Function of epidermal surfaces in the trapping efficiency of Nepenthes alata pitchers

Abstract

Summary Several epidermal microstructures characterize surfaces of pitcher plants and are presumably involved in their trapping function. Here we report the effects of Nepenthes alata surfaces on insect locomotion and trapping efficiency. The architectural designs of pitcher surfaces were characterized using scanning electron microscopy. Two insect species – fruitfly (Drosophila melanogaster) and ant (Iridomyrmex humilis) – were tested for their ability to remain and walk on them. The relative contributions of various epidermal structures to trapping ability were quantified. Pitchers were very effective traps for both insect species. They were slightly more efficient in capturing the ants, but slightly more effective in retaining captured flies. Trapping efficiency was attributed to the combined effects of several surfaces displaying different functions. The waxy zone played a key role in the slippery syndrome: in addition to the wax itself, the subjacent layer of convex lunate cells interfered considerably with insect locomotion. The unsubmersed glandular zone displayed an important retentive effect and secretions of the digestive glands are suspected to be adhesive. Pad performances of the hairy and smooth system of attachment are discussed to explain the differences between the two insect species. This study aims to encourage biomechanical studies of plant–insect surface mechanisms.

Harmless nectar source or deadly trap:Nepenthespitchers are activated by rain, condensation and nectar

“…The extreme temporal variation of pitcher capture efficiency has not been documented previously. It explains why the trapping function of the peristome has long remained overlooked (Lloyd 1942;Juniper et al 1989;Gaume et al 2002). Why should a carnivorous plant have evolved a trapping mechanism which is often ineffective and thus seemingly ill designed?…”

Attachment force of the beetle Cryptolaemus montrouzieri (Coleoptera, Coccinellidae) on leaflet surfaces of mutants of the pea Pisum sativum (Fabaceae) with regular and reduced wax coverage

“…Excellent attachment ability on various smooth artificial and natural surfaces has been previously reported for many insects (Way and Murdie 1965;Stork 1980;Edwards 1982;Eigenbrode 1996;Federle et al 2000;Gorb 2002, 2006a). In waxy plant substrates, the deteriorative effect of the crystalline wax coverage on insect attachment has been experimentally shown by many authors (Stork 1980(Stork , 1986Edwards 1982;Bodnaryk 1992;Eigenbrode 1996;Eigenbrode et al 2000;Federle et al 2000;Eigenbrode and Jetter 2002;Gaume et al 2002Gaume et al , 2004Gorb et al 2005;Voigt et al 2007). It has been found for several insect species and a series of plant species that insects can attach well to smooth substrates, without wax or with removed wax bloom, whereas they fail on waxy surfaces.…”

“…Regarding the latter function, it has been previously repeatedly reported that plant surfaces, bearing crystalline wax coverage, reduce the attachment of insects (Stork 1980(Stork , 1986Edwards 1982;Bodnaryk 1992;Eigenbrode 1996;Eigenbrode et al 2000;Federle et al 2000;Eigenbrode and Jetter 2002;Gaume et al 2002Gaume et al , 2004Gorb et al 2005;Voigt et al 2007). In some of these studies, conducted with different insect and plant species, it has been experimentally shown that insects were able to attach successfully to smooth substrates, without wax or with removed wax, but failed on pruinose surfaces.…”

Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface

“…The numerous studies on the function of Nepenthes pitchers have focused on the mechanism of insect attraction (6,7), on the trapping of insects by alkaloid anesthesia (8), by slippery epicuticular wax crystals (3,5,9,10) or by downwardpointing lunate cells (3) of the inner pitcher wall, on the properties of the glandular zone (11), and on the nature of the digestive fluid (12)(13)(14). Only recently, L. Gaume et al (15) conducted the first comprehensive study on the trapping mechanism of Nepenthes by comparing the effect of the different pitcher surface zones and by separating the mechanisms of prey capture and retention. Observations of insects placed on Nepenthes alata pitchers suggested that the inner waxy pitcher wall is the most important surface zone for the initial capture of insects (15).…”

“…Only recently, L. Gaume et al (15) conducted the first comprehensive study on the trapping mechanism of Nepenthes by comparing the effect of the different pitcher surface zones and by separating the mechanisms of prey capture and retention. Observations of insects placed on Nepenthes alata pitchers suggested that the inner waxy pitcher wall is the most important surface zone for the initial capture of insects (15). These results confirmed earlier observations that insects are trapped when they step on the waxy zone while visiting the nectaries on the inner side of the pitcher rim (peristome) (e.g., refs.…”