Plant-Insect Interactions

by

Paul-André Calatayud, Nicolas Sauvion, Denis Thiéry, François Rebaudo, Emmanuelle Jacquin-Joly

• LAST REVIEWED: 23 June 2023
• LAST MODIFIED: 23 June 2023
• DOI: 10.1093/obo/9780199830060-0193

Introduction

Plants and insects are highly diverse groups due to their ability to exploit a wide range of niches, from the desert to the arctic zone, and also almost all the plant species growing on the planet. Plants and insects make up together approximately half of all known species of multicellular organisms. Each plant interacts with insects in a different manner; insects may act as protection, dispersers, or fertilizers for plants, while plants may be a food/energy resource or nest location for insects. Starting with herbivory, plant-insect interactions date back to the Devonian period, about 420 million years ago, when plants first began their conquest of the land. But it was most probably in the Upper Carboniferous, about 320 million years ago, that these interactions became more intense, characterized also by the appearance of entomophily (i.e., insect pollination) about 252 million years ago, before the appearance of flowering plants (angiosperms).

General Overviews

Plant-insect interactions are classically viewed as mutualistic, antagonistic, or commensalistic. Mutualism is characterized by help between each partner, with both benefiting and neither harmed. Mutualisms include pollination (e.g., flowering plant/insect pollinator systems), plant guarding, or seed dispersal (e.g., plant/ant systems). In antagonistic relationships, one counterpart benefits and the other is harmed. This relationship includes phytophagy by insects (e.g., insect pests) but also insectivory by plants (e.g., carnivorous plants). In commensalism, one counterpart benefits but the other is not harmed (e.g., the commensal relationship of the Monarch butterfly larvae with certain species of milkweeds to store cardiac glycosides for defensive purposes). The founders of the field of plant-insect interactions include, among others: Jean-Henri Fabre, one of the pioneers of insect behavior and ecophysiology as well as the study of chemical communication in insects (Fabre 1879); Charles Darwin, the first to highlight the coevolution process between insect and plant communities (Darwin 1899); Andrew D. Hopkins, whose theory was the first to explain a mechanism of host plant fidelity in phytophagous insects (Hopkins 1916); and Karl von Frisch, the first to describe sensorial perception in insects inside their environment, particularly in plants (Frisch 1953). Several pioneering scientists pointed out the importance of plant chemistry to the establishment of such intimate relations (see Dethier 1941), and Snelling 1941 is the first work to define plants’ defense mechanisms against herbivorous insects. In 1958, the late Jan de Wilde organized the first symposium on insect-plant interactions in Wageningen, the Netherlands. The timing of this symposium corresponded to the first issue of the well-known scientific journal Entomologia Experimentalis et Applicata (cited under Journals). At the same time, a pioneering paper, Fraenkel 1959, defined the role and importance of secondary plant metabolites in plant-insect interactions. Knowledge of the sensory physiology of the gustatory system of insects took a big step forward with Schoonhoven and Dethier 1966, after incredibly sound research on insect olfaction by pioneering works such as Viallanes 1887, probably the first to study the antennal lobe structure in a hornet. The first major scholars of plant-insect interactions in the early twenty-first century include May R. Berenbaum and Art R. Zangerl at the University of Illinois, pioneers in chemical ecology of insect-plant interactions/detoxification of plant defenses/coevolution. Elizabeth (Liz) Bernays at Arizona University was considered one of the most influential scientists working on plant-herbivore interactions in the 1980s. Dame Miriam Rothschild was a classical example of a grand-old lady in caterpillar-plant interactions. Fritz and Simms 1992 is the first synthesis of plant-insect interactions.

• Darwin, Charles. 1899. The various contrivances by which orchids are fertilized by insects. 2d ed. London: John Murray.

  DOI: 10.5962/bhl.title.27790

  Darwin was the first to show plant-insect interactions in many orchid flowers that had evolved elaborate structures by natural selection in order to facilitate cross-pollination. He suggested that orchids and their insect pollinators evolved by interacting with one another over many generations, a process referred to as coevolution.

• Dethier, Vincent G. 1941. Chemical factors determining the choice of food plants by Papilio larvae. American Naturalist 75.756: 61–73.

  DOI: 10.1086/280929

  One of the first reviews on the importance of chemicals in the attraction between insects and plants (species of Papilio and Umbelliferae).

• Fabre, Jean-Henri. 1879. Etudes sur l’instinct et les moeurs des insectes. Souvenirs Entomologiques. Paris: Librairie Charles Delagrave.

  Introduced ethology (i.e., ecological studies) for the first time, studying insects’ behavior and linking it to their environment. Also described female giant peacock moths’ (Saturnia pyri) attraction of male counterparts by odorant emission, introducing, for the first time, chemical communication in insects.

• Fraenkel, Gottfried S. 1959. The raison d’être of secondary plant substances. Science 129.3361: 1466–1470.

  DOI: 10.1126/science.129.3361.1466

  The founder of the notion of the influence/importance of secondary plant substances on insects’ physiology and behavior.

• Frisch, Karl von. 1953. The dancing bees: An account of the life and senses of the honey bee. New York: Harcourt, Brace.

  Centered on sensory perceptions of honeybees inside their environments, and particularly toward plants, including the first investigation into the meaning of the waggle dance. A translation of Aus dem Leben der Bienen, 5th revised edition (Berlin: Springer-Verlag, 1953).

• Fritz, Robert S., and Ellen L. Simms. 1992. Plant resistance to herbivores and pathogens. Chicago: Univ. of Chicago Press.

  DOI: 10.7208/chicago/9780226924854.001.0001

  The first synthesis book on plant-herbivore interactions mostly focused on plant resistance, emphasizing ecological and evolutionary bases of resistance.

• Hopkins, Andrew D. 1916. Economic investigations of the scolytid bark and timber beetles of North America. In US Department of Agriculture Program of Work for 2017. Edited by US Department of Agriculture, 353. Washington, DC: US Department of Agriculture.

  Hopkins was the first to observe that “a species which breeds in two or more hosts will prefer to continue to breed in the host to which it has become adapted” (p. 353). This concept was called HHSP (Hopkins’ Host Selection Principle).

• Schoonhoven, Louis M., and Vincent G. Dethier. 1966. Sensory aspects of host-plant discrimination by lepidopteraous larvae. Archives Néerlandaises de Zoologie 16:497–530.

  DOI: 10.1163/036551666X00057

  Among the first studies on chemosensory systems in insects. The authors are among the pioneers of sensory systems analyses in phytophagous insects for host-plant discrimination.

• Snelling, Ralph O. 1941. Resistance of plants to insect attack. Botanical Review 7:543–586.

  DOI: 10.1007/BF02872411

  The first paper to define plants’ resistance to insects. In 1951, Painter categorized the mechanisms of plant resistance into three: tolerance, antibiosis, and non-preference (R. H. Painter, “Insect Resistance in Crop Plants,” Botanical Review 7.10 [1951]: 543–586).

• Viallanes, Henri. 1887. Etudes histologiques et organologiques sur les centres nerveux et les organes des sens des animaux articulés. Paris: Masson.

  This book in French contains one of the first studies of the olfactory system of arthropods.