A novel resource-service mutualism between bats and pitcher plants

Abstract

Mutualistic relationships between vertebrates and plants apart from the pollen and seed-dispersal syndromes are rare. At first view, carnivorous pitcher plants of the genus Nepenthes seem to be highly unlikely candidates for mutualistic interactions with animals, as they form dimorphic terrestrial and aerial pitchers that trap arthropods and small vertebrates. Surprisingly, however, the aerial pitchers of Nepenthes rafflesiana variety elongata are poor insect traps, with low amounts of insect-attractive volatile compounds and low amounts of digestive fluid. Here, we show that N. rafflesiana elongata gains an estimated 33.8 per cent of the total foliar nitrogen from the faeces of Hardwicke's woolly bats (Kerivoula hardwickii hardwickii) that exclusively roost in its aerial pitchers. This is the first case in which the faeces-trapping syndrome has been documented in a pitcher plant that attracts bats and only the second case of a mutualistic association between a carnivorous plant and a mammal to date.

Figure 1.

Service benefit provided by N. r. elongata to K. h. hardwickii. (a) Aerial pitcher of N. rafflesiana var. elongata. (b) The same pitcher with the front tissue removed to reveal a roosting Hardwick's woolly bat. (c) The shorter aerial pitcher of N. rafflesiana variety typica.

Figure 2.

Resource benefit provided by roosting K. h. hardwickii to N. r. elongata. (a) Box-plot of total foliar nitrogen of pitchers used as roosts (n = 38) and of control pitchers (n = 17). (b) Box-plot of foliar δ¹⁵N of pitchers used as roosts (n = 38), control pitchers (n = 17) and bat faeces (n = 3). The scarce stable isotope ¹⁵N accumulates from one trophic level to the next and thus stable isotope ratios of ¹⁵N/¹⁴N (δ¹⁵N) can be used to indicate the nitrogen source. Faeces from insectivorous bats have a higher δ¹⁵N signature than the insects they feed on or the insects that are trapped by the pitcher plant.