Plant cyanogenesis means the release of gaseous hydrogen cyanide (HCN) in response to cell damage and is considered as an effective defense against generalist herbivores. In contrast, specialists are generally believed not to be affected negatively by this trait. However, quantitative data on long-term effects of cyanogenesis on specialists are rare. In this study, we used lima bean accessions (Fabaceae: Phaseolus lunatus L.) with high quantitative variability of cyanogenic features comprising cyanogenic potential (HCNp; concentration of cyanogenic precursors) and cyanogenic capacities (HCNc; release of gaseous HCN per unit time). In feeding trials, we analyzed performance of herbivorous Mexican bean beetle (Coleoptera: Coccinellidae: Epilachna varivestis Mulsant) on selected lines characterized by high (HC-plants) and low HCNp (LC-plants). Larval and adult stages of this herbivore feed on a narrow range of legumes and prefer cyanogenic lima bean as host plant. Nevertheless, we found that performance of beetles (larval weight gain per time and body mass of adult beetles) was significantly affected by lima bean HCNp: Body weight decreased and developmental period of larvae and pupae increased on HC-plants during the first generation of beetles and then remained constant for four consecutive generations. In addition, we found continuously decreasing numbers of eggs and larval hatching as inter-generational effects on HC-plants. In contrast to HC-plants, constantly high performance was observed among four generations on LC-plants. Our results demonstrate that Mexican bean beetle, although preferentially feeding on lima bean, is quantitatively affected by the HCNp of its host plant. Effects can only be detected when considering more than one generation. Thus, cyanide-containing precursors can have negative effects even on herbivores adapted to feed on cyanogenic plants.
Summary1. Plants are simultaneously attacked by multiple herbivores and pathogens. While some plant defences act synergistically, others trade-off against each other. Such trade-offs among resistances to herbivores and pathogens are usually explained by the costs of resistance, i.e. resource limitations compromising a plant's overall defence. 2. Here, we demonstrate that trade-offs can also result from direct negative interactions among defensive traits. We studied cyanogenesis (release of HCN) of lima bean (Fabaceae: Phaseolus lunatus) and effects of this efficient anti-herbivore defence on resistance to a fungal pathogen (Melanconiaceae: Colletotrichum gloeosporioides). 3. Leaf tissue destruction by fungal growth was significantly higher on high cyanogenic (HC) lima bean accessions than on low cyanogenic (LC) plants. The susceptibility of HC accessions to the fungal pathogen was strongly correlated to reduced activity of resistance-associated polyphenol oxidases (PPOs) in leaves of these plants. LC accessions, in contrast, showed high PPO activity, which was correlated with distinct resistance to C. gloeosporioides. 4. Experimentally applied, gaseous HCN reduced PPO activity and significantly increased the size of lesions caused by C. gloeosporioides in LC leaves. 5. Field observations of a wild lima bean population in Mexico revealed a higher infection rate of HC compared to LC plant individuals. The types of lesions observed on the different cyanogenic plants in nature were similar to those observed on HC and LC plants in the laboratory. 6. Synthesis. We suggest that cyanogenesis of lima bean directly trades off with plant defence against fungal pathogens and that the causal mechanism is the inhibition of PPOs by HCN. Our findings provide a functional explanation for the observed phenomenon of the low resistance of HC lima beans in nature.
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