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Structure and properties of the glandular surface in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention

Abstract : Carnivorous plants of the genus Nepenthes grow in nutrient-poor habitats and have evolved specialised trapping organs, known as pitchers. These are composed of different surface zones serving the functions of attraction, capture and digestion of insects, which represent a main source of nitrogen. To investigate the role of the glandular digestive zone in the trapping mechanism of the pitcher, structural, mechanical and physico-chemical studies were applied to N. ventrata and combined with insect behavioural experiments. It was found that the glandular surface is microscopically rough since it is regularly structured with multicellular glands situated in epidermal depressions. The presence of downward-directed ‘hoods’ over the upper part of glands and sloped depressions in the proximal direction of the pitcher causes a marked anisotropy of the surface. The glandular zone surface is composed of relatively stiff material (Young’s modulus, 637.19±213.44·kPa). It is not homogeneous, in terms of adhesive properties, and contains numerous areas without adhesion as well as adhesive areas differing greatly in tenacity values (range, 1.39–28.24·kPa). The surface is readily wettable with water (contact angle, 31.9–36.0°C) and has a high surface free energy (56.84–61.93·mN·m–1) with a relatively high polar component (33.09–52.70·mN·m–1). To examine the effect of the glandular secretion on attachment systems of insects having hairy and smooth adhesive pads, forces generated on different surfaces by Calliphora vicina flies and Pyrrhocoris apterus bugs, respectively, were measured. Flies attached equally well to both fresh and air-dried glandular surfaces whereas bugs generated a significantly lower force on the fresh glandular surface compared with the air-dried one. It is assumed that the contribution of the glandular surface to insect retention, due to its effect on insect attachment, differs depending on insect weight and the type of insect attachment system. Surface anisotropy does not facilitate effective claw interlocking so that insects possessing only claws are probably not able to cling to the glandular surface. However, stiffness of the pitcher wall material in the digestive zone can provide claw clinging via punching of the pitcher wall by claws. Small insects lacking pads may use adhesive areas on the plant surface to attach themselves, but such solitary points with very strong adhesion possibly impede their overall locomotion and chance of escape. Pad-bearing insects are presumably able to attach to smooth parts of the glandular surface located between glands. High free surface energy of the plant substrate may promote adhesion. Gland secretion may decrease attachment ability in insects with smooth adhesive pads but not influence attachment of insects with hairy attachment systems.
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Elena Gorb, Victoria Kastner, Andrei Peressadko, Eduard Arzt, Laurence Gaume, et al.. Structure and properties of the glandular surface in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention. Journal of Experimental Biology, Cambridge University Press, 2004, 207 (17), pp.2947-2963. ⟨10.1242/jeb.01128⟩. ⟨hal-02388688⟩



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