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

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.

Ants in their plants:Pseudomyrmexants reduce primate, parrot and squirrel predation onMacrolobium acaciifolium(Fabaceae) seeds in Amazonian Brazil

“…These may be bigger or smaller in plants with ants, depending on the energy-balance between plant and ant mutualists (Frederickson & Gordon, 2009). Such between-individual variation has also been recorded for mutualisms insects and carnivorous plants (Scharmann et al, 2013). As a result, in a system with defensive ant mutualists, the simple predictions of optimal foraging (i.e.…”

Convergent and divergent evolution in carnivorous pitcher plant traps

“…Analogies can be drawn with sea anemones providing anemonefish with shelter from predators in return for defence against cnidarian predators (Godwin & Fautin, ). Nepenthes bicalcarata may benefit from colony waste for nutrition (Bazile et al ., ), the prevention of nutrient export by pitcher‐dwelling Diptera (Scharmann et al ., ) and the maintenance of the slipperiness of the trap by cleaning the peristome (Thornham et al ., ).…”

A phylogenomic analysis ofNepenthes(Nepenthaceae)

“…Furthermore, in recent years a range of studies have demonstrated various ecological adaptations related to nutrient acquisition and sometimes strongly linked to this morphological variation, such as the pitchers of Nepenthes rajah, adapted to catch the faeces of tree-shrews (Bauer et al, 2008; Ulrike Bauer et al, 2012b;Bazile et al, 2015;Clarke et al, 2009;Gaume et al, 2017;Lim et al, 2014;Merbach et al, 2002;Moran et al, 2012;Pavlovič et al, 2011;Scharmann et al, 2013;Scholz et al, 2010). These, along with variations of substrate and altitude, mark them the genus as a good putative example of an adaptive radiation (Bauer et al, 2012a;Clarke and Moran, 2016;Gaume et al, 2016;Thorogood et al, 2018).…”