Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Comparative and functional morphology of hierarchically structured anti-adhesive surfaces in carnivorous plants and kettle trap flowers

Simon Poppinga A C , Kerstin Koch B , Holger Florian Bohn A C and Wilhelm Barthlott A D
+ Author Affiliations
- Author Affiliations

A Nees-Institut für Biodiversität der Pflanzen, Meckenheimer Allee 170, D-53115 Bonn, Germany.

B University of Applied Science, Rhine-Wall, Landwehr 4, D-47533 Kleve, Germany.

C Present address: Plant Biomechanics Group Freiburg, University of Freiburg, Schänzlestrasse 1, D-79104 Freiburg im Breisgau, Germany.

D Corresponding author. Email: barthlott@uni-bonn.de

Functional Plant Biology 37(10) 952-961 https://doi.org/10.1071/FP10061
Submitted: 19 March 2010  Accepted: 14 June 2010   Published: 23 September 2010

Abstract

Plant surfaces that are slippery for insects have evolved independently several times in the plant kingdom, mainly in the groups of carnivorous plants and kettle trap flowers. The surface morphologies of 53 species from both groups were investigated by scanning electron microscopy. It was found that the surfaces possess highly diverse topographical structures. We present a classification of 12 types of anti-adhesive surfaces, in regard to the assembly and hierarchy of their structural elements. The observed structural elements are different combinations of epidermal cell curvatures with cuticular folds or 3D epicuticular wax crystals and idioblastic elements.

Additional keywords: insect attachment, pitcher trap, surface microstructure.


Acknowledgements

The authors thank the Akademie der Wissenschaften und Literatur Mainz (long-term project ‘Biodiversität im Wandel’) for their financial support, and Prof. F. Albers and Melanie Wiethölter from the Botanical Garden of Münster for providing plant material.


References


Barthlott W, Ehler N (1977) Raster-Elektronenmikroskopie der Epidermis-Oberflächen von Spermatophyten. Tropische und Subtropische Pflanzenwelt 19, 110. open url image1

Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, Wilhelmi H (1998) Classification and terminology of plant epicuticular waxes. Botanical Journal of the Linnean Society 126, 237–260.
CrossRef | open url image1

Barthlott W , Porembski S , Seine R , Theisen I (2007) ‘Carnivorous plants: a comprehensive guide to their biology and cultivation.’ (Timber Press: Portland)

Beutel RG, Gorb SN (2001) Ultrastructure of attachment specializations of hexapods (Arthropoda): evolutionary patterns inferred from a revised ordinal phylogeny. Journal of Zoological Systematics and Evolutionary Research 39, 177–207.
CrossRef | open url image1

Bhushan B, Koch K, Jung YC (2008) Biomimetic hierarchical structure for self-cleaning. Applied Physics Letters 93, 093101.
CrossRef | open url image1

Bohn HF, Federle W (2004) Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Proceedings of the National Academy of Sciences of the United States of America 101, 14138–14143.
CrossRef | CAS | PubMed | open url image1

Bolin JF, Maass E, Musselman LJ (2009) Pollination biology of Hydnora africana Thunb. (Hydnoraceae) in Namibia: brood-site mimicry with insect imprisonment. International Journal of Plant Sciences 170(2), 157–163.
CrossRef | open url image1

Cammerloher H (1923) Zur Biologie der Blüte von Aristolochia grandiflora Swartz. Österreichische Botanische Zeitschrift 72, 180–198.
CrossRef | open url image1

Daumann E (1968) Zur Bestäubungsökologie von Cypripedium calceolus L. Österreichische Botanische Zeitschrift 115, 434–446.
CrossRef | open url image1

Ensikat HJ, Barthlott W (1993) Liquid substitution – a versatile procedure for SEM specimen preparation of biological materials without drying or coating. Journal of Microscopy 172, 195–203.
CAS | PubMed |
open url image1

Federle W, Maschwitz U, Fiala B, Riederer M, Hölldobler B (1997) Slippery ant-plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae). Oecologia 112, 217–224.
CrossRef | open url image1

Gaume L, Gorb S, Rowe N (2002) Function of epidermal surfaces in the trapping efficiency of Nepenthes alata pitchers. The New Phytologist 156, 479–489.
CrossRef | open url image1

Gaume L, Perret P, Gorb E, Gorb S, Labat JJ, Rowe N (2004) How do plant waxes cause flies to slide? Experimental tests of wax-based trapping mechanisms in three pitfall carnivorous plants. Arthropod Structure & Development 33, 103–111.
CrossRef | CAS | PubMed | open url image1

Gorb SN (2001) ‘Attachment devices of insect cuticle.’ (Kluwer Academic Publishers: London)

Gorb SN (2008a) Smooth attachment devices in insects: functional morphology and biomechanics. Advances in Insect Physiology 34, 81–115.
CrossRef | open url image1

Gorb SN (2008b) Biological attachment devices: exploring nature’s diversity for biomimetics. Philosophical Transactions. Series A, Mathematical, Physical, and Engineering Sciences 366, 1557–1574.
CrossRef | PubMed | open url image1

Gorb EV, Gorb SN (2002) Attachment ability of the beetle Chrysolina fastuosa on various plant surfaces. Entomologia Experimentalis et Applicata 105, 13–28.
CrossRef | open url image1

Gorb E, Haas K, Henrich A, Enders S, Barbakadze N, Gorb SN (2005) Composite structure of the crystalline epicuticular wax layer of the slippery zone in the pitchers of the carnivorous plant Nepenthes alata and its effect on the insect attachment. The Journal of Experimental Biology 208, 4651–4662.
CrossRef | CAS | PubMed | open url image1

Gusman G , Gusman L (2002) ‘The genus Arisaema: a monograph for botanists and nature lovers.’ (Gantner: Ruggell)

Hall DW, Brown BV (1993) Pollination of Aristolochia littoralis (Aristolochiales: Arisolochiaceae) by males of Megaselia spp. (Diptera: Phoridae). Annals of the Entomological Society of America 86, 609–613. open url image1

Juniper BE, Burras JK (1962) How pitcher plants trap insects. New Scientist 269, 75–77. open url image1

Juniper BE , Robins RJ , Joel DM (1989) ‘The carnivorous plants.’ (Academic Press: London)

Knoll F (1914) Über die Ursache des Ausgleitens der Insektenbeine an wachsbedeckten Pflanzenteilen. Jahrbücher für Wissenschaftliche Botanik 54, 448–497. open url image1

Knoll F (1926) Die Arum-Blütenstande und ihre Besucher. Abhandlungen der Zoologisch – Botanischen Gesellschaft Wien 12, 382–481. open url image1

Koch K, Bhushan B, Barthlott W (2009a) Multifunctional surface structures of plants: an inspiration for biomimetics. Progress in Materials Science 54, 137–178.
CrossRef | CAS | open url image1

Koch K, Bhushan B, Jung YC, Barthlott W (2009b) Fabrication of artificial lotus leaves and significance of hierarchical structure for superhydrophobicity and low adhesion. Soft Matter 5, 1386–1393.
CrossRef | CAS | open url image1

Lloyd FE (1942) ‘The carnivorous plants.’ (Chronica Botanica: Waltham)

Markstädter C, Federle W, Jetter R, Riederer M, Hölldobler B (2000) Chemical composition of the slippery epicuticular wax blooms on Macaranga (Euphorbiaceae) ant-plants. Chemoecology 10, 33–40.
CrossRef | open url image1

Mayo SJ , Bogner J , Boyce PC (1997) ‘The genera of Araceae.’ (Royal Botanic Gardens: Kew)

Nishizawa T, Watano Y, Kinoshita E, Kawahara T, Ueda K (2005) Pollen movement in a natural population of Arisaema serratum (Araceae), a plant with a pitfall-trap flower pollination system. American Journal of Botany 92, 1114–1123.
CrossRef | open url image1

Oelschlägel B, Gorb S, Wanke S, Neinhuis C (2009) Structure and biomechanics of trapping flower trichomes and their role in the pollination biology of Aristolochia plants (Aristolochiaceae). New Phytologist 184(4), 988–1002.
CrossRef | PubMed | open url image1

Ollerton J, Liede S (1997) Pollination systems in the Asclepiadaceae: a survey and preliminary analysis. Biological Journal of the Linnean Society. Linnean Society of London 62, 593–610.
CrossRef | open url image1

Ollerton J, Masinde S, Meve U, Picker M, Whittington A (2009) Fly pollination in Ceropegia (Apocynaceae: Asclepiadoideae): biogeographic and phylogenetic perspectives. Annals of Botany 103, 1501–1514.
CrossRef | PubMed | open url image1

Peressadko A, Gorb S (2004) When less is more: experimental evidence for tenacity enhancement by division of contact area. The Journal of Adhesion 80, 247–261.
CrossRef | CAS | open url image1

Riedel M, Eichner A, Jetter R (2003) Slippery surfaces of carnivorous plants: composition of epicuticular wax crystals in Nepenthes alata Blanco pitchers. Planta 218, 87–97.
CrossRef | CAS | PubMed | open url image1

Vogel S (1965) Kesselfallen-Blumen. Die Umschau in Wissenschaft und Technik 65, 12–17. open url image1

Vogel S, Martens J (2000) A survey of the function of the lethal kettle traps of Arisaema (Araceae), with records of pollinating fungus gnats from Nepal. Botanical Journal of the Linnean Society 133, 61–100.
CrossRef | open url image1

Whitney HM, Chittka L, Bruce TJA, Glover BJ (2009) Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Current Biology 19, 948–953.
CrossRef | CAS | PubMed | open url image1

Wolda H, Sabrosky CW (1986) Insect visitors to two forms of Aristolochia pilosa in Las Cumbres, Panama. Biotropica 18, 295–299.
CrossRef | open url image1








Rent Article (via Deepdyve) Export Citation Cited By (16)

View Altmetrics