A Novel Type of Nutritional Ant–Plant Interaction: Ant Partners of Carnivorous Pitcher Plants Prevent Nutrient Export by Dipteran Pitcher Infauna

Martin Heil,Mathias Scharmann,Walter Federle,Daniel G Thornham,T Ulmar Grafe

doi:10.1371/journal.pone.0063556

Martin Heil, Mathias Scharmann + Show 3 more

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https://doi.org/10.1371/journal.pone.0063556

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Abstract

Many plants combat herbivore and pathogen attack indirectly by attracting predators of their herbivores. Here we describe a novel type of insect–plant interaction where a carnivorous plant uses such an indirect defence to prevent nutrient loss to kleptoparasites. The ant Camponotus schmitzi is an obligate inhabitant of the carnivorous pitcher plant Nepenthes bicalcarata in Borneo. It has recently been suggested that this ant–plant interaction is a nutritional mutualism, but the detailed mechanisms and the origin of the ant-derived nutrient supply have remained unexplained. We confirm that N. bicalcarata host plant leaves naturally have an elevated 15N/14N stable isotope abundance ratio (δ15N) when colonised by C. schmitzi. This indicates that a higher proportion of the plants’ nitrogen is insect-derived when C. schmitzi ants are present (ca. 100%, vs. 77% in uncolonised plants) and that more nitrogen is available to them. We demonstrated direct flux of nutrients from the ants to the host plant in a 15N pulse-chase experiment. As C. schmitzi ants only feed on nectar and pitcher contents of their host, the elevated foliar δ15N cannot be explained by classic ant-feeding (myrmecotrophy) but must originate from a higher efficiency of the pitcher traps. We discovered that C. schmitzi ants not only increase the pitchers' capture efficiency by keeping the pitchers’ trapping surfaces clean, but they also reduce nutrient loss from the pitchers by predating dipteran pitcher inhabitants (infauna). Consequently, nutrients the pitchers would have otherwise lost via emerging flies become available as ant colony waste. The plants’ prey is therefore conserved by the ants. The interaction between C. schmitzi, N. bicalcarata and dipteran pitcher infauna represents a new type of mutualism where animals mitigate the damage by nutrient thieves to a plant.

Highlights

Insects and flowering plants are the two most diverse lineages of eukaryotes today, and their manifold interactions affect virtually all terrestrial life
Using stable isotope analysis on natural and tracer-fed N. bicalcarata plants and by studying the interaction of C. schmitzi with the pitcher infauna, we address the following questions: (1) Is the net nutrient balance for N. bicalcarata improved when C. schmitzi is present? (2) Is there a flow of nutrients from C. schmitzi ants to the host plant? (3) Do C. schmitzi ants prey on dipteran infauna? (4) Do C. schmitzi ants reduce the number of infauna adults emerging?
Bicalcarata We found that the natural 15N/14N stable isotope abundance ratio (d15N) of N. bicalcarata was significantly higher when colonised by C. schmitzi for both climbing and rosette stage plants, and that rosettes had a higher d15N than climbers

Summary

Introduction

Insects and flowering plants are the two most diverse lineages of eukaryotes today, and their manifold interactions affect virtually all terrestrial life. Both insect and plant diversity can be explained to some extent by their ability to form complex interactions with each other. F. (Fig. 1 A) traps and digests almost any insect, and ants in particular [3,4,5], yet simultaneously houses an obligate ant partner, Camponotus schmitzi Starcke [6,7,8](Fig. 1 B). Nepenthes are tropical perennials whose insect traps are jug-shaped structures at the tips of their leaves, filled with liquid. The plants undergo an ontogenetic shift in growth habit, starting off as rosettes, bearing ‘‘lower’’ or ‘‘ground’’ pitchers, and developing into a liana producing ‘‘upper‘‘ or ‘‘aerial‘‘ pitchers [9,10]

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