The Ecology of Plant/insect Interactions: Implications of Digestive Strategy for Feeding by Phytophagous Insects

A key question in insect/plant ecology asks why plants are abundant in relation to insect herbivores, and consequently, why insects are not capable of eating all plants (Hairston et al. 1960, Murdoch 1966, Bernays and Graham 1988, Abe and Higashi 1991). Many studies implicate plant chemistry as being primarily responsible for limiting host choice and use among insect herbivores. This contention is supported by a wealth of literature describing many secondary chemicals that inhibit herbivory by a wide range of insects (e.g. Feeny 1976, Strong et al. 1984, Howe and Westley 1988). Alternative explanations have not been considered thoroughly, although preliminary studies suggest that several other factors may play a prominent role in structuring insect/ plant interactions. The role of natural enemies in limiting host range has been proposed as being much greater than perceived (Lawton and McNeill 1979, Bernays and Graham 1988) and new hypotheses describing the action of potential defences question accepted views of how plants respond to herbivory (Jermy 1993, Vicari and Bazeley 1993). Recent conjecture suggests a need to reappraise perspectives of insect-plant relationships, focdssing on these alternatives (Bernays and Graham 1988, Abe and Higashi 1991). Abe and Higashi (1991) contend that cellulose is a vital factor structuring terrestrial communities. Central to their argument is the fact that most phytophagous insects do not digest cellulose (Martin 1991), and that a restricted ability to digest cellulose limits the consumption of plants, so that cellulose acts as a broad-spectrum defence (Abe and Higashi 1991). As a consequence, most phytophagous insects are specialised consumers of cytoplasm and the abundance of plants is a result of the scarcity of generalist (cytoplasm and cell wall) plant consumers (Abe and Higashi 1991). The idea that the plant cell wall presents a physical barrier to herbivores is not new (Murdoch 1966), and the chemical problems associated with digesting the cell wall components are well documented (Van Soest 1982, Higashi et al. 1992). Despite this, cellulose and other cell wall components have not featured prominently in explaining the nutritional ecology of insects feeding on living plant material. Recent research describing how insect herbivores choose and utilise plants emphasises the roles that cellulose and associated plant components can play in the ecology of individual insects. Cellulose is characteristically associated with hemicellulose, lignin, cutin, silica and protein in cell walls (Van Soest 1982). In addition to posing similar digestibility problems, these components combine to form the fibrous cell wall conferring an assortment of mechanical properties on plants. In this paper I elaborate upon the basic premise of Abe and Higashi (1991) from the viewpoint that the effects on communities are driven by effects on individuals, given that small nutritional differences are capable of causing large changes in the population biology of herbivorous insects (McNeill and Southwood 1978). I identify further consequences of a high cellulose diet for herbivorous insects specialised for consuming cytoplasm, and examine the body of evidence supporting an alternative view of how plant attributes affect herbivory. I also suggest a framework suggesting future hypotheses and directions for research into plant/insect interactions and why there should be a shift in the emphasis in this research.