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Keywords:

  • ant–plant interaction;
  • myrmecotrophy;
  • carnivorous plants;
  • mutualism;
  • cleaning behaviour

Summary

1. Beneficial ‘services’ in mutualistic interactions have often not evolved de novo, but from ancestral traits that had a function before the emergence of the association. These traits can then acquire novel functions in a mutualism. Even in many close insect–plant relationships, the services provided by each partner are still unclear.

2. In the well-known association between the carnivorous pitcher plant, Nepenthes bicalcarata, and Camponotus schmitzi ants in Borneo, the ants benefit by receiving food and nesting space in swollen, hollow pitcher tendrils, but the benefits to the plant are less clear. Previous studies have suggested that the ants protect against herbivory, prevent putrefaction of pitchers by removing prey items from them or increase the pitcher’s prey retention rate by attacking pitcher visitors.

3. Field observations showed that C. schmitzi ants regularly clean the pitcher rim (peristome), which is the main surface responsible for prey capture. We found that this behaviour increases the carnivorous plant’s prey capture efficiency and helps to maintain it over the pitcher’s life span. Running tests with Oecophylla smaragdina ants on colonised and ant-free older pitchers demonstrated 45·8% higher capture efficiency in pitchers inhabited by C. schmitzi. Head counts of trapped ants showed that C. schmitzi-colonised pitchers indeed captured significantly (45·2%) more prey than uncolonised pitchers of the same age.

4. The peristomes of ant-free older pitchers were strongly contaminated by fungal hyphae and other particles. Experimental contamination of clean pitcher peristomes with starch also strongly reduced capture efficiency. While the peristome was cleaned rapidly in ant-colonised pitchers and capture efficiency returned to the previous level within approximately 1 week, no cleaning and recovery were observed in ant-free pitchers.

5. Within the genus Nepenthes, N. bicalcarata has exceptionally long-lived pitchers. We propose that C. schmitzi ants benefit N. bicalcarata by keeping the pitchers effective over long periods of time, likely allowing the plant to acquire more nutrients per pitcher and thereby minimise pitcher construction costs.

6. Our findings demonstrate that the cleaning behaviour typical of many plant–ants has acquired a novel function in this ant–plant association, giving rise to a new type of myrmecotrophic mutualism.