Indirect interactions between herbivores mediated by herbivore-induced plant trait changes can be more frequent and have a larger impact on biodiversity and community structure than direct competition between herbivores (Ohgushi 2005; Anderson, Inouye & Underwood 2009). Plants respond to herbivore damage by changes in allelochemistry, cell structure and growth, physiology, morphology, phenology (Karban & Baldwin 1997; Denno & Kaplan 2007) or nutritional content (Denno et al. 2000; Sandström, Telang & Moran 2000). These herbivore-induced plant responses may not only have multiple indirect effects on the performance and abundance of other herbivores (Van Zandt & Agrawal 2004; Poveda et al. 2005), but also influence their behaviour and spatial distribution (Van Dam, Hadwich & Baldwin 2000). Plant-mediated indirect interactions may involve herbivores that are separated spatially (Bezemer et al. 2003), temporally (Johnson et al. 2002) and/or taxonomically (Bailey & Whitham 2006).
The applied relevance of plant-mediated interactions in terms of yield losses to invertebrate pests in agricultural crops is largely unknown. This is surprising given the large potential for such interactions, with most crops being affected by a sequence of different herbivore species with contrasting ecologies and host-plant effects. The quantitative importance of effects depends on the spatial and temporal scales at which these effects play out. While quantitative and long-term studies on plant-mediated interactions have often been called for (Bolker et al. 2003; Werner & Peacor 2003), few have gone beyond qualitative snapshot studies (Hougen-Eitzman & Karban 1995; Utsumi, Ando & Miki 2010).
Here, we investigate the potential of plant-mediated indirect interactions between insect herbivore species to affect yield losses in cacao. Cacao Theobroma cacao L. is one of the most important cash crops worldwide, but also a species severely affected by pests and diseases. These have been estimated to be responsible for up to 30% losses in global production (Ploetz 2007) and can play a major role in cacao boom and bust cycles (Clough, Faust & Tscharntke 2009). The cocoa pod borer Conopomorpha cramerella Snellen (Lepidoptera: Gracillariidae) is the major cacao pest in Southeast Asia, causing crop losses up to 50% (Day 1989). The larvae mine into medium-sized pods, causing quantitative and qualitative effects on the yield, and impede the separation of husk and pod contents (Fig. 1c). The mirid parasite Helopeltis sulawesi Stonedahl (Hemiptera: Miridae) feeds on pods of all ages and young shoots of cacao (Giesberger 1983). The surface of damaged pods is covered with scars and a thick sclerotic layer, and this may promote the abscission of young fruits (cherelles) (Muhamad & Way 1995; Fig. 1b). In Southeast Asia, Helopeltis spp. are considered as serious pests by farmers and agriculturalists (Muhamad & Way 1995, personal observation A. Wielgoss, Y. Clough). As such, Helopeltis spp. are often used as a trigger for insecticide application, especially because imagos and early stages of the main pest C. cramerella are difficult to detect. Helopeltis sulawesi and C. cramerella may co-occur in the same pod at the same time, but H. sulawesi often damages the pod surface from the cherelle stage onwards, that is, 3 months before the preferred time-window for oviposition by C. cramerella.
We hypothesized that the biology and the sequence of attack by the two herbivore species can lead to indirect interactions between them. Sap-feeding by Helopeltis spp. induces changes in the pod texture early in the pod development, before the stage preferred by C. cramerella for oviposition, which suggests a potential for asymmetric effects of the mirid on the pod borer.
We conducted a large-scale, 2-year study in 43 smallholder cacao plots on the island of Sulawesi, the main cacao-producing region in Indonesia. We expected that the damage by the local mirid species, H. sulawesi, will be negatively associated with subsequent damage by C. cramerella. In a two-choice experiment, we tested whether C. cramerella females discriminate between healthy pods and pods damaged by H. sulawesi. The results are quantified both in terms of herbivore response, potential environmental response and in terms of the impact on cacao yield.