How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance

Abstract

Predators and plant resistance may act together to control herbivorous arthropod populations or antagonistically, which would reduce the control of pest populations. In a field experiment we enhanced predation by adding simulated leaf domatia to plants. Leaf domatia are small structures that often harbor predaceous arthropods that are potentially beneficial to the plant. We also manipulated host plant quality by inducing resistance with controlled, early season exposure of seedlings to spider mite herbivory. Our manipulations had profound consequences for the natural community of arthropods that inhabited the plants. Leaf domatia had a direct positive effect on abundances of two species of bugs and one species of thrips, all of which are largely predators of herbivores. On leaves with domatia, each of the predators was found inside the domatia two to three times more often than outside the domatia. Eggs of predaceous bugs inside leaf domatia were protected from parasitism compared to eggs outside the domatia. The positive effects of leaf domatia on predator abundances were associated with reduced populations of herbivorous spider mites, aphids, and whiteflies. Plants with experimental leaf domatia showed significantly enhanced reproductive performance. Induced resistance also affected the community of arthropods. Of the abundant predators, all of which also fed on the plant, only minute pirate bugs were negatively affected by induced resistance. Populations of herbivorous spider mites and whiteflies were directly and negatively affected by induction. In contrast, aphid populations were higher on plants with induced resistance compared to uninduced plants. Effects of induced resistance and domatia were additive for each of the predators and for aphids. However, spider mite and whitefly populations were not suppressed further by employing both induced resistance and domatia compared to each strategy alone. Our manipulations suggest that plant defense strategies can have positive effects on some species and negative effects on others. Negative effects of “resistance traits” on predators and positive effects on some herbivores may reduce the benefits of constitutive expression of resistance traits and may favor inducible defense strategies. Multiple plant strategies such as inducible resistance and morphological traits that aid in the recruitment of predators of herbivores may act together to maximize plant defenses, although they may also be redundant and not act additively.

Domatia reduce larval cannibalism in predatory mites

“…Owing to this protection, the survival of predators on plants with domatia would be higher than on plants without domatia ( Agrawal & Karban, 1997;Agrawal et al , 2000;English-Loeb et al , 2002 ). Our work confirms the hypothesis of protection through domatia: through the use of domatia, larvae of predatory mites can escape from conspecific adults, thus decreasing the risk of cannibalism.…”

“…Many studies have shown that plants with natural domatia or artificial domatia harbour more individuals and species of carnivorous and fungivorous arthropods ( Agrawal & Karban, 1997;Agrawal et al , 2000;Norton et al , 2000;English-Loeb et al , 2002;Matos et al , 2006 ), but surprisingly, only a few studies have identified what kind of protection domatia actually offer to the mites. Thus far, it is clear that domatia can protect the mites against adverse abiotic conditions such as drought ( Walter & O'Dowd, 1992;Grostal & O'Dowd, 1994) , intra-guild predation ( Norton et al , 2001 ) and counterattacking prey ( Faraji et al , 2002a ), but not whether they also offer protection against cannibalism.…”

Mites and leaf domatia: no evidence of mutualism in Coffea arabica plants

“…Although studies have suggested that domatia may also decrease mite desiccation (e.g., O'Dowd & Willson 1989), to date no study has empirically corroborated this assumption (Grostal & O'Dowd 1994, Romero & Benson 2005. In return, the beneficial mites can decrease plant damages caused by pathogenic fungi (Norton et al 2000) or phytophagous mites (Agrawal et al 2000, Romero & Benson 2004. As an alternative hypothesis, Romero & Benson (2004) suggested that leaf domatia could buffer predator-prey oscillations by providing refuge for prey (typically phytophages); phytophages protected in domatia may disperse onto the leaf surface in a continuous flux providing a reliable food source for predators, thus minimizing local extinction.…”

Vector and virus induce plant responses that benefit a non-vector herbivore

“…Both species pierce parenchym cells and consume their contents, causing substantial leaf damage. Spider mites induce a defence response detrimental to spider mites (Agrawal, Karban, & Colfer 2000;Gols, Roosjen, Dijkman, & Dicke 2003;Kant, Sabelis, Haring, & Schuurink 2008;Karban & Carey 1984), and thrips attacking TSWV-free plants induce a defensive plant response detrimental to thrips (Belliure et al 2005). Both anti-thrips and anti-spider-mite defences involve the activation of the JA signalling pathway in several plant species (Abe et al,2008;De Vos et al 2005;Gols et al 2003;Kant et al 2004Kant et al , 2008.…”