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First published online July 26, 2004
Journal of Experimental Biology 207, 2947-2963 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01128
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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

Elena Gorb1,*, Victoria Kastner1, Andrei Peressadko1, Eduard Arzt1, Laurence Gaume2, Nick Rowe2 and Stanislav Gorb1

1 Evolutionary Biomaterials Group, Max Planck Institute for Metals Research, Heisenbergstr. 3, D-70569 Stuttgart, Germany
2 Botanique et Bioinformatique de l'Architecture des Plantes, UMR CNRS 5120, Boulevard de la Lironde - TA40/PS2, F-34398 Montpellier, Cedex 5, France



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Fig. 1. Experimental set-up for estimation of material properties by microindentation. SS, sapphire sphere; FOS, fibre optical sensor; GS, glass spring; MR, mirror; PS, plant sample.

 


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Fig. 2. Typical force-distance curves used for evaluation of elasticity and adhesive properties of the surface. (A) Without adhesion. (B) With adhesion. Fa, adhesion force; Fn, maximal applied force; Loading, part of the curve corresponding to the loading process; Retracting, part of the curve corresponding to the retracting process.

 


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Fig. 3. Experimental set-up for friction force measurements (A) and a typical force-time curve (B) used for estimation of maximal friction force (Ffr) generated by insects. FS, force sensor; HR, hair; IN, insect; PC, computer; SC, sensor control; SP, support; TS, tested surface.

 


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Fig. 4. SEM micrographs of the glandular surface. (A) General view of the surface. (B) Gland of the upper part of the digestive zone. (C) Gland of the middle part of the digestive zone. (D) Surface of the gland. (E) Crystals on the gland surface. Arrows show the direction to the peristome. CR, crystal; GL, gland; HD, hood.

 


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Fig. 5. 3-D images (A,C,E) and profiliograms (B,D,F) of different parts of the glandular surface. (A,B) Part between glands (objective 50, magnification 50x0.4). (C,D) Gland in the upper part of the digestive zone (objective 20, magnification 20x1.3). (E,F) Gland in the middle part of the digestive zone (objective 20, magnification 20x2.0). Arrows in A,C,E show the axes for profiles in B,D,F, respectively.

 


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Fig. 6. Anatomy of the digestive zone (light microscopy). (A) Transverse section of the pitcher wall. (B) Longitudinal and (C) transverse sections of the gland, general view. (D) Longitudinal section of the glandular head. (E-G) Transverse sections of the gland. Arrows show the direction to the peristome. CU, cuticle; EC, endodermoid component; ED, epidermal depression; GH, glandular head; HD, hood; IE, inner epidermis; IM, inner margin of the cell wall; IW, internal cell wall; LW, lateral cell wall; ME, mesophyll; OE, outer epidermis; OM, outer margin of the cell wall; OW, outer cell wall; SI, secretion inclusion; SL, second layer of cells; TL, third layer of cells; TR, tracheid element. Scale bar: A,D, 20 µm; B,C,E-G, 50 µm.

 


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Fig. 7. Anatomy of the digestive zone (fluorescence microscopy). (A,B) Transverse section of the gland in a light (A) and fluorescence microscope (B). (C) Whole-mounted surface preparation in a fluorescence microscope. Arrow shows the direction to the peristome. EC, endodermoid component; HD, hood; OW, outer cell wall. Scale bar: 100 µm.

 


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Fig. 8. Microindentation experiments on the glandular surface. (A) Force-time curve indicating that the material of the plant sample exhibited visco-elastic properties. Pitcher surface was loaded during the first 15 s (Load), then kept in contact with the upper sample for the next 45 s (Relaxation). (B) The indentation of the sample vs applied force (points). The solid line indicates the fit of the indentation data with the Hertz theory.

 


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Fig. 9. Dependence of the adhesion force on load. (A) Data of all points on three pitchers. Different symbols correspond to different pitchers. (B,C) Values measured on the same point (selected examples) with increasing applied force. In six out of eight cases, the adhesion increased significantly linearly with the applied force (B), while it remained constant for the other two cases (C). Fa, adhesion force; Fn, applied force.

 


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Fig. 10. Frequency histograms of the distribution of points with different values of the adhesion force (A) and the tenacity (B). Only the value of the first test at each point was taken into account.

 


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Fig. 11. Attachment devices of insect species studied. (A-C) Smooth pulvilli of the bug Pyrrhocoris apterus. (A) Distal part of the tarsus, lateral aspect. (B) Pretarsus, ventral aspect. (C) Surface of the pulvillus. (D,E) Hairy pulvilli of the fly Calliphora vicina. (D) Right pulvillus. (E) Tenent setae with the terminal elements (spatulae). CL, claws; HK, hooked setae; la, lateral direction; PU, pulvilli; SP, spatulae; TA, terminal tarsomere; UT, unguitractor plate; ve, ventral direction.

 


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Fig. 12. Maximal friction force generated by insects on different substrates. (A) Comparison between three surfaces tested. (B) Comparison between two insect species. According to the Ryan-Eliot-Gabriel-Welsh test of multiple comparisons of means, run after ANOVA, means with different letters differ significantly from each other.

 





© The Company of Biologists Ltd 2004