Author: Austin Garner

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The adhesive structures of geckos have been the subject of extensive inquiry across a variety of disciplines ever since Autumn et al. (2002) discovered that van der Waals intermolecular forces are the main driver of gecko adhesion. Geckos adhere to surfaces using expanded subdigital scales (scansors/lamellae) that are covered in thousands of beta-keratin fibrils (setae) that branch into hundreds or thousands of triangular-shaped tips (spatulae) that are about 200 nanometers in width (see slideshow for images). Spatulae make intimate contact with a surface resulting in van der Waals intermolecular forces. Gecko adhesive toe pads are multifunctional; they are a reversible dry adhesive, they can adhere to a variety of surfaces, they can adhere underwater in some conditions, they have self-cleaning and self-drying capabilities, and they can adhere in a vacuum (see Autumn et al. 2014 for a recent review of gecko adhesion). A number of gecko-inspired synthetic adhesives have been generated over the years, but have not yet managed to replicate the multifunctionality observed in the natural system (Niewiarowski et al. 2016). There are a number of potential explanations for this, but one could be that most gecko-inspired synthetic adhesives are simplified single fibers that do not fully replicate the multiply branched structure of gecko setae. Anoles, however, have independently evolved adhesive toe pads with fundamentally simpler microstructures compared to their gecko counterparts; anole setae are single fibers with a single, larger spatulate tip and more closely resemble the gecko-inspired synthetic adhesives that are currently capable of being generated (see slideshow for images). Therefore, anoles may be an excellent model fibrillar system to better understand the observed functional discrepancy between synthetic and natural fibrillar adhesives.

In an invited paper recently accepted for publication in Integrative and Comparative Biology, my co-authors and I (see full citation below) briefly reviewed the relevant literature concerning the anole adhesive system, discussed how investigation of this convergently evolved system could impact our general understanding of fibrillar adhesion, and suggested a number of hypotheses and areas of future inquiry that could be tackled in future work.

Anole adhesive toe pads have often been suggested as evolutionary key innovations (Losos 2011), yet they have not been nearly as well studied as gecko adhesive toe pads. Nevertheless, general morphometrics, clinging ability on smooth substrates, and correlations between adhesive toe pad size, clinging ability, and habitat use have been reported for anoles (Losos 2011). Studies, however, reporting Anolis clinging ability on ecologically-relevant surfaces, detailed morphometric data of anoline setae, and the multifunctional properties of anoline adhesive toe pads are limited or nonexistent. Anoles may be excellent models for fibrillar adhesion for four main reasons: (1) anole setae are closer in dimensions and morphology to the currently producible gecko-inspired synthetic adhesives, (2) anole setae are not multiply branched which may reduce the complexity of modeling and/or explaining adhesion especially under non-ideal circumstances, (3) anole setae also more closely resemble the theoretical models previously used to explain gecko adhesion, and (4) the extensive evolutionary and ecological data on anoles may assist in answering persisting questions regarding the adhesion ecology and evolution of adhesive pad-bearing lizards.

Although the gecko adhesive system has been particularly well-studied over the past two decades, many fundamentals of biological fibrillar adhesion still need to be worked out or are otherwise unknown. We believe that parallel investigation of the anoline fibrillar adhesive system may assist in filling these gaps in our knowledge, and thus we encourage an interdisciplinary, communal effort to investigate the adhesive ecology, evolution, morphology, performance, and behavior of anoles.

Full citation

Garner, A.M., M.C. Wilson, A.P. Russell, A. Dhinojwala, and P.H. Niewiarowski. Going Out on a Limb: How Investigation of the Anoline Adhesive System can Enhance our Understanding of Fibrillar Adhesion. Integrative and Comparative Biology. In press. Link to article.

References

Autumn K, Niewiarowski PH, Puthoff JB. 2014. Gecko Adhesion as a Model System for Integrative Biology, Interdisciplinary Science, and Bioinspired Engineering. Annual Review of Ecology, Evolution and Systematics 45(1):445-470.

Autumn K, Sitti M, Liang YA, Peattie AM, Hansen WR, Sponberg S, Kenny TW, Fearing R, Israelachvili JN, Full RJ. 2002. Evidence for van der Waals adhesion in gecko setae. Proceedings of the National Academy of Sciences, USA 99(19):12252-12256.

Losos JB. 2011. Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press.

Niewiarowski PH, Stark AY, Dhinojwala A. 2016. Sticking to the story: outstanding challenges in gecko-inspired adhesives. Journal of Experimental Biology 219(7):912-919.

Figure 1. Differences in claw clipping used in Bloch and Irschick (2005) and our study. (A) Bloch and Irschick (2005) clipped the entire claw after the distal end of the toe pad. (B) In our study, we partially clipped the distalmost portion of the claw.

Toe and claw clipping are common techniques used to identify individuals in mark and recapture studies, but their impacts on whole organism performance are unclear (Dunham et al., 1988). Anoles have not only developed subdigital adhesive toe pads to promote adhesion on relatively smooth substrates, but have also retained claws to enhance attachment to rough substrates (Irschick et al., 1996; Zani, 2000). Thus, clipping entire toes or claws may have drastic effects on the clinging ability of anoles or other adhesive pad-bearing lizards. In our recent article published in Acta Herpetologica, my co-authors and I investigated how partially removing the claws of brown anoles affects their adhesive performance.

Figure 2. Mean maximum clinging force of Anolis sagrei with intact and partially clipped claws. Overall, partial claw clipping had no significant effect on maximum clinging ability.

Bloch and Irschick (2005) removed entire claws from Anolis carolinensis (Fig. 1A) and measured its impact on their clinging ability. Not surprisingly, claw removal resulted in a significant decrease in the clinging ability of A. carolinensis, likely a consequence of the severing of flexor tendons that are critical in adhesive toe pad engagement. In an effort to test this hypothesis and preserve these tendons, we used a motorized force sensor (Niewiarowski et al., 2008) to measure the maximum clinging ability of 19 Anolis sagrei before and after their claws were partially clipped (Fig. 1B).

Overall, we found that partial claw clipping did not significantly impact maximum clinging ability (Figure 2). This suggests that clipping the entire claws of anoles may indeed sever the flexor tendons crucial to toe pad engagement. Furthermore, we expected clinging ability to increase after partial claw clipping because claws should theoretically interfere with the contact the subdigital adhesive pads are capable of producing. However, this did not appear to be the case, suggesting that claws may not inhibit the engagement of subdigital pads or that morphological features and/or behavioral traits reduce the effect of this interaction.

Anolis sagrei

Although permanent marking solutions would be most beneficial for mark and recapture studies, partial claw clipping may be a useful alternative for shorter-term studies because it does not appear to reduce adhesive performance on smooth substrates. Future work should further consider the interactions between subdigital adhesive toe pads and claws, and determine the possible ramifications for adhesion and adhesive locomotion, particularly on rough substrates. Be sure to check out our full article for more details!

References

Bloch, N., Irschick, D.J. (2005): Toe-clipping dramatically reduces clinging performance in a pad-bearing lizard (Anolis carolinensis). J. Herpetol. 39: 288-293.

Dunham, A.E., Morin, P.J., Wilbur, H.M. (1988): Methods for the study of reptile populations. In: Biology of the Reptilia, pp. 331-386. Gans, C. Huey, R.B., Eds, Alan R. Liss, Inc., New York.

Irschick, D.J., Austin, C.C., Petren, K., Fisher, R.N., Losos, J.B., Ellers, O. (1996): A comparative analysis of clinging ability among pad-bearing lizards. Biol. J. Linn. Soc. 59: 21-35.

Niewiarowski, P.H., Lopez, S., Ge, L., Hagan, E., Dhinojwala, A. (2008): Sticky gecko feet: the role of temperature and humidity. PLoS ONE 3: e2192.

Zani, P. (2000): The comparative evolution of lizard claw and toe morphology and clinging performance. J. Evol. Biol. 13: 316-325.