Species-Specific Effects of Herbivory on the Oviposition Behavior of the Moth Manduca sexta

In Southwestern USA, the jimsonweed Datura wrightii and the nocturnal sphinx moth Manduca sexta form a pollinator-plant and herbivore-plant association. While certain plant volatile organic compounds (VOCs) attract moths for oviposition, it is likely that other host-derived olfactory cues, such as herbivore-induced VOCs, repel moths for oviposition. Here, we studied the oviposition preference of female M. sexta towards intact and damaged host plants of three species: D. wrightii, D. discolor (a less preferred feeding resource but also used by females for oviposition), and Solanum lycopersicum–tomato–(used by moths as an oviposition resource only). Damage was inflicted to the plants either by larval feeding or artificial damage. Mated females were exposed to an intact plant and a damaged plant and allowed to lay eggs for 10 min. Oviposition preferences of females were highly heterogeneous in all cases, but a larger proportion of moths laid significantly fewer eggs on feeding-damaged and artificially damaged plants of S. lycopersicum. Many females also avoided feeding-damaged D. discolor and D. wrightii plants induced by treatment with methyl jasmonate. Chemical analyses showed a significant increase in the total amount of VOCs released by vegetative tissues of feeding-damaged plants, as well as species-specific increases in emission of certain VOCs. In particular, feeding-damaged S. lycopersicum plants emitted (-)-linalool, an odorant that repels moths for oviposition. Finally, the emission of D. wrightii floral VOCs, which are important in mediating feeding by adult moths (and hence pollination), did not change in plants damaged by larval feeding. We propose that the observed differential effects of herbivory on oviposition choice are due to different characteristics (i.e., mutually beneficial or parasitic) of the insect–plant interaction.

[1]  T. Turlings,et al.  Timing of induced volatile emissions in maize seedlings , 1998, Planta.

[2]  Nathalie Delvas,et al.  Phenolic compounds that confer resistance to spruce budworm , 2011 .

[3]  J. Rojas.  Influence of Host Plant Damage on the Host-Finding Behavior of Mamestra brassicae (Lepidoptera: Noctuidae) , 1999 .

[4]  M. R. Sparks.  Physical and Chemical Stimuli Affecting Oviposition Preference of Manduca sexta (Lepidoptera: Sphingidae) , 1973 .

[5]  M. Haring,et al.  Tomato linalool synthase is induced in trichomes by jasmonic acid , 2007, Plant Molecular Biology.

[6]  C. Preston,et al.  The eco-physiological complexity of plant responses to insect herbivores , 1999, Planta.

[7]  H. Alborn,et al.  Effects on oviposition behaviour and larval development of Spodoptera littoralis by herbivore‐induced changes in cotton plants , 1999 .

[8]  I. Baldwin,et al.  Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata , 2000, Oecologia.

[9]  J. Daniel Hare,et al.  Constitutive and Jasmonate-Inducible Traits of Datura wrightii , 2006, Journal of Chemical Ecology.

[10]  J. Gershenzon,et al.  Multiple stress factors and the emission of plant VOCs. , 2010, Trends in plant science.

[11]  B. Piechulla,et al.  Influence of Green Leaf Herbivory by Manduca sexta on Floral Volatile Emission by Nicotiana suaveolens1[W] , 2008, Plant Physiology.

[12]  R. Karban,et al.  Induced defense in Nicotiana attenuata (Solanaceae) fruit and flowers , 2005, Oecologia.

[13]  J. Tumlinson,et al.  Induced synthesis of plant volatiles , 1997, Nature.

[14]  A. Kessler,et al.  Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study , 2009 .

[15]  M. Dicke,et al.  Comparative Analysis of Headspace Volatiles from Different Caterpillar-Infested or Uninfested Food Plants of Pieris Species , 1997, Journal of Chemical Ecology.

[16]  J. Vercammen,et al.  Automated dynamic sampling system for the on-line monitoring of biogenic emissions from living organisms. , 2001, Journal of chromatography. A.

[17]  T. A. Beek,et al.  Isolation and identification of volatile kairomone that affects acarine predatorprey interactions Involvement of host plant in its production , 1990, Journal of Chemical Ecology.

[18]  E. Haubruge,et al.  Assessment of oviposition site quality by aphidophagous hoverflies: reaction to conspecific larvae , 2010, Animal Behaviour.

[19]  Yingbai Shen,et al.  Volatiles released in succession from artificially damaged ashleaf maple leaves , 2001 .

[20]  L. S. Adler,et al.  Leaf herbivory and nutrients increase nectar alkaloids. , 2006, Ecology letters.

[21]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[22]  P. Landolt.  Effects of host plant leaf damage on cabbage looper moth attraction and oviposition , 1993 .

[23]  S. Ramaswamy.  Host finding by moths: sensory modalities and behaviours. , 1988 .

[24]  F. Bigler,et al.  The Induction of Volatile Emissions in Maize by Three Herbivore Species with Different Feeding Habits: Possible Consequences for Their Natural Enemies , 1998 .

[25]  Richard M. Caprioli,et al.  Defensive Function of Herbivore-Induced Plant Volatile Emissions in Nature , 2022 .

[26]  G. Bataille.  L'Abbé C , 1950 .

[27]  Junji Takabayashi,et al.  Herbivory-induced volatiles elicit defence genes in lima bean leaves , 2000, Nature.

[28]  Judith L. Bronstein,et al.  ATTRACTING ANTAGONISTS: DOES FLORAL NECTAR INCREASE LEAF HERBIVORY? , 2004 .

[29]  M. R. Sparks.  A Surrogate Leaf for Oviposition by the Tobacco Hornworm , 1970 .

[30]  J. Hildebrand,et al.  Novel, Non-Solanaceous Hostplant Record for Manduca sexta (Lepidoptera: Sphingidae) in the Southwestern United States , 2000 .

[31]  R. Karban.  The ecology and evolution of induced resistance against herbivores , 2011 .

[32]  G. Davidowitz,et al.  Reproductive biology of Datura wrightii: the benefits of a herbivorous pollinator. , 2009, Annals of botany.

[33]  J. Tumlinson,et al.  Systemic release of chemical signals by herbivore-injured corn. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[34]  R. A. Bell,et al.  Techniques for Rearing Laboratory Colonies of Tobacco Hornworms and Pink Bollworms , 1976 .

[35]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[36]  C. I. Miles,et al.  Host recognition by the tobacco hornworm is mediated by a host plant compound , 2001, Nature.

[37]  G. Xing,et al.  Oviposition deterrents in larval frass of the cotton boll worm, Helicoverpa armigera (Lepidoptera: Noctuidae): chemical identification and electroantennography analysis. , 2006, Journal of insect physiology.

[38]  M. Sabelis,et al.  Plants are better protected against spider-mites after exposure to volatiles from infested conspecifics , 1992, Experientia.

[39]  J. Sanes,et al.  Structure and development of antennae in a moth, Manduca sexta. , 1976, Developmental biology.

[40]  J. Daniel Hare.  Variation in Herbivore and Methyl Jasmonate-Induced Volatiles Among Genetic Lines of Datura wrightii , 2007, Journal of Chemical Ecology.

[41]  G. Davidowitz,et al.  Nectar usage in a southern Arizona hawkmoth community , 2008 .

[42]  C. Preston,et al.  Eating the evidence? Manduca sexta larvae can not disrupt specific jasmonate induction in Nicotiana attenuata by rapid consumption , 2000, Planta.

[43]  Jeffrey A. Riffell,et al.  Characterization and Coding of Behaviorally Significant Odor Mixtures , 2009, Current Biology.

[44]  E. Backus.  Sensory systems and behaviours which mediate hemipteran plant-feeding: A taxonomic overview , 1988 .

[45]  Jeffrey A. Riffell,et al.  Behavioral consequences of innate preferences and olfactory learning in hawkmoth–flower interactions , 2008, Proceedings of the National Academy of Sciences.

[46]  M. Dicke,et al.  Multitrophic effects of herbivore‐induced plant volatiles in an evolutionary context , 2000 .

[47]  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.

[48]  M. Haring,et al.  Differential Timing of Spider Mite-Induced Direct and Indirect Defenses in Tomato Plants1[w] , 2004, Plant Physiology.

[49]  D. Seigler,et al.  Electroantennogram and oviposition responses of Manduca sexta to volatile components of tobacco and tomato , 1980 .

[50]  R. Raguso,et al.  Trumpet Flowers of the Sonoran Desert: Floral Biology of Peniocereus Cacti and Sacred Datura , 2003, International Journal of Plant Sciences.

[51]  J. Gershenzon,et al.  The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[52]  L. Riddiford,et al.  Regulation of reproductive behaviour and egg maturation in the tobacco hawk moth, Manduca sexta , 1984 .

[53]  I. Baldwin,et al.  Volatile signaling in plant-plant-herbivore interactions: what is real? , 2002, Current opinion in plant biology.

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

[55]  A. Madden,et al.  Biology of the Tobacco Hornworm in the Southern Cigar-Tobacco District , 1945 .

[56]  John G Hildebrand,et al.  Antagonistic effects of floral scent in an insect–plant interaction , 2010, Proceedings of the Royal Society B: Biological Sciences.

[57]  W. Boland,et al.  Effects of Feeding Spodoptera littoralis on Lima Bean Leaves. II. Continuous Mechanical Wounding Resembling Insect Feeding Is Sufficient to Elicit Herbivory-Related Volatile Emission , 2005, Plant Physiology.

[58]  J. Tumlinson,et al.  Plant volatiles as a defense against insect herbivores , 1999, Plant physiology.

[59]  B. Hansson,et al.  Oviposition deterring components in larval frass of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae): a behavioural and electrophysiological evaluation , 1993 .

[60]  W. J. Lewis,et al.  Herbivore-infestedplants selectivelyattract parasitoids , 1998 .

[61]  John H. Loughrin,et al.  Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plant. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[62]  G. Fraenkel,et al.  The specificity of the tobacco hornworm, Protoparce sexta, to solanaceous plants. , 1960 .

[63]  M. Mescher,et al.  Caterpillar-induced nocturnal plant volatiles repel conspecific females , 2001, Nature.