Biomechanics and ecology of the interaction between insects and plant surfaces

Project leader: Walter Federle

Staff: Tanja Günther (since 2002), Patrick Drechsler (since 2002), Thomas Endlein (since 2003), Holger Bohn (since 2003)

Objectives: The objective of our work is an integrative approach to study the ecology and biomechanics of insect attachment to the plant surface. The project spans three hierarchical levels ranging from the ecological function to the detailed mechanism: 1) Proximate mechanisms of insect-plant interactions 2) Interaction between attachment and locomotion and 3) Mechanism of surface adhesion and friction in insects.

Approach: We use a variety of biomechanical methods ranging from force measurement at different size scales, morphometry, interference reflection microscopy, atomic force microscopy and high speed motion analysis. In addition to experimental laboratory work, we study insect behavior under natural conditions by doing field work in SE Asia.

Progress: 1) Our research demonstrates that mechanical factors can play a key role in insect-plant interactions. In the mutualism between ants and Macaranga trees, slippery 'wax barriers' not only act as filters favoring specialist over generalist ants but also represent an ecological isolation mechanism which gives rise to host specificity. The presence or absence of slippery wax barriers has a variety of ecological and evolutionary implications for Macaranga-ant associations. We have discovered that 'wax-running' in Crematogaster (Decacrema) ants is based on a combination of special morphological and locomotory adaptations.

2) We have discovered that ants can dynamically control attachment according to surface and loading conditions. Control of adhesion is largely achieved by non-neuronal 'preflexes' based on inherent mechanical properties of the tarsal system, which complement a relatively simple active control.

3) We were able to quantify the physical properties of insect adhesive secretion. These studies have shown that the classical 'wet adhesion' model used to explain insect surface attachment is insufficient to explain observed forces and has to be replaced by a combined wet adhesion–rubber friction model.

Significance: The integrative study of the biomechanics of insect attachment to plant surfaces not only provides insight into the ecology of specific insect-plant interactions but also into general principles employed in nature. Research on the mechanism of surface adhesion and on the techniques insects use to dynamically control adhesion has the potential to yield inspiration for the development of biomimetic adhesives and climbing robots. Moreover, our work has revealed underlying mechanisms of insect-plant interactions, which would be incomprehensible without a biomechanical analysis.

Future projects: The analysis of ant-plant interactions in the genus Macaranga will be extended by quantifying the mechanical properties of slippery wax crystals, by performing a comparative biomechanical characterization of wax-running behavior and by clarifying the evolutionary role of wax barriers in Macaranga-ant speciation processes. Our studies on the control mechanisms involved in surface attachment of ants will be extended to other types of attachment organs and to other insect orders. Further studies on the general biomechanics of insect adhesion will focus on the material properties of adhesive cuticle and its interaction with different substrates.

Collaborations: On Macaranga-ant associations with Heike Feldhaar, Brigitte Fiala, Jürgen Gadau (Biocenter Würzburg), Markus Riederer (Botany II, Würzburg) and Ulrich Maschwitz (Frankfurt University), on tree frog adhesion with Jon Barnes (Glasgow University), on the biophysics of adhesive pads with Werner Baumgartner (Anatomy and cell biology, Würzburg) and on insect locomotion with Robert Full (UC Berkeley).

Publications:

Current external funding: Emmy Noether Programme

Emmy Noether- Programme (DFG-FE547/1), Sonderforschungsbereich 567 / TP C6

Selective barrier effect of waxy stems in Macaranga ant-plants. The wax coating has been wiped off in the lower part of the stem. Due to their slippery surface, waxy Macaranga trees are inaccessible to most generalist ants (e.g. Crematogaster cf. artifex, below). Only the specialist ant partners (Crematogaster (Decacrema) msp.2, above) are capable of climbing the stems without any difficulty and are thus well protected against predators and competitors.

Interference reflection microscopy image of a Weaver ant adhesive pad in contact with glass showing the hydrophilic and hydrophobic phases of insect adhesive secretion (scale bar=5µm).

Extreme attachment performance in Weaver ants (Oecophylla smaragdina). Workers are capable of carrying more than 100 times their own body weight upside down on perfectly smooth surfaces.