Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids

Herbivore-induced plant volatiles have been suggested to function as indirect defence signals that attract natural enemies of herbivores. Several insect parasitoids are known to exploit such plant-provided cues to locate hosts. It is unclear if individual plants benefit from the action of parasitoids. We investigated this question in maize plants under attack by Spodoptera littoralis larvae and found that parasitization by the endoparasitoids Cotesia marginiventris and Campoletis sonorensis significantly reduced feeding and weight gain in the host larvae. As a result, young maize plants attacked by a single parasitized larva suffered much less feeding damage and, at maturity, produced about 30% more seed than plants that were attacked by an unparasitized larva. Such fitness benefits may have contributed to selection pressures that shaped the evolution of herbivore-induced indirect defence signals in plants.

[1]  T. C. Turlings,et al.  Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte) , 2001, CHEMOECOLOGY.

[2]  S. Wratten,et al.  Wound‐induced changes in the acceptability of tomato to larvae of Spodoptera littoralis: a laboratory bioassay , 1985 .

[3]  T. R. Ashley,et al.  Effect of Host Age, Parasitoid Age and Temperature on Interspecific Competition Between Chelonus Insularis Cresson, Cotesia Marginiventris Cresson and Microplitis Manilae Ashmead , 1992 .

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

[5]  Regino Zamora,et al.  Top‐Down Effects in a Tritrophic System: Parasitoids Enhance Plant Fitness , 1994 .

[6]  H. McAuslane,et al.  Stimuli influencing host microhabitat location in the parasitoid Campoletis sonorensis , 1991 .

[7]  D. Janzen COEVOLUTION OF MUTUALISM BETWEEN ANTS AND ACACIAS IN CENTRAL AMERICA , 1966, Evolution; international journal of organic evolution.

[8]  A. Agrawal,et al.  Why Induced Defenses May Be Favored Over Constitutive Strategies in Plants , 2000 .

[9]  J. J. Kruse,et al.  Effect of food plant switching by a herbivore on its parasitoid: Cotesia melanoscela development in Lymantria dispar exposed to reciprocal dietary crosses , 1999 .

[10]  M. Dicke,et al.  Ecology of infochemical use by natural enemies in a tritrophic context. , 1992 .

[11]  M. Dicke Are herbivore‐induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? , 1999 .

[12]  J. Daniel Hare Multitrophic Level Interactions: Plant genetic variation in tritrophic interactions , 2002 .

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

[14]  P. Oliveira The ecological function of extrafloral nectaries : herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae) , 1997 .

[15]  Foraging behavior of Campoletis sonorensis in response to Heliothis virescens and cotton plants , 1990 .

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

[17]  T. R. Ashley Growth Pattern Alterations in Fall Armyworm, Spodoptera Frugiperda, Larvae After Parasitization by Apanteles Marginiventris, Campoletis Grioti, Chelonus Insularis, and Eiphosoma Vitticole , 1983 .

[18]  I. Cruz,et al.  Efeito da idade de lagartas de Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) no desempenho do parasitóide Campoletis flavicincta (Ashmead) (Hymenoptera: Ichneumonidae) e consumo foliar por lagartas parasitadas e não-parasitadas , 1997 .

[19]  F. Slansky Utilization of Energy and Nitrogen by Larvae of the Imported Cabbageworm, Pieris rapae , as Affected by Parasitism by Apanteles glomeratus , 1978 .

[20]  S. Dorn,et al.  Herbivore‐induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis , 1998 .

[21]  T. R. Ashley,et al.  Influence of Fall Armyworm, Spodoptera Frugiperda, (Lepidoptera: Noctuldae) Larvae and Corn Plant Damage on Host Finding in Apanteles marginiventris (Hymenoptera: Braconidae) , 1983 .

[22]  Marcel Dicke,et al.  Parasitoid‐plant mutualism: parasitoid attack of herbivore increases plant reproduction , 2000 .

[23]  A. Agrawal,et al.  Induced responses to herbivory and increased plant performance , 1998, Science.

[24]  M. Sabelis,et al.  UvA-DARE ( Digital Academic Repository ) Do anthocorid predators respond to synomones from Psylla-infested pear trees in field conditions ? , 2006 .

[25]  I. Baldwin Jasmonate-induced responses are costly but benefit plants under attack in native populations. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  E. Finidori-Logli ROLE OF PLANT VOLATILES IN THE SEARCH HOST BY PARASITOID Diglyphus isaea (HYMENOPTERA: EULOPHIDAE) FOR A , 1996 .

[27]  Richard Karban,et al.  Induced Responses to Herbivory , 1997 .

[28]  A. Agrawal INDUCED RESPONSES TO HERBIVORY IN WILD RADISH: EFFECTS ON SEVERAL HERBIVORES AND PLANT FITNESS , 1999 .

[29]  P. Klinkhamer,et al.  Conflicting interests of plants and the natural enemies of herbivores. , 2000 .

[30]  M. Mangel,et al.  THE BENEFITS OF INDUCED DEFENSES AGAINST HERBIVORES , 1997 .

[31]  J. Tumlinson,et al.  Symposium: Insect Behavioral Ecology--'90: Do Parasitoids Use Herbivore-Induced Plant Chemical Defenses to Locate Hosts? , 1991 .

[32]  T. C. Turlings,et al.  Effects of plant metabolites on the behavior and development of parasitic wasps , 1998 .

[33]  B. Lanzrein,et al.  Biology and morphology of the parasitoid Chelonus inanitus (Braconidae, Hymenoptera) and effects on the development of its host Spodoptera littoralis (Noctuidae, Lepidoptera) , 1994 .

[34]  J. Thaler Jasmonate-inducible plant defences cause increased parasitism of herbivores , 1999, Nature.

[35]  Mustafizur M. Rahman,et al.  Effect of Parasitism on Food Consumption of Pieris rapae Larvae , 1970 .

[36]  Louise E. M. Vet,et al.  Plant-carnivore interactions: evolutionary and ecological consequences for plant, herbivore and carnivore , 1999 .