2640815
Temeles, E. J., Newman, J. T., Newman, J. H., Cho, S. Y., Mazzotta, A. R., & Kress, W. J. 2016. Pollinator competition as a driver of floral divergence: an experimental test. PLOS ONE, 11(1), 1–17, e0146431. DOI: 10.1371/journal.pone.0146431
Terry, J. C. D., Morris, R. J., & Bonsall, M. B. 2017. Trophic interaction modifications: an empirical and theoretical framework. Ecology Letters,20(10), 1219–1230. DOI: 10.1111/ele.12824
Theis, N., Kesler, K., & Adler, L. S. 2009. Leaf herbivory increases floral fragrance in male but not female Cucurbita pepo subsp. texana (Cucurbitaceae) flowers. American Journal of Botany, 96(5), 897–903. DOI: 10.3732/ajb.0800300
Torezan-Silingardi, H. M. 2011. Predatory behavior of Pachodynerus brevithorax (Hymenoptera: Vespidae, Eumeninae) on endophytic herbivore beetles in the Brazilian tropical savanna. Sociobiology, 57(1), 181–189.
Trona, F., Anfora, G., Bengtsson, M., Witzgall, P., & Ignell, R. 2010. Coding and interaction of sex pheromone and plant volatile signals in the antennal lobe of the codling moth Cydia pomonella. Journal of Experimental Biology, 213(24), 4291–4303. DOI: 10.1242/jeb.047365
Utsumi, S., & Ohgushi, T. 2008. Host plant variation in plant-mediated indirect effects: moth boring-induced susceptibility of willows to a specialist leaf beetle. Ecological Entomology, 33(2), 250–260. DOI: 10.1111/j.1365-2311.2007.00959.x
Utsumi, S., Ando, Y., & Miki, T. 2010a. Linkages among trait-mediated indirect effects: a new framework for the indirect interaction web. Population Ecology, 52(4), 485–497. DOI: 10.1007/s10144-010-0237-2
Utsumi, S., Kishida, O., & Ohgushi, T. 2010b. Trait-mediated indirect interactions in ecological communities. Population Ecology, 52(4), 457–459. DOI: 10.1007/s10144-010-0236-3
Werner, E. E., & Peacor, S. D. 2003. A review of trait-mediated indirect interactions in ecological communities. Ecology, 84(5), 1083–1100. DOI: 10.1890/0012-9658(2003)084[1083:AROTII]2.0.CO;2
Whitney, W. D. 1902. The century dictionary, an encyclopedic lexicon of the english language. New York: The Century Co, I (316).
Willmer, P. (Ed.). 2011. Pollination and floral ecology. Princeton, New Jersey: Princeton University Press: p.778.
Wootton, J. T. 1994a. The nature and consequences of indirect effects in ecological communities. Annual Review of Ecology and Systematics, 25(1), 443–466. DOI: 10.1146/annurev.es.25.110194.002303
Wootton, J. T. 1994b. Putting the pieces together: testing the independence of interactions among organisms. Ecology, 75(6), 1544–1551. DOI: 10.2307/1939615
Zangerl, A. R., & Berenbaum, M. R. 2009. Effects of florivory on floral volatile emissions and pollination success in the wild parsnip. Arthropod-Plant Interactions, 3(3), 181–191. DOI: 10.1007/s11829-009-9071-x
