Background Carnivorous plants are an ideal model system for evaluating the role of secondary metabolites in plant ecology and evolution. Carnivory is a striking example of convergent evolution to attract, capture and digest prey for nutrients to enhance growth and reproduction and has evolved independently at least ten times. Though the roles of many traits in plant carnivory have been well studied, the role of secondary metabolites in the carnivorous habit is considerably less understood. Scope This review provides the first synthesis of research in which secondary plant metabolites have been demonstrated to have a functional role in plant carnivory. From these studies we identify key metabolites for plant carnivory and their functional role, and highlight biochemical similarities across taxa. From this synthesis we provide new research directions for integrating secondary metabolites into understanding of the ecology and evolution of plant carnivory. Conclusions Carnivorous plants use secondary metabolites to facilitate prey attraction, capture, digestion and assimilation. We found ~170 metabolites for which a functional role in carnivory has been demonstrated. Of these, 26 compounds are present across genera that independently evolved a carnivorous habit, suggesting convergent evolution. Some secondary metabolites have been co-opted from other processes, such as defence or pollinator attraction. Secondary metabolites in carnivorous plants provide a potentially powerful model system for exploring the role of metabolites in plant evolution. They also show promise for elucidating how the generation of novel compounds, as well as the co-option of pre-existing metabolites, provides a strategy for plants to occupy different environments.

Background and aims Secondary metabolites are integral to multiple key plant processes: growth regulation, pollinator attraction, interactions with conspecifics, competitors and symbionts, yet their role in plant adaptation remains an underexplored area of research. Carnivorous plants use secondary metabolites to acquire nutrients from prey, but the extent of the role of secondary metabolites in plant carnivory is not known. We aimed to determine the extent of the role of secondary metabolites in facilitating carnivory of the Cape sundew, Drosera capensis. Methods We conducted metabolomic analysis of 72 plants in a time-series experiment before and after simulated prey capture. We used UHPLC-MS/MS and retention time index to identify compounds in the leaf trap tissue which changed up to 72 hrs following simulated prey capture. We identified associated metabolic pathways, and cross-compared these compounds to metabolites previously known to be involved in carnivorous plants across taxa. Key results For the first time in a carnivorous plant, we have profiled the whole-leaf metabolome response to prey capture. Reliance on secondary plant metabolites was higher than previously thought–2383 out of 3257 compounds in fed leaves had statistically significant concentration changes in comparison to unfed controls. Of these, ~34 compounds are also associated with carnivory in other species; 11 are unique to Nepenthales. At least 20 compounds had 10-fold changes in concentration, 12 of which had 30-fold changes and are typically associated with defence or attraction in non-carnivorous plants. Conclusions Secondary plant metabolites are utilised in plant carnivory to an extent greater than previously thought–we found a whole metabolome response to prey capture. Plant carnivory, at the metabolic level, likely evolved from at least two distinct functions–attraction and defence. Findings of this study support the hypothesis that secondary metabolites play an important role in plant diversification and adaptation to new environments.

Venus flytrap (Dionaea muscipula) has had a conservation status of vulnerable since the 1970s. Little research has focussed on the ecology and even less has examined its juvenile stages. For the first time, reliance on invertebrate prey for growth was assessed in seedling Venus flytrap by systematic elimination of invertebrates from the growing environment. Prey were experimentally removed from a subset of Venus flytrap seedlings within a laboratory environment. The amount of growth was measured by measuring trap midrib length as a function of overall growth as well as prey spectrum. There was significantly lower growth in prey-eliminated plants than those utilising prey. This finding, although initially unsurprising, is actually contrary to the consensus that seedlings (traps < 5 mm) do not catch prey. Furthermore, flytrap was shown to have prey specificity at its different growth stages; the dominant prey size for seedlings did not trigger mature traps. Seedlings are capturing and utilising prey for nutrients to increase their overall trap size. These novel findings show Venus flytrap to have a much more complex evolutionary ecology than previously thought.