The three sundew species we investigated exhibit different roles for visual and chemical cues as well as spatial separation between flower and traps to lessen the pollinator-prey conflict. In spite of differences in spatial separation between flowers and traps in the three species, only a similarly small proportion of flower visitors were caught in traps of each species. This finding is consistent with previous studies of other carnivorous sundews where prey caught in traps consisted of only a few percent pollinators11,12. We hypothesized that the small number of pollinators caught in carnivorous traps could be due to either the ability of flower visitors to free themselves (and perhaps learn to avoid traps) or to other mechanisms employed by the plants that spare flower visitors. Our results indicate that a large proportion of flower visitors were not able to free themselves from the sticky secretions. This suggests other mechanisms such as visual, chemical, or spatial/temporal separation between flower and traps may be employed by the plants to minimize trapping of flower visitors. Our results show that flowers of both D. spatulata and D. arcturi are unusual because no chemicals were detected in their headspaces, suggesting pollinators are attracted to visual cues of flowers while spatial separation between flowers and traps may reduce entrapment of pollinators. In our experiments on colour preference of flower visitors, white caught significantly more flower visitors than red, black or transparent colours. Flower visitors usually show strong responses to visual stimuli24. White and yellow are the most dominant floral colours in native New Zealand fauna and syrphid flies show strong preferences for these two colours25. It could be argued that since we haven’t examined the pollen load of flower visitors that syrphids and non-syrphid diptrans are not important pollinators. However syrphids and non-syrphid dipterans are well established pollinators especially at high elevations where these plants grow26. Both D. spatulata and D. arcturi have a white flower and these are associated with the non-carnivorous but cohabiting cushion plant, Donatia novae-zelandiae (Hooker). The cushion plant is common and produces large numbers of similar appearing white flowers at the same time (Fig. 4S). Interestingly, many floral compounds have been detected in the headspace of the cushion plant (unpublished). This suggests that both sundew species utilize white flowers to visually mimic the flowers of cushion plants and benefit from a common search image of insect pollinators while saving physiological costs of producing scents that could also cost ecologically if herbivores are attracted. Colour and shape mimicry have been reported in the pollination of an orchid27.

Because we found that sticky traps of both D. spatulata and D. arcturi do not release volatiles that could attract prey insects, prey capture by traps is either mediated by visual cues, or by random landing resulting in passive capture. Schaefer and Ruxton20 concluded that red colouration is an adaptive trait that increases capture rates for carnivorous plants. However, Jürgens et al.28 suggested that both pollinators and prey land less on red disc models than on green discs in the sundew habitat of New Zealand. In our field experiments, other insects not visiting flowers showed no preference for various visual cues, suggesting these two plants employ passive sticky traps to catch prey. Similarly, the red colouration of Drosera rotundifolia (L.) was not important in the attraction of prey insects19. Both D. spatulata and D. arcturi sundews grow with cushion plants in ombrotrophic open bogs whose soil is nutrient poor, especially in nitrogen. Although sundew carnivorous plants would seem to benefit by using an odour to attract prey to their traps and another odour to guide pollinators to their flowers, producing two different scents could be costly. In open bogs, there are few other plant species (except the low growing, mat-forming cushion plant) that offer landing perches. Thus, passive trapping may be sufficient to capture insects in such environments. Passive trapping is also suggested by the lack of selectivity in prey capture, as shown for D. spatulata traps at ground level that mainly captured walking insects of Hymenoptera and Coleoptera, while traps of D. arcturi that are just above ground level caught a mixture of flying and walking insects (Fig. 1).

In our experiments, colour alone was not enough to reduce the number of flower visitors caught on red discs representing carnivorous traps when the white and red discs were adjacent. Only when the two coloured discs were separated by 5 or 10 cm did the number of flower visitors land more on the white discs rather than on the red ones, suggesting that spatial separation between flower and trap, in combination with flower colour, is employed by these two species to protect pollinators. Anderson11 found no pollinators were caught in the traps of two Drosera species with short and long scapes, while the flowers of the species with short scapes received less pollinator visits compared to flowers of the other species with long scapes. He suggested that Drosera species evolved long scapes to receive more floral visits rather than to protect the pollinator from traps. Our findings of little overlap in flower visitors and prey on flowers and traps agree with those of Anderson. However, Anderson11 did not provide a mechanism by which plants could prevent pollinators from being caught in traps, either by visual or chemical signals, especially in species with short scapes. When the spatial separation between flower and traps was small as in D. auriculata, the number of flower visitors caught on traps was still relatively low, suggesting a non-spatial mechanism such as a semiochemical one for protecting pollinators.

Our chemical analysis is the first to identify volatiles released from both flowers and traps of a carnivorous plant, yielding unique odours with no overlap in chemical composition. Floral odour contained 2′-aminoacetophenone and 2-phenylethanol as the main compounds, while trap odour had plumbagin as the main compound. 2-phenylethanol is a well-known floral volatile22, while 2′-aminoacetophenone has not been reported as a floral compound but as a volatile from honey29. Our synthetic blend of floral compounds attracted both flower visitors and prey insects. In contrast, the synthetic blend of trap volatiles was not attractive to flower visitors but rather attracted prey insects. Floral and trap odours released together resulted in a significant reduction in the number of flower visitors but also a significant increase in the number of prey insects captured. The behavioural activity of specific compounds in the floral and trap blends remains to be determined. Plumbagin has been identified in the extract of the traps of other Drosera species30 but we show for the first time that the compound is present in biologically-active headspace.

In D. auriculata, visual cues alone were not enough to protect flower visitors since both green and pink discs attracted almost equal numbers of flower visitors. In contrast, flower visitors showed a preference for pink discs with floral odour compared to green discs with trap odour. This suggests that odour is the main mechanism employed by carnivorous D. auriculata to guide flower visitors to their flowers. Associative learning of odour is well documented in insects31. Although visual cues were less important in reducing pollinator-prey conflict, more flower visitors were caught in a trapping model with visual cues than without. Similarly, more flower visitors were caught in a trapping model with both visual and chemical cues compared to a similar model without chemical cues. This suggests an additive interaction between colour and odour in attracting flower visitors to the plants, while odour was critical for the flower visitors to discriminate between flowers and traps. Synergistic interactions among colour, shape and odour in attraction of insects are known. For example, bark beetles exhibit increased attraction to aggregation pheromone when released from various coloured silhouettes resembling trees32,33. Honeybees are known to more strongly associate rewards with colours when combined with flower fragrances34,35. Tsetse flies are attracted in higher numbers to dark cylinders the size of vertebrate hosts and emanating CO 2 and acetone than to the same cylinders without the odours36.

The pollinator-prey conflict in carnivorous plants has been defined by Wickler6 and Wiens7 and demonstrated by Zamora8. Our objective was not to demonstrate the pollinator-prey conflict but rather to investigate whether the three Drosera species have evolved specific mechanisms to protect pollinators. Previously, two mechanisms have been proposed to alleviate this conflict: a) spatial separation between the trapping surfaces and the flowers; and b) temporal separation where prey-catching is not functioning while the plant is flowering9,10. In both D. spatulata and D. arcturi, spatial separation is the main mechanism that reduces the number of flower visitors caught on the trapping surfaces, while visual cues help to guide flower visitors to flowers. In these two species, prey attraction is not mediated by visual or chemical cues; rather passive trapping was the main mechanism to capture prey insects. The lack of ability to attract prey in the two species violates the condition of the carnivorous syndrome in which prey are lured to the traps10,17,37. The relatively few landing perches in the bogs facilitates prey capture by traps and would provide little selection pressure for traps to evolve attractive chemical cues.

In D. auriculata where spatial separation is reduced and temporal separation does not occur, there could be strong selection pressure to evolve another mechanism to minimize pollinator-prey conflict. In contrast to scentless D. spatulata and D. arcturi, unique odours were identified from the flower and trap headspaces of D. auriculata that mediate the attraction of flower visitors to flowers while avoiding sticky traps, whereas trap odours attract prey insects. This species can be considered truly carnivorous because it fulfills the condition of the carnivorous syndrome. Our results report the first example of odour used by carnivorous sundew plants to attract prey insects since first hypothesized by Darwin17. Our findings suggest co-evolution between insect pollinators and carnivorous plants in which the latter provide either spatially separated visual cues or distinct odours as an “honest” signal to allow flower visitors to avoid being trapped.