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

Zoologie II, Biozentrum, Am Hubland, 97074 Würzburg, Germany.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 10/2004; 101(39):14138-43. DOI: 10.1073/pnas.0405885101
Source: PubMed


Pitcher plants of the genus Nepenthes have highly specialized leaves adapted to attract, capture, retain, and digest arthropod prey. Several mechanisms have been proposed for the capture of insects, ranging from slippery epicuticular wax crystals to downward-pointing lunate cells and alkaloid secretions that anesthetize insects. Here we report that perhaps the most important capture mechanism has thus far remained overlooked. It is based on special surface properties of the pitcher rim (peristome) and insect "aquaplaning." The peristome is characterized by a regular microstructure with radial ridges of smooth overlapping epidermal cells, which form a series of steps toward the pitcher inside. This surface is completely wettable by nectar secreted at the inner margin of the peristome and by rain water, so that homogenous liquid films cover the surface under humid weather conditions. Only when wet, the peristome surface is slippery for insects, so that most ant visitors become trapped. By measuring friction forces of weaver ants (Oecophylla smaragdina) on the peristome surface of Nepenthes bicalcarata, we demonstrate that the two factors preventing insect attachment to the peristome, i.e., water lubrication and anisotropic surface topography, are effective against different attachment structures of the insect tarsus. Peristome water films disrupt attachment only for the soft adhesive pads but not for the claws, whereas surface topography leads to anisotropic friction only for the claws but not for the adhesive pads. Experiments on Nepenthes alata show that the trapping mechanism of the peristome is also essential in Nepenthes species with waxy inner pitcher walls.

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    • "Although N. hemsleyana obtains about a third of its total foliar nitrogen from the feces or urine of K. hardwickii (Grafe et al., 2011), the ability of its pitchers to trap insects, albeit reduced (Moran, 1996), suggests that N. hemsleyana follows a dual strategy of nitrogen acquisition. The orifice diameter of N. hemsleyana is significantly larger than that of N. rafflesiana, but it retains the ability to trap arthropod prey by aquaplaning when the peristome is wet [whether by rain, humidity or nectar (Bohn and Federle, 2004; Bauer et al., 2009, 2011, 2015)]. The wettable peristome and the long waxy zone between the peristome and the girdle are nearly 100% effective in retaining prey that has fallen into the pitcher (Gaume and Di Giusto, 2009; Bauer et al., 2011). "
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    ABSTRACT: Question: How does the pitcher plant Nepenthes hemsleyana facilitate roosting of mutualistic bats? Hypothesis: Pitchers have adaptations that match the shape and body size of small woolly bats. Organisms: The pitcher plant Nepenthes hemsleyana, its close relative N. rafflesiana, and the woolly bat Kerivoula hardwickii. Field sites: Peat swamps and heath forests in western Brunei Darussalam on the island of Borneo. Methods: We measured various morphological traits of N. hemsleyana that might facilitate bat roosting. We compared these traits with those of N. rafflesiana, which is not visited by bats. We compared the sizes and characteristics of the pitchers with the body sizes of roosting bats. Conclusions: As predicted, aerial pitchers matched the body size of bats and had lower digestive fluid levels than pitchers of a close relative. Thus, small morphological differences between closely related species have caused rapid dietary niche divergence.
    Evolutionary ecology research 08/2015; 16:581-591. · 0.90 Impact Factor
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    • "Wetting phenomenon occurs when a solid–gas interface turns into a solid–liquid interface on a solid surface [1]. It is a critical issue in controlling the wettability of solid materials in surface engineering, including oil recovery, lubrication, coating, sealing, printing and liquid adhesion [2] [3] [4] [5] [6] [7]. For example, the flange surfaces is usually designed and processed to the expected spiral lay so as to obtain strong anisotropic wettability, which performs a better sealing effect. "
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    ABSTRACT: Anisotropic wetting of machined surfaces is widely applied in industries which can be greatly affected by roughness and solid's chemical properties. However, there has not been much work on it. A free-energy thermodynamic model is presented by analyzing geometry morphology of machined surfaces (2-D model surfaces), which demonstrates the influence of roughness on anisotropic wetting. It can be concluded that the energy barrier is one of the main reasons for the anisotropic wetting existing in the direction perpendicular to the lay. In addition, experiments in investigating anisotropic wetting, which was characterized by the static contact angle and droplet's distortion, were performed on machined surfaces with different roughness on hydrophilic and hydrophobic materials. The droplet's anisotropy found on machined surfaces increased with mean slope of roughness profile Kr. It indicates that roughness on anisotropic wetting on hydrophilic materials has a stronger effect than that on hydrophobic materials. Furthermore, the contact angles predicted by the model are basically consistent with the experimentally ones.
    Applied Surface Science 03/2015; 331. DOI:10.1016/j.apsusc.2014.12.071 · 2.71 Impact Factor
    • "The peristome surface is characterised by an intricate micro-pattern which, in most species, renders it highly wettable. While the surface is safe for insects to walk on when dry, it turns extremely slippery when it is wetted by rain or condensation (Bohn and Federle 2004; Bauer et al. 2008). While most Nepenthes trap insects, some species have recently been shown to engage in mutualistic relationships with vertebrates (Clarke et al. 2009; Grafe et al. 2011; Greenwood et al. 2011). "
    Bauer · Rembold · Grafe ·
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    ABSTRACT: Carnivorous pitcher plants capture insect prey to acquire essential nutrients while growing on extremely poor soils. A few individual species have evolved mutualistic relationships with small mammals that visit the traps to harvest nectar, and in return leave faecal droppings in the pitchers. Here we report that a diverse guild of nectar-harvesting vertebrates visits pitchers of two common lowland Nepenthes species without providing any obvious benefit for the plants. Over four consecutive field seasons, we observed four species of sunbirds and one species of tree shrew drinking nectar from pitcher plants. Foraging activity was highest in the morning and late afternoon. Van Hasselt’s, Brown-throated and olive-backed sunbirds were regular and highly abundant pitcher visitors in two different field sites. A crimson sunbird and a lesser tree shrew were each observed harvesting nectar on one occasion. The vertebrates harvested nectar from the pitcher rim (peristome) of N. rafflesiana and from the underside of the pitcher lid of N. gracilis. A comparison of the nectar production of these and three further sympatric species revealed exceptionally high quantities of nectar for N. rafflesiana. Other factors such as plant and pitcher abundance and the habitat preferences of the observed vertebrates are likely to also play a role in their choice to visit particular species. This is the first account of a case of obvious nectar robbing from Nepenthes pitchers by a guild of species that are too large to serve as prey, while the pitcher size and shape prevent faecal droppings from reaching the pitcher’s inside. This interaction provides an example of a possible starting point for the evolution of the elaborate mutualistic relationships observed in some species. Follow-up adaptations of pitcher shape could enable the plants to catch the droppings of their visitors and turn an exploitative relationship into a mutualism.
    Journal of Natural History 01/2015; DOI:10.1080/00222933.2015.1059963 · 0.88 Impact Factor
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