Bats Are Acoustically Attracted to Mutualistic Carnivorous Plants

Abstract

Mutualisms between plants and animals shape the world's ecosystems. In such interactions, achieving contact with the partner species is imperative. Plants regularly advertise themselves with signals that specifically appeal to the partner's perceptual preferences. For example, many plants have acquired traits such as brightly colored, fragrant flowers that attract pollinators with visual, olfactory, or--in the case of a few bat-pollinated flowers--even acoustic stimuli in the form of echo-reflecting structures. However, acoustic attraction in plants is rare compared to other advertisements and has never been found outside the pollination context and only in the Neotropics. We hypothesized that this phenomenon is more widespread and more diverse as plant-bat interactions also occur in the Paleotropics. In Borneo, mutualistic bats fertilize a carnivorous pitcher plant while roosting in its pitchers. The pitcher's orifice features a prolonged concave structure, which we predicted to distinctively reflect the bats' echolocation calls for a wide range of angles. This structure should facilitate the location and identification of pitchers even within highly cluttered surroundings. Pitchers lacking this structure should be less attractive for the bats. Ensonifications of the pitchers around their orifice revealed that this structure indeed acts as a multidirectional ultrasound reflector. In behavioral experiments where bats were confronted with differently modified pitchers, the reflector's presence clearly facilitated the finding and identification of pitchers. These results suggest that plants have convergently acquired reflectors in the Paleotropics and the Neotropics to acoustically attract bats, albeit for completely different ecological reasons.

Convergent and divergent evolution in carnivorous pitcher plant traps

“…Divergence in the carnivorous syndrome in (a–f) Nepenthes and (g–j) Sarraceniaceae. Several species of Nepenthes have diverged (at least partially) from the carnivorous syndrome and coevolved mutualistic relationships with animal partners: (a) N. albomarginata has a white band of hairs which attracts termites ( Hospitalitermes bicolor ); (b) N. bicalcarata produces swollen tendrils in which mutualistic ants ( Camponotus schmitzi ) rear broods; (c) N. hemsleyana has a modified pitcher shape and fluid level to facilitate bat roosting (Lim et al ., ) and an elongated inner pitcher wall to reflect the ultrasound calls of bats, enabling them to locate and identify plants in dense vegetation (Schöner et al ., ); montane species which associate mainly with tree shrews ( Tupaia montana ) include (d) N. macrophylla , (e) N. lowii and (f) N. rajah ; examples of divergence of pitcher morphologies across the Sarraceniaceae lineage include hooded pitchers with fenestrations of (g) Sarracenia minor and (h) Darlingonia californica , as well as the open pitfall traps of (i) Sarracenia and (j) Heliamphora . Images not to scale.…”

Ecological outsourcing: a pitcher plant benefits from transferring pre‐digestion of prey to a bat mutualist

“…; Schöner et al . ). The fact that some important traits for prey capture, for example the viscoelastic pitcher fluid, can still be found in N. hemsleyana (Bazile et al .…”

“…; Schöner et al . ; Schöner, Simon & Schöner ). In exchange, these pitcher plants receive multiple benefits: all associated mammals have foraging areas that most likely exceed the catchment area of the plants’ arthropod attractants by far.…”

“…Nepenthes hemsleyana has an enlarged and highly echo‐reflective back wall structure, which helps the bats to find and identify the pitchers (Schöner et al . ). This back wall is on average 57.81% larger than that of N. rafflesiana .…”

“…) and an echo reflector that facilitates pitcher detection and identification by the bats (Schöner et al . ; Schöner, Simon & Schöner ).…”