Herbivore-Specific, Density-Dependent Induction of Plant Volatiles: Honest or “Cry Wolf” Signals?

Plants release volatile chemicals upon attack by herbivorous arthropods. They do so commonly in a dose-dependent manner: the more herbivores, the more volatiles released. The volatiles attract predatory arthropods and the amount determines the probability of predator response. We show that seedlings of a cabbage variety (Brassica oleracea var. capitata, cv Shikidori) also show such a response to the density of cabbage white (Pieris rapae) larvae and attract more (naive) parasitoids (Cotesia glomerata) when there are more herbivores on the plant. However, when attacked by diamondback moth (Plutella xylostella) larvae, seedlings of the same variety (cv Shikidori) release volatiles, the total amount of which is high and constant and thus independent of caterpillar density, and naive parasitoids (Cotesia vestalis) of diamondback moth larvae fail to discriminate herbivore-rich from herbivore-poor plants. In contrast, seedlings of another cabbage variety of B. oleracea (var. acephala: kale) respond in a dose-dependent manner to the density of diamondback moth larvae and attract more parasitoids when there are more herbivores. Assuming these responses of the cabbage cultivars reflect behaviour of at least some genotypes of wild plants, we provide arguments why the behaviour of kale (B. oleracea var acephala) is best interpreted as an honest signaling strategy and that of cabbage cv Shikidori (B. oleracea var capitata) as a “cry wolf” signaling strategy, implying a conflict of interest between the plant and the enemies of its herbivores: the plant profits from being visited by the herbivore's enemies, but the latter would be better off by visiting other plants with more herbivores. If so, evolutionary theory on alarm signaling predicts consequences of major interest to students of plant protection, tritrophic systems and communication alike.

[1]  S. Dorn,et al.  Genetic Variation in Behavioral Response to Herbivore-Infested Plants in the Parasitic Wasp, Cotesia glomerata (L.) (Hymenoptera: Braconidae) , 2004, Journal of Insect Behavior.

[2]  J. Takabayashi,et al.  Induced production of extrafloral nectar in intact lima bean plants in response to volatiles from spider mite-infested conspecific plants as a possible indirect defense against spider mites , 2006, Oecologia.

[3]  A. Aharoni,et al.  Genetic Engineering of Terpenoid Metabolism Attracts Bodyguards to Arabidopsis , 2005, Science.

[4]  L. Packer,et al.  Complementary sex determination substantially increases extinction proneness of haplodiploid populations. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Vincent A. A. Jansen,et al.  Global persistence despite local extinction in acarine predator-prey systems: Lessons from experimental and mathematical exercises. , 2005 .

[6]  T. Maeda,et al.  The effects of rearing conditions on the olfactory response of predatory mites, Phytoseiulus persimilis and Amblyseius womersleyi (Acari: Phytoseiidae). , 2000 .

[7]  M. Sabelis,et al.  Nonequilibrium Population Dynamics of “Ideal and Free” Prey and Predators , 1999, The American Naturalist.

[8]  Yosiaki Itǒ,et al.  Population fluctuations of the diamondback moth,Plutella xylostella (L.) on cabbages inBacillus thuringiensis sprayed and non sprayed plots and factors affecting within-generation survival of immatures , 1988, Researches on Population Ecology.

[9]  A. C. Lewis,et al.  Insect Learning: Ecology and Evolutinary Perspectives , 1993 .

[10]  W. Lewis,et al.  Exploitation of Herbivore-Induced Plant Odors by Host-Seeking Parasitic Wasps , 1990, Science.

[11]  J. Takabayashi,et al.  Oviposition preferences of herbivores are affected by tritrophic interaction webs , 2002 .

[12]  T. Nishioka,et al.  Changing green leaf volatile biosynthesis in plants: An approach for improving plant resistance against both herbivores and pathogens , 2006, Proceedings of the National Academy of Sciences.

[13]  J. Takabayashi,et al.  Effects of specialist parasitoids on oviposition preference of phytophagous insects: encounter–dilution effects in a tritrophic interaction , 2003 .

[14]  Christine Woodcock,et al.  Intercropping increases parasitism of pests , 1997, Nature.

[15]  Pieris rapae (Ledidoptera : Pieridae) females avoid oviposition on Rorippa indica plants infested by conspecific larvae , 1999 .

[16]  L. Schoonhoven Host-marking pheromones in lepidoptera, with special reference to twoPieris spp , 1990, Journal of Chemical Ecology.

[17]  T. Nishioka,et al.  A comparison of the responses of Tetranychus urticae (Acari : Tetranychidae) and Phytoseiulus persimilis (Acari : Phytoseiidae) to volatiles emitted from lima bean leaves with different levels of damage made by T. urticae or Spodoptera exigua (Lepidoptera : Noctuidae) , 2003 .

[18]  M. Zalucki,et al.  Development and Survival of the Diamondback Moth (Lepidoptera: Plutellidae) at Constant and Alternating Temperatures , 2002 .

[19]  M. Sabelis,et al.  How Plants Obtain Predatory Mites as Bodyguards , 1987 .

[20]  Vincent A. A. Jansen,et al.  Common language or Tower of Babel? On the evolutionary dynamics of signals and their meanings , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[21]  M. Sabelis,et al.  Fitness consequences of food-for-protection strategies in plants , 2005 .

[22]  M. Sabelis,et al.  Coevolution of Patch Selection Strategies of Predator and Prey and the Consequences for Ecological Stability , 1993, The American Naturalist.

[23]  Maurice W. Sabelis,et al.  Should all plants recruit bodyguards? : conditions for a polymorphic ESS of synomone production in plants , 1988 .

[24]  T. Mitsunaga,et al.  Influence of food supply on longevity and parasitization ability of a larval endoparasitoid, Cotesia plutellae (Hymenoptera : Braconidae) , 2004 .

[25]  J. H. Tumlinson,et al.  Herbivore-infested plants selectively attract parasitoids , 1998, Nature.

[26]  M. Sabelis,et al.  Plant strategies of manipulating predatorprey interactions through allelochemicals: Prospects for application in pest control , 1990, Journal of Chemical Ecology.

[27]  M. Sabelis,et al.  Response of a phytoseiid predator to herbivore-Induced plant volatiles: Selection on attraction and effect on prey exploitation , 1997, Journal of Insect Behavior.

[28]  R. May,et al.  Aggregation of Predators and Insect Parasites and its Effect on Stability , 1974 .

[29]  J. Takabayashi,et al.  Herbivore-species-specific interactions between crucifer plants and parasitic wasps (Hymenoptera: Braconidae) that are mediated by infochemicals present in areas damaged by herbivores , 2000 .

[30]  L. Beukeboom,et al.  Single locus complementary sex determination in Hymenoptera: an "unintelligent" design? , 2006, Frontiers in Zoology.

[31]  John H. Loughrin,et al.  How caterpillar-damaged plants protect themselves by attracting parasitic wasps. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[32]  B. Sznajder,et al.  Ecology meets plant physiology: herbivore-induced plant responses and their indirect effects on arthropod communities , 2007 .

[33]  Takayuki Ohgushi,et al.  Ecological communities: Plant mediation in indirect interaction webs , 2007 .

[34]  Shu-Sheng Liu,et al.  Cotesia plutellae parasitizing Plutella xylostella: Host-age dependent parasitism and its effect on host development and food consumption , 2002, BioControl.

[35]  Diamondback moth females oviposit more on plants infested by non‐parasitised than by parasitised conspecifics , 2008 .

[36]  R. Charlton,et al.  Genetic variation in foraging traits among inbred lines of a predatory mite , 2002, Heredity.

[37]  Toshiharu Tanaka,et al.  Biological characteristics of a larval endoparasitoid, Cotesia plutellae (Hymenoptera : Braconidae) : Host stage preference, subsequent sex ratio of progeny and mate location of males , 1999 .

[38]  T. Maeda,et al.  Variation in the olfactory response of 13 populations of the predatory mite Amblyseius womersleyi to Tetranychus urticae-infested plant volatiles (Acari: Phytoseiidae, Tetranychidae). , 2001, Experimental & applied acarology.

[39]  V. Jansen,et al.  Altruism through beard chromodynamics , 2006, Nature.

[40]  M. Thomson,et al.  Odour concentration affects odour identity in honeybees , 2005, Proceedings of the Royal Society B: Biological Sciences.

[41]  M. Dicke,et al.  Induction of Direct and Indirect Plant Responses by Jasmonic Acid, Low Spider Mite Densities, or a Combination of Jasmonic Acid Treatment and Spider Mite Infestation , 2003, Journal of Chemical Ecology.

[42]  Allan Stewart-Oaten,et al.  Aggregation by Parasitoids and Predators: Effects on Equilibrium and Stability , 1989, The American Naturalist.

[43]  M. Hassell Parasitism in patchy environments: inverse density dependence can be stabilizing. , 1984, IMA journal of mathematics applied in medicine and biology.

[44]  N. Ohsaki,et al.  Food Plant Choice of Pieris Butterflies as a Trade‐Off between Parasitoid Avoidance and Quality of Plants , 1994 .

[45]  C. Munn Birds that ‘cry wolf’ , 1986, Nature.