Feeding-Induced Changes in Plant Quality Mediate Interspecific Competition Between Sap-Feeding Herbivores

Abstract

Feeding‐induced plant resistance is a well‐documented phenomenon for leaf‐chewing insects. Furthermore, feeding‐induced resistance provides the mechanistic basis for many cases of delayed interspecific competition, whereby previous feeding by one species diminishes the performance of other herbivores which attack the same plant later in the season. This phenomenon, however, has been very poorly investigated for sap‐feeding insects. The results we present here for salt marsh‐inhabiting planthoppers (Prokelisia dolus and P. marginata) provide one of the few known examples of delayed, plant‐mediated interspecific competition between two sap‐feeding insects. Three lines of experimental evidence from the laboratory, field cages, and open field plots provide support for the detrimental effects of previous feeding by one planthopper species on the subsequent survival and performance of the other. Laboratory experiments showed that prior feeding on cordgrass by one congener resulted in reduced performance of the other in the following generation. However, the effect was asymmetric. Prior feeding by P. dolus resulted in prolonged development and reduced body size (a correlate of fecundity) in P. marginata, whereas only development was protracted in P. dolus when plants were previously exposed to P. marginata. Consequently, P. dolus appears to be the superior competitor in the context of delayed, plant‐mediated interactions. The negative effects of previous feeding by P. dolus on the development time, body size, and survival of P. marginata obtained in the laboratory were confirmed both in cages and on cage‐free islets of cordgrass in the field. Feeding‐induced reductions in host‐plant quality by P. dolus may provide additional impetus for P. marginata to migrate from shared habitats on the high marsh to nutritionally superior plants in the low marsh rarely occupied by P. dolus. The mechanism underlying the delayed competitive effects between Prokelisia planthoppers is most likely diminished plant nutrition, because feeding by P. dolus significantly reduces the concentration of essential amino acids in cordgrass. The asymmetry of plant‐mediated competition between the Prokelisia species may be due to the ability of P. dolus to better tolerate feeding‐depleted levels of plant nitrogen via compensatory feeding. Even though these two planthoppers do not suffer significant fitness reductions during contemporaneous interactions, they compete severely in the context of feeding‐induced plant resistance which is expressed later in the season. This result, coupled with the fact that most studies of interspecific interaction between herbivorous insects are contemporaneous, indicates that interspecific competition may be profoundly underestimated as a structuring force in phytophagous insect communities.

Direct and feeding‐induced interactions between two rice planthoppers, Sogatella furcifera and Nilaparvata lugens: effects on dispersal capability and performance

“…Asymmetric effects of interspecific crowding on wing form have been reported in other studies involving planthoppers (Prokelisia species) in which one species triggered macroptery selectively in the other (Denno & Roderick, 1992). In this study, macropters were produced by the inferior competitor (Prokelisia marginata), which suffered reduced survival and extended development in the presence of the competitive dominant (Prokelisia dolus) (Denno & Roderick, 1992;Denno et al, 2000). Similarly, in the present study, macropters were produced in female N. lugens in the presence of S. furcifera (Fig.…”

“…Thus, wing form is determined by an environmentally sensitive switch that specifies the development of either a macropter or a brachypter (Harrison, 1980;Roff, 1986;Roff & Fairbairn, 1991;Matsumura, 1996a;Zera & Denno, 1997). Various environmental cues such as intraspecific crowding, host plant nutrition, temperature, and photoperiod influence wing-form determination (Harrison, 1980;Zera & Denno, 1997), however the effect of interspecific crowding on wingform determination has been studied poorly in most insect herbivores (but see Lamb & MacKay, 1987;Denno & Roderick, 1992;Denno et al, 2000).…”

Prior flea beetle herbivory affects oviposition preference and larval performance of a potato beetle on their shared host plant

“…Authors have argued recently that interspecific competition may have more of an influence on herbivore community dynamics than acknowledged previously (Damman, 1993;Denno et al, 1995). Some have emphasised the importance of more subtle, plant-mediated interactions between species (Faeth, 1988(Faeth, , 1992Hunter, 1992;Denno et al, 2000). This study provides evidence for temporally separated, indirect competition between E. fuscula and L. juncta.…”

Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe

“…In drought conditions leaf maturation may become unsuitable food tissues earlier in the season due to the accumulation of defense compounds. However at the same time, their concentration in nitrogen increases which may enhance insect performances [28,45,48,60]. Drought effects also depend on the insect feeding guild.…”

“…In this case, changes in insect populations that were directly affected by drought will in turn have effects on other insect species. These effects, often mediated through changes in plant chemistry and physiology induced by the feeding of primary pests [28], may immediately impact co-occurring species or persist for several growing seasons. Indirect effects are often negative: droughtincreased performance of early defoliators often induces longlasting plant resistance that will have negative effects on insect species occurring later in the season [96].…”