Abstract
Evolutionary theory of plant defences against herbivores predicts a trade-off between direct (anti-herbivore traits) and indirect defences (attraction of carnivores) when carnivore fitness is reduced. Such a trade-off is expected in plant species that kill herbivore eggs by exhibiting a hypersensitive response (HR)-like necrosis, which should then negatively affect carnivores. We used the black mustard (Brassica nigra) to investigate how this potentially lethal direct trait affects preferences and/or performances of specialist cabbage white butterflies (Pieris spp.), and their natural enemies, tiny egg parasitoid wasps (Trichogramma spp.). Both within and between black mustard populations, we observed variation in the expression of Pieris egg-induced HR. Butterfly eggs on plants with HR-like necrosis suffered lower hatching rates and higher parasitism than eggs that did not induce the trait. In addition, Trichogramma wasps were attracted to volatiles of egg-induced plants that also expressed HR, and this attraction depended on the Trichogramma strain used. Consequently, HR did not have a negative effect on egg parasitoid survival. We conclude that even within a system where plants deploy lethal direct defences, such defences may still act with indirect defences in a synergistic manner to reduce herbivore pressure.
References
- 1
Schoonhoven LM, van Loon JJA& Dicke M . 2005 Insect–plant biology, 2nd edn. Oxford, UK: Oxford University Press. Google Scholar - 2
Dicke M& Baldwin IT . 2010 The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help.’. Trends Plant Sci. 15, 167–175. (doi:10.1016/j.tplants.2009.12.002). Crossref, PubMed, Web of Science, Google Scholar - 3
Kessler A& Heil M . 2011 The multiple faces of indirect defences and their agents of natural selection. Funct. Ecol. 25, 348–357. (doi:10.1111/j.1365-2435.2010.01818.x). Crossref, Web of Science, Google Scholar - 4
Agrawal AA, Janssen A, Bruin J, Posthumus MA& Sabelis MW . 2002 An ecological cost of plant defence: attractiveness of bitter cucumber plants to natural enemies of herbivores. Ecol. Lett. 5, 377–385. (doi:10.1046/j.1461-0248.2002.00325.x). Crossref, Web of Science, Google Scholar - 5
Heil M& Baldwin IT . 2002 Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci. 7, 61–67. (doi:10.1016/S1360-1385(01)02186-0). Crossref, PubMed, Web of Science, Google Scholar - 6
Strauss SY& Agrawal AA . 1999 The ecology and evolution of plant tolerance to herbivory. Trends Ecol. Evol. 14, 179–185. (doi:10.1016/S0169-5347(98)01576-6). Crossref, PubMed, Web of Science, Google Scholar - 7
Campbell BC& Duffey SS . 1979 Tomatine and parasitic wasps: potential incompatibility of plant antibiosis with biological control. Science 205, 700–702. (doi:10.1126/science.205.4407.700). Crossref, PubMed, Web of Science, Google Scholar - 8
Ballhorn DJ, Kautz S, Lion U& Heil M . 2008 Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). J. Ecol. 96, 971–980. (doi:10.1111/j.1365-2745.2008.01404.x). Crossref, Web of Science, Google Scholar - 9
Dyer L, Dodson C, Beihoffer J& Letourneau D . 2001 Trade-offs in antiherbivore defenses in Piper cenocladum: ant mutualists versus plant secondary metabolites. J. Chem. Ecol. 27, 581–592. (doi:10.1023/a:1010345123670). Crossref, PubMed, Web of Science, Google Scholar - 10
Heil M, Fiala B& Linsenmair KE . 1999 Reduced chitinase activities in ant plants of the genus Macaranga. Naturwissenschaften 86, 146–149. (doi:10.1007/s001140050589). Crossref, Web of Science, Google Scholar - 11
Gols R, Bukovinszky T, van Dam NM, Dicke M, Bullock JM& Harvey JA . 2008 Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations. J. Chem. Ecol. 34, 132–143. (doi:10.1007/s10886-008-9429-z). Crossref, PubMed, Web of Science, Google Scholar - 12
Gols R, Wagenaar R, Bukovinszky T, van Dam NM, Dicke M, Bullock JM& Harvey JA . 2008 Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology 89, 1616–1626. (doi:10.1890/07-0873.1). Crossref, PubMed, Web of Science, Google Scholar - 13
Strauss SY, Rudgers JA, Lau JA& Irwin RE . 2002 Direct and ecological costs of resistance to herbivory. Trends Ecol. Evol. 17, 278–285. (doi:10.1016/S0169-5347(02)02483-7). Crossref, Web of Science, Google Scholar - 14
Koricheva J . 2002 Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83, 176–190. (doi:10.1890/0012-9658(2002)083[0176:maosov]2.0.co;2). Crossref, Web of Science, Google Scholar - 15
Koricheva J& Romero GQ . 2012 You get what you pay for: reward-specific trade-offs among direct and ant-mediated defences in plants. Biol. Lett. 8, 628–630. (doi:10.1098/rsbl.2012.0271). Link, Web of Science, Google Scholar - 16
Barbosa P, Gross P& Kemper J . 1991 Influence of plant allelochemicals on the tobacco hornworm and its parasitoid, Cotesia congregata. Ecology 72, 1567–1575. (doi:10.2307/1940956). Crossref, Web of Science, Google Scholar - 17
Bukovinszky T, Poelman EH, Gols R, Prekatsakis G, Vet LEM, Harvey JA& Dicke M . 2009 Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 160, 299–308. (doi:10.1007/s00442-009-1308-y). Crossref, PubMed, Web of Science, Google Scholar - 18
Bukovinszky T, Gols R, Smid HM, Bukovinszkine Kiss G, Dicke M& Harvey JA . 2012 Consequences of constitutive and induced variation in the host's food plant quality for parasitoid larval development. J. Insect Physiol. 58, 367–375. (doi:10.1016/j.jinsphys.2011.12.017). Crossref, PubMed, Web of Science, Google Scholar - 19
Harvey JA . 2000 Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness. Ecol. Entomol. 25, 267–278. (doi:10.1046/j.1365-2311.2000.00265.x). Crossref, Web of Science, Google Scholar - 20
Ode PJ . 2006 Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu. Rev. Entomol. 51, 163–185. (doi:10.1146/annurev.ento.51.110104.151110). Crossref, PubMed, Web of Science, Google Scholar - 21
Lill JT& Marquis RJ . 2001 The effects of leaf quality on herbivore performance and attack from natural enemies. Oecologia 126, 418–428. (doi:10.1007/s004420000557). Crossref, PubMed, Web of Science, Google Scholar - 22
Agrawal AA . 2011 Current trends in the evolutionary ecology of plant defence. Funct. Ecol. 25, 420–432. (doi:10.1111/j.1365-2435.2010.01796.x). Crossref, Web of Science, Google Scholar - 23
Poelman EH, van Loon JJA& Dicke M . 2008 Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci. 13, 534–541. (doi:10.1016/j.tplants.2008.08.003). Crossref, PubMed, Web of Science, Google Scholar - 24
Benrey B& Denno RF . 1997 The slow-growth-high-mortality hypothesis: a test using the cabbage butterfly. Ecology 78, 987–999. Web of Science, Google Scholar - 25
Pilson D . 1996 Two herbivores and constraints on selection for resistance in Brassica rapa. Evolution 50, 1492–1500. (doi:10.2307/2410886). Crossref, PubMed, Web of Science, Google Scholar - 26
Pilson D . 2000 The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in Brassica rapa. Evol. Ecol. 14, 457–489. (doi:10.1023/A:1010953714344). Crossref, Web of Science, Google Scholar - 27
Agrawal AA . 2007 Macroevolution of plant defense strategies. Trends Ecol. Evol. 22, 103–109. (doi:10.1016/j.tree.2006.10.012). Crossref, PubMed, Web of Science, Google Scholar - 28
Reymond P . 2013 Perception, signaling and molecular basis of oviposition-mediated plant responses. Planta 238, 247–258. (doi:10.1007/s00425-013-1908-y). Crossref, PubMed, Web of Science, Google Scholar - 29
Hilker M& Fatouros NE . Submitted. Plant responses to insect egg deposition. Ann. Rev. Entomol.. Web of Science, Google Scholar - 30
Holland JN& DeAngelis DL . 2002 Ecological and evolutionary conditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproduction. Theor. Pop. Biol. 61, 251–263. (doi:10.1006/tpbi.2001.1571). Crossref, PubMed, Web of Science, Google Scholar - 31
Balbyshev NF& Lorenzen JH . 1997 Hypersensitivity and egg drop: a novel mechanism of host plant resistance to Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 90, 652–657. Crossref, Web of Science, Google Scholar - 32
Fatouros NE, Lucas-Barbosa D, Weldegergis BT, Pashalidou FG, van Loon JJA, Dicke M, Harvey JA, Gols R& Huigens ME . 2012 Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS ONE 7, e43607. (doi:10.1371/journal.pone.0043607). Crossref, PubMed, Web of Science, Google Scholar - 33
Petzold-Maxwell J, Wong S, Arellano C& Gould F . 2011 Host plant direct defence against eggs of its specialist herbivore, Heliothis subflexa. Ecol. Entomol. 36, 700–708. (doi:10.1111/j.1365-2311.2011.01315.x). Crossref, Web of Science, Google Scholar - 34
Shapiro AM& De Vay JE . 1987 Hypersensitivity reaction of Brassica nigra L. (Cruciferae) kills eggs of Pieris butterflies (Lepidoptera, Pieridae). Oecologia 71, 631–632. (doi:10.1007/BF00379310). Crossref, PubMed, Web of Science, Google Scholar - 35
Doss RP, Oliver JE, Proebsting WM, Potter SW, Kuy SR, Clement SL, Williamson RT, Carney JR& DeVilbiss ED . 2000 Bruchins: insect-derived plant regulators that stimulate neoplasm formation. Proc. Natl Acad. Sci. USA 97, 6218–6223. (doi:10.1073/pnas.110054697). Crossref, PubMed, Web of Science, Google Scholar - 36
Desurmont GA& Weston PA . 2011 Aggregative oviposition of a phytophagous beetle overcomes egg-crushing plant defences. Ecol. Entomol. 36, 335–343. (doi:10.1111/j.1365-2311.2011.01277.x). Crossref, Web of Science, Google Scholar - 37
Seino Y, Suzuki Y& Sogawa K . 1996 An ovicidal substance produced by rice plants in response to oviposition by the whitebacked planthopper, Sogatella furcifera (Horvath) (Homoptera: Delphacidae). Appl. Entomol. Zool. 31, 467–473. Crossref, Web of Science, Google Scholar - 38
Seino Y& Suzuki Y . 1997 Biotransformation of benzyl benzoate from benzoic acid in rice watery ovipositional lesion tissues induced by Sogatella furcifera (HORVATH) (Homoptera, Delphacidae). Appl. Entomol. Zool. 32, 530–532. Crossref, Web of Science, Google Scholar - 39
Fatouros NE, Dicke M, Mumm R, Meiners T& Hilker M . 2008 Foraging behavior of egg parasitoids exploiting chemical information. Behav. Ecol. 19, 677–689. (doi:10.1093/beheco/arn011). Crossref, Web of Science, Google Scholar - 40
Bos F, Bosveld M, Groenendijk D, van Swaay C& Wynhoff I . 2006 De Dagvlinders van Nederland: Vespreiding en Bescherming, p. 381. Utrecht, The Netherlands: KNNV Uitgeverij. Google Scholar - 41
Feltwell J . 1982 Large white butterfly: the biology, biochemistry and physiology of Pieris brassicae (Linnaeus). The Hague, The Netherlands: Dr. W. Junk Publishers. Google Scholar - 42
Consoli FL, Parra JRP& Zucchi R . 2010 Egg parasitoids in agroecosystems with emphasis on Trichogramma. Dordrecht, The Netherlands: Springer. Crossref, Google Scholar - 43
Little D, Gouhier-Darimont C, Bruessow F& Reymond P . 2007 Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol. 143, 784–800. (doi:10.1104/pp.106.090837). Crossref, PubMed, Web of Science, Google Scholar - 44
Fatouros NE& Huigens ME . 2012 Phoresy in the field: natural occurrence of Trichogramma egg parasitoids on butterflies and moths. BioControl 57, 493–502. (doi:10.1007/s10526-011-9427-x). Crossref, Web of Science, Google Scholar - 45
Pineda A, Zheng SJ, van Loon JJA& Dicke M . 2012 Rhizobacteria modify plant–aphid interactions: a case of induced systemic susceptibility. Plant Biol. 14, 83–90. (doi:10.1111/j.1438-8677.2011.00549.x). Crossref, PubMed, Web of Science, Google Scholar - 46
Jolivet C& Bernasconi G . 2006 Experimental analysis of constitutive and induced defence in a plant–seed–predator system. Funct. Ecol. 20, 966–972. (doi:10.1111/j.1365-2435.2006.01196.x). Crossref, Web of Science, Google Scholar - 47
Smallegange RC, Loon JJA, Blatt SE, Harvey JA, Agerbirk N& Dicke M . 2007 Flower vs. leaf feeding by Pieris brassicae: glucosinolate-rich flower tissues are preferred and sustain higher growth rate. J. Chem. Ecol. 33, 1831–1844. (doi:10.1007/s10886-007-9350-x). Crossref, PubMed, Web of Science, Google Scholar - 48
Lucas-Barbosa D, van Loon JJA, Gols R, van Beek TA& Dicke M . 2013 Reproductive escape: annual plant responds to butterfly eggs by accelerating seed production. Funct. Ecol. 27, 245–254. (doi:10.1111/1365-2435.12004). Crossref, Web of Science, Google Scholar - 49
Hopkins RJ, van Dam NM& van Loon JJ . 2009 Role of glucosinolates in insect–plant relationships and multitrophic interactions. Annu. Rev. Entomol. 54, 57–83. (doi:10.1146/annurev.ento.54.110807.090623). Crossref, PubMed, Web of Science, Google Scholar - 50
Harvey JA& Gols R . 2011 Development of Mamestra brassicae and its solitary endoparasitoid Microplitis mediator on two populations of the invasive weed Bunias orientalis. Popul. Ecol. 53, 587–596. (doi:10.1007/s10144-011-0267-4). Crossref, Web of Science, Google Scholar - 51
Santolamazza-Carbone S, Velasco P, Soengas P& Cartea M . 2013 Bottom-up and top-down herbivore regulation mediated by glucosinolates in Brassica oleracea var. acephala. Oecologia 174, 893–907. (doi:10.1007/s00442-013-2817-2). Crossref, PubMed, Web of Science, Google Scholar - 52
Steppuhn A& Baldwin IT . 2008 Induced defenses and the cost–benefit paradigm. Induced plant resistance to herbivory (ed.& Schaller A ), pp. 61–83. Dordrecht, The Netherlands: Springer. Crossref, Google Scholar - 53
Berenbaum M& Neal JJ . 1985 Synergism between myristicin and xanthotoxin, a naturally coocurring plant toxicant. J. Chem. Ecol. 11, 1349–1358. (doi:10.1007/BF01012136). Crossref, PubMed, Web of Science, Google Scholar - 54
Rasmann S& Agrawal AA . 2009 Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Curr. Opin. Plant Biol. 12, 473–478. (doi:10.1016/j.pbi.2009.05.005). Crossref, PubMed, Web of Science, Google Scholar - 55
Rasmann S, Erwin AC, Halitschke R& Agrawal AA . 2011 Direct and indirect root defences of milkweed (Asclepias syriaca): trophic cascades, trade-offs and novel methods for studying subterranean herbivory. J. Ecol. 99, 16–25. (doi:10.1111/j.1365-2745.2010.01713.x). Crossref, Web of Science, Google Scholar - 56
Vrieling K& Wijk CM . 1992 Estimating costs and benefits of the pyrrolizidine alkaloids of Senecio jacobaea under natural conditions.Proc. 8th Int. Symp. on Insect–Plant Relationships (eds, Menken SBJ, Visser JH& Harrewijn P ), Wageningen, The Netherlands, August, pp. 77–78. Dordrecht, The Netherlands: Springer. Crossref, Google Scholar