Plants Anticipating Help: A New Hypothesis in Plant Defence Theory

Plants can 'cry for help' in response to herbivory as well as anticipate herbivory by detecting specific environmental cues before damage occurs. But can plants 'anticipate help?' Building on the optimal defence and information transfer models of induced plant defence, we argue they can. We find literature support for key assumptions of the 'anticipating help' hypothesis, which proposes plants can (1) detect cues that signal reliable protection from enemies of herbivores (bodyguards), and (2) downregulate direct anti-herbivore resistance when bodyguards compensate. In an original a priori test of the assumptions of cue detection and downregulation of direct resistance, we use a meta-analysis of sequential herbivory experiments. We found that plants express induced susceptibility (dampened direct resistance) towards leaf-chewing herbivores only after induction by myrmecophilous sap-feeding herbivores, a putative cue for reliable ant-mediated protection against chewing herbivores. More generally, we expect 'anticipating help' behaviour in plants when local environmental cues predict reliable anti-herbivore protection from bodyguards that compensate for dampened direct resistance at a reduced fitness cost. The 'anticipating help' hypothesis can explain several enigmatic issues, such as induced susceptibility, associational resistance of plants, and how indirect resistance may benefit plant fitness under a wider range of conditions than previously recognised.