The Waxy Surface in Nepenthes Pitcher Plants: Variability, Adaptive Significance and Developmental Evolution

Giusto, Bruno Di; Guéroult, Michaël; Rowe, Nick; Gaume, Laurence

doi:10.1007/978-1-4020-6695-5_8

Cited by 7 publications

(14 citation statements)

References 19 publications

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“…In N. rafflesiana , the slippery waxy surface of the pitchers was shown to play a minor role in the trapping function of the plant, being even a variable character of weak adaptive significance [13]. In contrast, the viscoelastic and retentive properties of the fluid are probably crucial for this tropical plant often submitted to high rainfall regimes and great variation in fluid concentration, since they persist at high dilutions by water, thereby allowing insect trapping during rainy seasons.…”

Section: Discussionmentioning

confidence: 99%

“…However, some Nepenthes species lack such specialized surfaces [12] or lose them later in development [13] suggesting that the trapping mechanism of Nepenthes pitcher plants is more complex than commonly acknowledged. Moreover, reports of secretion of wetting agents [3] or viscous substances [14] in some species point to other potential roles of the digestive fluid.…”

Section: Introductionmentioning

confidence: 99%

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A Viscoelastic Deadly Fluid in Carnivorous Pitcher Plants

Gaume

Forterre

2007

PLoS ONE

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BackgroundThe carnivorous plants of the genus Nepenthes, widely distributed in the Asian tropics, rely mostly on nutrients derived from arthropods trapped in their pitcher-shaped leaves and digested by their enzymatic fluid. The genus exhibits a great diversity of prey and pitcher forms and its mechanism of trapping has long intrigued scientists. The slippery inner surfaces of the pitchers, which can be waxy or highly wettable, have so far been considered as the key trapping devices. However, the occurrence of species lacking such epidermal specializations but still effective at trapping insects suggests the possible implication of other mechanisms.Methodology/Principal FindingsUsing a combination of insect bioassays, high-speed video and rheological measurements, we show that the digestive fluid of Nepenthes rafflesiana is highly viscoelastic and that this physical property is crucial for the retention of insects in its traps. Trapping efficiency is shown to remain strong even when the fluid is highly diluted by water, as long as the elastic relaxation time of the fluid is higher than the typical time scale of insect movements.Conclusions/SignificanceThis finding challenges the common classification of Nepenthes pitchers as simple passive traps and is of great adaptive significance for these tropical plants, which are often submitted to high rainfalls and variations in fluid concentration. The viscoelastic trap constitutes a cryptic but potentially widespread adaptation of Nepenthes species and could be a homologous trait shared through common ancestry with the sundew (Drosera) flypaper plants. Such large production of a highly viscoelastic biopolymer fluid in permanent pools is nevertheless unique in the plant kingdom and suggests novel applications for pest control.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A Viscoelastic Deadly Fluid in Carnivorous Pitcher Plants

Gaume

Forterre

2007

PLoS ONE

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“…Pitchers lacking both lunate cells and wax were found only in a few species from this genus, such as N. ampularia [29], N. bicalcarata [8,16,32–35], N. rafflesiana [13,36], and N. veitchii [37]. …”

Section: Discussionmentioning

confidence: 99%

The effect of surface anisotropy in the slippery zone of Nepenthes alata pitchers on beetle attachment

Gorb¹,

Gorb²

2011

Beilstein J. Nanotechnol.

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SummaryThe slippery zone in pitchers of the carnivorous plant Nepenthes alata bears scattered prominent lunate cells and displays continuous epicuticular crystalline wax coverage. The aim of this study was to examine the influence of the surface anisotropy, caused by the shape of lunate cells, on insect attachment ability. Traction tests with ladybird beetles Coccinella septempunctata were performed in two types of experiments, where surface samples of (1) intact pitchers, (2) chemically de-waxed pitchers, and (3) their polymer replicas were placed horizontally. Beetle traction forces were measured when they walked on test surfaces in either an upward (towards the peristome) or downward (towards the pitcher bottom) direction, corresponding to the upright or inverted positions of the pitcher. On intact pitcher surfaces covered with both lunate cells and wax crystals, experiments showed significantly higher forces in the direction towards the pitcher bottom. To distinguish between the contributions, from claw interlocking and pad adhesion, to insect attachment on the pitcher surfaces, intact versus claw-ablated beetles were used in the second type of experiment. On both de-waxed plant samples and their replicas, intact insects generated much higher forces in the downward direction compared to the upward one, whereas clawless insects did not. These results led to the conclusion that, (i) due to the particular shape of lunate cells, the pitcher surface has anisotropic properties in terms of insect attachment, and (ii) claws were mainly responsible for attachment enhancement in the downward pitcher direction, since, in this direction, they could interlock with overhanging edges of lunate cells.

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“…Most of them are vines characterized by an ontogenetic pitcher dimorphism with young rosette or self-supporting plants exhibiting terrestrial pitchers of the "lower" type and older climbing plants exhibiting aerial pitchers of the "upper" type (Cheek and Jebb 2001;Di Giusto et al 2008). Until recently, most studies aimed at elucidating the trapping mechanism of Nepenthes pitcher plants focused on the capture and retentive function of slippery surfaces with a special emphasis on the waxy layer that covers the upper inner part of the pitcher in most Nepenthes species (Juniper and Burras 1962;Juniper et al 1989;Gaume et al 2002Gaume et al , 2004Gorb et al 2005).…”

Section: Introductionmentioning

confidence: 99%

“…A study also reported that the trapping surface was the peristome or nectar rim of the pitcher in N. bicalcarata (Bohn and Federle 2004). Nevertheless, some Nepenthes species are polymorphic with regard to the presence of a waxy layer (Lloyd 1942;Di Giusto et al 2008), while others are monomorphic for the absence of this layer. The presence and size of the peristome is also variable among species (Cheek and Jebb 2001).…”

Section: Introductionmentioning

confidence: 99%

Contribution of pitcher fragrance and fluid viscosity to high prey diversity in a Nepenthes carnivorous plant from borneo

et al. 2008

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Mechanisms that improve prey richness in carnivorous plants may involve three crucial phases of trapping:attraction, capture and retention. Nepenthes rafflesiana var. typica is an insectivorous pitcher plant that is widespread in northern Borneo. It exhibits ontogenetic pitcher dimorphism with the upper pitchers trapping more flying prey than the lower pitchers. While this difference in prey composition has been ascribed to differences in attraction,the contribution of capture and retention has been overlooked. This study focused on distinguishing between the prey trapping mechanisms, and assessing their relative contribution to prey diversity. Arthropod richness and diversity of both visitors and prey in the two types of pitchers were analysed to quantify the relative contribution of attraction to prey trapping. Rate of insect visits to the different pitcher parts and the presence or absence of a sweet fragrance was recorded to clarify the origin and mechanism of attraction. The mechanism of retention was studied by insect bioassays and measurements of fluid viscosity. Nepenthes rafflesiana was found to trap a broader prey spectrum than that previously described for any Nepenthes species,with the upper pitchers attracting and trapping a greater quantity and diversity of prey items than the lower pitchers. Capture efficiency was low compared with attraction or retention efficiency. Fragrance of the peristome,or nectar rim,accounted mainly for the observed non-specific, better prey attraction by the upper pitchers, while the retentive properties of the viscous fluid in these upper pitchers arguably explains the species richness of their flying prey. The pitchers of N. rafflesiana are therefore more than simple pitfall traps and the digestive fluid plays an important yet unsuspected role in the ecological success of the species.

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The Waxy Surface in Nepenthes Pitcher Plants: Variability, Adaptive Significance and Developmental Evolution

Cited by 7 publications

References 19 publications

A Viscoelastic Deadly Fluid in Carnivorous Pitcher Plants

A Viscoelastic Deadly Fluid in Carnivorous Pitcher Plants

The effect of surface anisotropy in the slippery zone of Nepenthes alata pitchers on beetle attachment

Contribution of pitcher fragrance and fluid viscosity to high prey diversity in a Nepenthes carnivorous plant from borneo

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