Parasitic Wasps Can Reduce Mortality of Teosinte Plants Infested With Fall Armyworm: Support for a Defensive Function of Herbivore-Induced Plant Volatiles

Many parasitic wasps use volatiles emitted by plants under herbivore attack to find their hosts. It has therefore been proposed that these inducible plant volatiles serve an indirect defense function by recruiting parasitoids and other natural enemies. This suggested function remains controversial because there is little evidence that, in terms of fitness, plants benefit from the actions of natural enemies, particularly parasitoids, which do not immediately kill their hosts. We aimed to address this controversy in a semi-natural field experiment in Mexico, where we used large screen tents to evaluate how parasitoids can affect plant performance. The tritrophic study system comprised teosinte (Zea spp.), the ancestor of maize, Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) and Campoletis sonorensis Cameron (Hymenoptera: Ichneumonidae), which have a long evolutionary history together. In tents without parasitoids, S. frugiperda larvae inflicted severe damage to the plants, whereas in the presence of parasitoid wasps, leaf damage was reduced by as much as 80%. Parasitoids also mitigated herbivore-mediated mortality among young teosinte plants. Although these findings will not resolve the long-standing debate on the adaptive function of herbivore-induced plant volatiles, they do present strong support for the hypothesis that plants can benefit from the presence of parasitoid natural enemies of their herbivores.

• Publication year

  2018

• Venue

  Frontiers in Ecology and Evolution

• Publication date

  2018-05-18

• Fields of study

  Biology, Environmental Science

• Identifiers
  DOI 10.3389/fevo.2018.00055
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar

• No claims are published for this paper.

• No concepts are published for this paper.

• Tritrophic Interactions Mediated by Herbivore-Induced Plant Volatiles: Mechanisms, Ecological Relevance, and Application Potential.

  2018cited by this paper
• Fine-tuning the 'plant domestication-reduced defense' hypothesis: specialist vs generalist herbivores.

  2018cited by this paper
• Changes in plant growth and seed production in wild lima bean in response to herbivory are attenuated by parasitoids

  2018cited by this paper
• Domestication impacts on plant–herbivore interactions: a meta-analysis

  2017cited by this paper
• Endure and call for help : Strategies of black mustard plants to deal with a specialized caterpillar

  2017cited by this paper
• Comparing the attraction of two parasitoids to herbivore-induced volatiles of maize and its wild ancestors, the teosintes

  2016cited by this paper
• Fitness consequences of indirect plant defence in the annual weed, Sinapis arvensis

  2015cited by this paper
• Crop domestication and its impact on naturally selected trophic interactions.

  2015cited by this paper
• From induced resistance to defence in plant‐insect interactions

  2015influential reference
• Floral volatiles interfere with plant attraction of parasitoids: ontogeny-dependent infochemical dynamics in Brassica rapa

  2015cited by this paper
• R: A language and environment for statistical computing.

  2014influential reference
• Tritrophic interactions on cultivated maize and its wild ancestor "teosinte"

  2014cited by this paper
• Insect and pathogen attack and resistance in maize and its wild ancestors, the teosintes

  2014cited by this paper
• Herbivore‐induced plant volatiles: targets, perception and unanswered questions

  2014influential reference
• Cannibalism and Virus Production in Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) Larvae Fed with Two Leaf Substrates Inoculated with Baculovirus spodoptera

  2013cited by this paper
• Facilitated by nature and agriculture: performance of a specialist herbivore improves with host-plant life history evolution, domestication, and breeding

  2013cited by this paper
• The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack.

  2013cited by this paper
• Differential Performance and Parasitism of Caterpillars on Maize Inbred Lines with Distinctly Different Herbivore-Induced Volatile Emissions

  2012cited by this paper
• Author response: Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature

  2012influential reference
• Less is More: Treatment with BTH and Laminarin Reduces Herbivore-Induced Volatile Emissions in Maize but Increases Parasitoid Attraction

  2012cited by this paper
• Non‐consumptive effects of a natural enemy on a non‐prey herbivore population

  2012cited by this paper
• Trophic Complexity and the Adaptive Value of Damage-Induced Plant Volatiles

  2012influential reference
• Minor effects of two elicitors of insect and pathogen resistance on volatile emissions and parasitism of Spodoptera frugiperda in Mexican maize fields

  2012cited by this paper
• The origin and dynamic evolution of chemical information transfer

  2011cited by this paper
• Dispensing synthetic green leaf volatiles in maize fields increases the release of sesquiterpenes by the plants, but has little effect on the attraction of pest and beneficial insects.

  2011cited by this paper
• Attractiveness of Constitutive and Herbivore-Induced Sesquiterpene Blends of Maize to the Parasitic Wasp Cotesia marginiventris (Cresson)

  2011cited by this paper
• Ecological role of volatiles produced by plants in response to damage by herbivorous insects.

  2011influential reference
• Current trends in the evolutionary ecology of plant defence

  2011cited by this paper
• The multiple faces of indirect defences and their agents of natural selection

  2011cited by this paper
• The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'.

  2010cited by this paper
• Inhibition of lipoxygenase affects induction of both direct and indirect plant defences against herbivorous insects

  2009cited by this paper
• Learned and naïve natural enemy responses and the interpretation of volatile organic compounds as cues or signals.

  2009cited by this paper
• A Maize (E)-β-Caryophyllene Synthase Implicated in Indirect Defense Responses against Herbivores Is Not Expressed in Most American Maize Varieties[W][OA]

  2008cited by this paper
• Negative interactions between chemical resistance and predators affect fitness in soybeans

  2008cited by this paper
• Identification of seven species of hymenopteran parasitoids of Spodoptera frugiperda, using polymerase chain reaction amplification and restriction enzyme digestion

  2008influential reference
• Plant immunity to insect herbivores.

  2008cited by this paper
• Relative importance of consumptive and non‐consumptive effects of predators on prey and plant damage: the influence of herbivore ontogeny

  2008cited by this paper
• Indirect defence via tritrophic interactions.

  2008cited by this paper
• Parasitoid load affects plant fitness in a tritrophic system

  2008cited by this paper
• Predator Presence Moves Helicoverpa armigera Larvae to Distraction

  2007cited by this paper
• Impact of the Third Trophic Level in an Obligate Mutualism: Do Yucca Plants Benefit from Parasitoids of Yucca Moths?

  2006cited by this paper
• The Role of Indole and Other Shikimic Acid Derived Maize Volatiles in the Attraction of Two Parasitic Wasps

  2006cited by this paper
• Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods.

  2006cited by this paper
• A comparison of naïve and conditioned responses of three generalist endoparasitoids of lepidopteran larvae to host-induced plant odours

  2006cited by this paper
• Tritrophic Interactions and Reproductive Fitness of the Prairie Perennial Silphium laciniatum Gillette (Asteraceae)

  2006cited by this paper
• Fragments of ATP synthase mediate plant perception of insect attack.

  2006influential reference
• Host specificity in arthropod biological control, methods for testing and interpretation of the data

  2006cited by this paper
• The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores.

  2006cited by this paper
• In situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatile organic compounds to parasitic wasps.

  2005cited by this paper
• Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity

  2005influential reference
• A six‐arm olfactometer permitting simultaneous observation of insect attraction and odour trapping

  2004cited by this paper
• The Role of Methyl Salicylate in Prey Searching Behavior of the Predatory Mite Phytoseiulus persimilis

  2004cited by this paper
• High Genetic Variability of Herbivore-Induced Volatile Emission within a Broad Range of Maize Inbred Lines1

  2004cited by this paper
• Occurrence and direct control potential of parasitoids and predators of the fall armyworm (Lepidoptera: Noctuidae) on maize in the subtropical lowlands of Mexico

  2004cited by this paper
• Cascading effects of a specialist parasitoid on plant biomass in a Citrus agroecosystem

  2003cited by this paper
• A single domestication for maize shown by multilocus microsatellite genotyping

  2002cited by this paper
• Site fidelity in habitats with contrasting levels of nest predation and brood parasitism

  2001cited by this paper
• Response of natural populations of predators and parasitoids to artificially induced volatile emissions in maize plants (Zea mays L.)

  2001cited by this paper
• Defensive function of herbivore-induced plant volatile emissions in nature.

  2001influential reference
• Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids

  2001cited by this paper
• Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte)

  2001cited by this paper
• Overcompensation of plants in response to herbivory and the by-product benefits of mutualism.

  2000influential reference
• Parasitoid‐plant mutualism: parasitoid attack of herbivore increases plant reproduction

  2000cited by this paper
• Biology, ecology and use in pest management of Telenomus remus

  2000cited by this paper
• Parasitism of the herbivore Pieris brassicae L. (Lep., Pieridae) by Cotesia glomerata L. (Hym., Braconidae) does not benefit the host plant by reduction of herbivory

  1999cited by this paper
• Attraction of parasitic wasps by caterpillar-damaged plants.

  1999cited by this paper
• Jasmonate-inducible plant defences cause increased parasitism of herbivores

  1999influential reference
• Development of the parasitoid, Cotesia rubecula (Hymenoptera: Braconidae) in Pieris rapae and Pieris brassicae (Lepidoptera: Pieridae): evidence for host regulation.

  1999cited by this paper
• Fitness consequences of cannibalism in the fall armyworm, Spodoptera frugiperda

  1999cited by this paper
• Timing of induced volatile emissions in maize seedlings

  1998cited by this paper
• Herbivore-infested plants selectively attract parasitoids

  1998influential reference
• Induced Responses to Herbivory

  1997cited by this paper
• Parasitism-induced Effects on Host Growth and Metabolic Efficiency in Tobacco Hornworm Larvae Parasitized by Cotesia congregata.

  1997cited by this paper
• An Elicitor of Plant Volatiles from Beet Armyworm Oral Secretion

  1997cited by this paper
• Intercropping increases parasitism of pests

  1997cited by this paper
• Effects of life history, domestication and agronomic selection on plant defence against insects: Evidence from maizes and wild relatives

  1997cited by this paper
• Top-down cascade from a bitrophic predator in an old-field community

  1996cited by this paper
• Innate responses of the parasitoidsCotesia glomerata andC. rubecula (Hymenoptera: Braconidae) to volatiles from different plant-herbivore complexes

  1996cited by this paper
• How caterpillar-damaged plants protect themselves by attracting parasitic wasps.

  1995cited by this paper
• Generalist Predator Consumption of Armyworm (Lepidoptera: Noctuidae) and Effect of Predator Removal on Damage in No-Till Corn

  1994cited by this paper
• Top‐Down Effects in a Tritrophic System: Parasitoids Enhance Plant Fitness

  1994cited by this paper
• Volatile herbivore-induced terpenoids in plant-mite interactions: Variation caused by biotic and abiotic factors

  1994cited by this paper
• Response of the braconid parasitoid Cotesia (=Apanteles) glomerata to volatile infochemicals: effects of bioassay set‐up, parasitoid age and experience and barometric flux

  1992cited by this paper
• Exploitation of Herbivore-Induced Plant Odors by Host-Seeking Parasitic Wasps

  1990cited by this paper
• How Plants Obtain Predatory Mites as Bodyguards

  1987influential reference
• Campoletis sonorensis [Hym.: Ichneumonidae] as a parasitoid ofSpodoptera frugiperda [Lep.: Noctuidae]: Host stage preference and functional response

  1985cited by this paper
• The Fall Army Worm

  1928influential reference

• Targeted Manipulation of a Tomato Terpene Synthase Enhances TMTT-Mediated Attraction of Eretmocerus corni for Sustainable Whitefly Control.

  2026cites this paper
• Plants Anticipating Help: A New Hypothesis in Plant Defence Theory.

  2025cites this paper
• Searching for a common host: parasitoids of Lema daturaphila on Datura stramonium in Central Mexico

  2025cites this paper
• Damage and Entomophagy in Natural Infestations of Spodoptera frugiperda (Lepidoptera: Noctuidae) in Maize Landraces in Oaxaca, Mexico

  2024cites this paper
• Field evidence for the role of plant volatiles induced by caterpillar-derived elicitors in the prey location behavior of predatory social wasps

  2024cites this paper
• Comparative analysis of defensive secondary metabolites in wild teosinte and cultivated maize under flooding and herbivory stress.

  2024cites this paper
• Volatile-mediated plant-plant communication and higher-level ecological dynamics.

  2023cites this paper
• Sustainable management of fall armyworm, Spodoptera frugiperda (J.E. Smith): challenges and proposed solutions from an African perspective

  2022cites this paper
• Conservation Biological Control as an Important Tool in the Neotropical Region

  2022cites this paper
• Tree Communication: the Effects of “Wired” and “Wireless” Channels on Interactions with Herbivores

  2022cites this paper
• Indirect plant defenses: volatile organic compounds and extrafloral nectar

  2021cites this paper
• Evolutionary ecology: Plant volatile profile changes after escaping specialist insects.

  2021cites this paper
• CATERPILLARS SUPPRESS HERBIVORE-INDUCED VOLATILE 3 EMISSIONS IN MAIZE

  2021cites this paper
• Evolutionary changes in an invasive plant support the defensive role of plant volatiles

  2021cites this paper
• Observations on the Relationships between Endophytic Metarhizium robertsii, Spodoptera frugiperda (Lepidoptera: Noctuidae), and Maize

  2021cites this paper
• A comparison of the direct and indirect defence abilities of cultivated maize versus perennial and annual teosintes

  2020cites this paper
• A comparison of the direct and indirect defence abilities of cultivated maize versus perennial and annual teosintes

  2020cites this paper
• Focused Identification of Germplasm Strategy (FIGS): Polishing a rough diamond.

  2020cites this paper
• Arbuscular mycorrhizal fungi (AMF) influences growth and insect community dynamics in Sorghum-sudangrass (Sorghum x drummondii)

  2020cites this paper
• Spodoptera frugiperda Caterpillars Suppress Herbivore-Induced Volatile Emissions in Maize

  2020cites this paper
• Factors influencing the occurrence of fall armyworm parasitoids in Zambia

  2020cites this paper
• Variation in parasitoidism of Protocalliphora azurea (Diptera: Calliphoridae) by Nasonia vitripennis (Hymenoptera: Pteromalidae) in Spain

  2019cites this paper
• Does enhanced nutrient availability increase volatile emissions in cranberry?

  2019cites this paper
• Variation in parasitoidism of Protocalliphora azurea 1 (Diptera: Calliphoridae) by Nasonia vitripennis 2 (Hymenoptera: Pteromalidae) in Spain 3

  2019cites this paper
• Bringing Ecology Back: How Can the Chemistry of Indirect Plant Defenses Against Herbivory Be Manipulated to Improve Pest Management?

  2018cites this paper