Hyposalinity reduces coordination and adhesion of sea urchin tube feet.

Climate change will increase the frequency and intensity of low-salinity (hyposalinity) events in coastal marine habitats. Sea urchins are dominant herbivores in these habitats and are generally intolerant of salinity fluctuations. Their adhesive tube feet are essential for survival, effecting secure attachment and locomotion in high wave energy habitats, yet little is known about how hyposalinity impacts their function. We exposed green sea urchins (Strongylocentrotus droebachiensis) to salinities ranging from ambient (32‰) to severe (14‰) and assessed tube feet coordination (righting response, locomotion) and adhesion [disc tenacity (force per unit area)]. Righting response, locomotion and disc tenacity decreased in response to hyposalinity. Severe reductions in coordinated tube foot activities occurred at higher salinities than those that affected adhesion. The results of this study suggest moderate hyposalinities (24-28‰) have little effect on S. droebachiensis dislodgement risk and survival post-dislodgment, while severe hyposalinity (below 24‰) likely reduces movement and prevents recovery from dislodgment.

The same but different: setal arrays of anoles and geckos indicate alternative approaches to achieving similar adhesive effectiveness.

The functional morphology of squamate fibrillar adhesive systems has been extensively investigated and has indirectly and directly influenced the design of synthetic counterparts. Not surprisingly, the structure and geometry of exemplar fibrils (setae) have been the subject of the bulk of the attention in such research, although variation in setal morphology along the length of subdigital adhesive pads has been implicated to be important in the effective functioning of these systems. Adhesive setal field configuration has been described for several geckos, but that of the convergent Anolis lizards, comprised of morphologically simpler fibrils, remains largely unexplored. Here, we examine setal morphology along the proximodistal axis of the digits of Anolis equestris and compare our findings to those for a model gecko, Gekko gecko. Consistent with previous work, we found that the setae of A. equestris are generally thinner, shorter, and present at higher densities than those of G. gecko and terminate in a single spatulate tip. Contrastingly, the setae of G. gecko are hierarchically branched in structure and carry hundreds of spatulate tips. Although the splitting of contacts into multiple smaller tips is predicted to increase the adhesive performance of a fiber compared to an unbranched one, we posited that the adhesive performance of G. gecko and A. equestris would be relatively similar when the configuration of the setal fields of each was accounted for. We found that, as in geckos, setal morphology of A. equestris follows a predictable pattern along the proximodistal axis of the pad, although there are several critical differences in the configuration of the setal fields of these two groups. Most notably, the pattern of variation in setal length of A. equestris is effectively opposite to that exhibited by G. gecko. This difference in clinal variation mirrors the difference in the direction in which the setal fields of anoles and geckos are peeled from the substrate, consistent with the hypothesis that biomechanical factors are the chief determinants of these patterns of variation. Future empirical work, however, is needed to validate this. Our findings set the stage for future comparative studies investigating the functional morphology of these convergent adhesive apparatuses. Such investigations will lead to an enhanced understanding of the interactions between form, function, and environment of fibril-based biological adhesive systems.

Tokay geckos (Gekkonidae: Gekko gecko) preferentially use substrates that elicit maximal adhesive performance.

Gecko substrate use is likely influenced by adhesive performance, yet few studies have demonstrated this empirically. Herein, we examined the substrate use, adhesive performance and vertical clinging behaviour of Gekko gecko in captivity to investigate whether adhesive performance influences patterns of substrate use. We found that geckos were observed significantly more often on the substrate (glass) that elicited maximal adhesive performance relative to its availability within our experimental enclosures, indicating that geckos preferentially use substrates on which their adhesive performance is maximal. Our work here provides additional, yet crucial data establishing connections between adhesive performance and patterns of substrate use in captivity, suggesting the hypothesis that substrate preferences of free-ranging geckos should be correlated with adhesive performance. Clearly, further experimental and field research is necessary to test this hypothesis and identify other parameters that individually and/or collectively influence the habitat use of free-ranging geckos.

Home-field advantage: native gecko exhibits improved exertion capacity and locomotor ability in structurally complex environments relative to its invasive counterpart.

BACKGROUND: Invasive species are of substantial concern because they may threaten ecosystem stability and biodiversity worldwide. Not surprisingly, studies examining the drivers of biological invasion have increased in number over the past few decades in an effort to curtail invasive species success by way of informing management decisions. The common house gecko, Hemidactylus frenatus, has successfully invaded the Pacific islands where it appears to thrive in and dominate non-natural habitats offering high food availability (i.e., well-lit human dwellings) compared to native geckos. Previous work demonstrated that H. frenatus can outperform the native gecko, Lepidodactylus lugubris, in terms of maximal sprint speed on relatively simple planar surfaces (e.g., building walls). Lepidodactylus lugubris and other native geckos, however, may have superior locomotor performance in three-dimensional, structurally complex habitats. RESULTS: Here we compared the locomotor behaviour and exertion capacity of the native gecko, Gehyra oceanica, and the invasive gecko, Hemidactylus frenatus, on the island of Mo'orea, French Polynesia, on fabricated structures simulating structurally complex substrates. We found that the native gecko exhibits improved locomotor performance compared to the invasive gecko on structurally complex substrates. We also completed encounter surveys to document free-ranging habitat use and behaviour of these two species. We discovered that H. frenatus were more common in natural habitats than previously observed and used similar substrates as G. oceanica, although G. oceanica appeared to use substrates with greater perch heights (i.e., trees). CONCLUSIONS: Our findings revealed that locomotor performance in complex environments may contribute to the previously observed habitat segregation between native and invasive Pacific island geckos. Furthermore, our locomotor and habitat use data are consistent with the hypothesis that G. oceanica may be resistant to invasion of H. frenatus in natural environments. Our study calls for more detailed ecophysiological and ecomorphological studies of both native and invasive Pacific gecko species.

Response to underwater laser pointer in the Orange-finned Anemonefish Amphiprion chrysopterus and three-spot damselfish Dascyllus trimaculatus.

Response of orange-finned anemonefish Amphiprion chrysopterus and three-spot damselfish Dascyllus trimaculatus to red laser-pointer light was studied in Mo'orea, French Polynesia. Four magnificent anemones Heteractis magnifica and their resident fish were observed for typical behaviours (biting, chasing, hiding, posing, lunging and retreating) with and without exposure to laser-pointer light. Lunging behaviour increased significantly for both fish species upon exposure to laser-pointer light; none of the other behaviours changed significantly. We advance the hypothesis that orange-finned anemonefish and three-spot damselfish interpret laser pointer stimulation as a territorial threat.

Repeated Hyposalinity Pulses Immediately And Persistently Impair The Sea Urchin Adhesive System.

Climate change will increase the frequency and intensity of extreme climatic events (e.g., storms) that result in repeated pulses of hyposalinity in nearshore ecosystems. Sea urchins inhabit these ecosystems and are stenohaline (restricted to salinity levels ∼ 32 ‰), thus are particularly susceptible to hyposalinity events. As key benthic omnivores, sea urchins use hydrostatic adhesive tube feet for numerous functions, including attachment to and locomotion on the substratum as they graze for food. Hyposalinity severely impacts sea urchin locomotor and adhesive performance but several ecologically-relevant and climate change-related questions remain. First, does sea urchin locomotion and adhesion acclimate to repeated pulses of hyposalinity? Second, how do tube feet respond to tensile forces during single and repeated hyposalinity events? Third, do the negative effects of hyposalinity exposure persist following return to normal salinity levels? To answer these questions, we repeatedly exposed green sea urchins (Strongylocentrotus droebachiensis) to pulses of three different salinities (control: 32 ‰, moderate hyposalinity: 22 ‰, severe hyposalinity: 16 ‰) over the course of two months and measured locomotor performance, adhesive performance, and tube foot tensile behavior. We also measured these parameters 20 hours after sea urchins returned to normal salinity levels. We found no evidence that tube feet performance and properties acclimate to repeated pulses of hyposalinity, at least over the timescale examined in this study. In contrast, hyposalinity has severe consequences on locomotion, adhesion, and tube foot tensile behavior and these impacts are not limited to the hyposalinity exposure. Our results suggest both moderate and severe hyposalinity events have the potential to increase sea urchin dislodgment and reduce movement, which may impact sea urchin distribution and their role in marine communities.

Get to the point: Claw morphology impacts frictional interactions on rough substrates.

Claws are a common anatomical feature among limbed amniotes and contribute to a variety of functions including prey capture, locomotion, and attachment. Previous studies of both avian and non-avian reptiles have found correlations between habitat use and claw morphology, suggesting that variation in claw shape permits effective functioning in different microhabitats. How, or if, claw morphology influences attachment performance, particularly in isolation from the rest of the digit, has received little attention. To examine the effects of claw shape on frictional interactions, we isolated the claws of preserved specimens of Cuban knight anoles (Anolis equestris), quantified variation in claw morphology via geometric morphometrics, and measured friction on four different substrates that varied in surface roughness. We found that multiple aspects of claw shape influence frictional interactions, but only on substrates for which asperities are large enough to permit mechanical interlocking with the claw. On such substrates, the diameter of the claw's tip is the most important predictor of friction, with narrower claw tips inducing greater frictional interactions than wider ones. We also found that claw curvature, length, and depth influence friction, but that these relationships depend on the substrate's surface roughness. Our findings suggest that although claw shape plays a critical role in the effective clinging ability of lizards, its relative importance is dependent upon the substrate. Description of mechanical function, as well as ecological function, is critical for a holistic understanding of claw shape variation.

Polar bear paw pad surface roughness and its relevance to contact mechanics on snow.

Microscopic papillae on polar bear paw pads are considered adaptations for increased friction on ice/snow, yet this assertion is based on a single study of one species. The lack of comparative data from species that exploit different habitats renders the ecomorphological associations of papillae unclear. Here, we quantify the surface roughness of the paw pads of four species of bear over five orders of magnitude by calculating their surface roughness power spectral density. We find that interspecific variation in papillae base diameter can be explained by paw pad width, but that polar bear paw pads have 1.5 times taller papillae and 1.3 times more true surface area than paw pads of the American black bear and brown bear. Based on friction experiments with three-dimensional printed model surfaces and snow, we conclude that these factors increase the frictional shear stress of the polar bear paw pad on snow by a factor of 1.3-1.5 compared with the other species. Absolute frictional forces, however, are estimated to be similar among species once paw pad area is accounted for, suggesting that taller papillae may compensate for frictional losses resulting from the relatively smaller paw pads of polar bears compared with their close relatives.

An investigation of gecko attachment on wet and rough substrates leads to the application of surface roughness power spectral density analysis.

The roughness and wettability of surfaces exploited by free-ranging geckos can be highly variable and attachment to these substrates is context dependent (e.g., presence or absence of surface water). Although previous studies focus on the effect of these variables on attachment independently, geckos encounter a variety of conditions in their natural environment simultaneously. Here, we measured maximum shear load of geckos in air and when their toes were submerged underwater on substrates that varied in both surface roughness and wettability. Gecko attachment was greater in water than in air on smooth and rough hydrophobic substrates, and attachment to rough hydrophilic substrates did not differ when tested in air or water. Attachment varied considerably with surface roughness and characterization revealed that routine measurements of root mean square height can misrepresent the complexity of roughness, especially when measured with single instruments. We used surface roughness power spectra to characterize substrate surface roughness and examined the relationship between gecko attachment performance across the power spectra. This comparison suggests that roughness wavelengths less than 70 nm predominantly dictate gecko attachment. This study highlights the complexity of attachment in natural conditions and the need for comprehensive surface characterization when studying biological adhesive system performance.

Revisiting the classification of squamate adhesive setae: historical, morphological and functional perspectives.

Research on gecko-based adhesion has become a truly interdisciplinary endeavour, encompassing many disciplines within the natural and physical sciences. Gecko adhesion occurs by the induction of van der Waals intermolecular (and possibly other) forces between substrata and integumentary filaments (setae) terminating in at least one spatulate tip. Gecko setae have increasingly been idealized as structures with uniform dimensions and a particular branching pattern. Approaches to developing synthetic simulacra have largely adopted such an idealized form as a foundational template. Observations of entire setal fields of geckos and anoles have, however, revealed extensive, predictable variation in setal form. Some filaments of these fields do not fulfil the morphological criteria that characterize setae and, problematically, recent authors have applied the term 'seta' to structurally simpler and likely non-adhesively competent fibrils. Herein we briefly review the history of the definition of squamate setae and propose a standardized classificatory scheme for epidermal outgrowths based on a combination of whole animal performance and morphology. Our review is by no means comprehensive of the literature regarding the form, function, and development of the adhesive setae of squamates and we do not address significant advances that have been made in many areas (e.g. cell biology of setae) that are largely tangential to their classification and identification. We contend that those who aspire to simulate the form and function of squamate setae will benefit from a fuller appreciation of the diversity of these structures, thereby assisting in the identification of features most relevant to their objectives.

Digital hyperextension has no influence on the active self-drying of gecko adhesive subdigital pads.

The remarkable properties of the gecko adhesive system have been intensively studied. Although many gecko-inspired synthetic adhesives have been designed and fabricated, few manage to capture the multifunctionality of the natural system. Analogous to previously documented self-cleaning, recent work demonstrated that gecko toe pads dry when geckos take steps on dry substrates (i.e., self-drying). Whether digital hyperextension (DH), the distal to proximal peeling of gecko toe pads, is involved in the self-drying process, had not been determined. Here, the effect of DH on self-drying was isolated by preventing DH from occurring during normal walking locomotion of Gekko gecko after toe pads were wetted. Our initial analysis revealed low statistical power, so we increased our sample size to determine the robustness of our result. We found that neither DH nor the DH-substrate interaction had a significant effect on the maximum shear adhesive force after self-drying. These results suggest that DH is not necessary for self-drying to occur. Interestingly, however, we discovered that shear adhesion is higher on a surface tending hydrophobic compared to a hydrophilic surface, demonstrating that gecko adhesion is sensitive to substrate wettability during the subdigital pad drying process. Furthermore, we also observed frequent damage to the adhesive system during shear adhesion testing post-drying, indicating that water may compromise the structural integrity of the adhesive structures. Our results not only have behavioral and ecological implications for free-ranging geckos but also have the potential to influence the design and fabrication of gecko-inspired synthetic adhesives that can regain adhesion after fouling with water.

A Physical Model Approach to Gecko Adhesion Opportunity and Constraint: How Rough Could It Be?

It has been nearly 20 years since Autumn and colleagues established the central role of van der Waals intermolecular forces in how geckos stick. Much has been discovered about the structure and function of fibrillar adhesives in geckos and other taxa, and substantial success has been achieved in translating natural models into bioinspired synthetic adhesives. Nevertheless, synthetics still cannot match the multidimensional performance observed in the natural gecko system that is simultaneously robust to dirt and water, resilient over thousands of cycles, and purportedly competent on surfaces that are rough at drastically different length scales. Apparent insensitivity of adhesion to variability in roughness is particularly interesting from both a theoretical and applied perspective. Progress on understanding the extent to which and the basis of how the gecko adhesive system is robust to variation in roughness is impeded by the complexity of quantifying roughness of natural surfaces and a dearth of data on free-ranging gecko substrate use. Here we review the main challenges in characterizing rough surfaces as they relate to collecting relevant estimates of variation in gecko adhesive performance across different substrates in their natural habitats. In response to these challenges, we propose a practical protocol (borrowing from thermal biophysical ecological methods) that will enable researchers to design detailed studies of structure-function relationships of the gecko fibrillar system. Employing such an approach will help provide specific hypotheses about how adhesive pad structure translates into a capacity for robust gecko adhesion across large variation in substrate roughness. Preliminary data we present on this approach suggest its promise in advancing the study of how geckos deal with roughness variation. We argue and outline how such data can help advance development of design parameters to improve bioinspired adhesives based on the gecko fibrillar system.

Bioinspired remora adhesive disc offers insight into evolution.

Remoras are a family of fishes that can attach to other swimming organisms via an adhesive disc evolved from dorsal fin elements. However, the factors driving the evolution of remora disc morphology are poorly understood. It is not possible to link selective pressure for attachment to a specific host surface because all known hosts evolved before remoras themselves. Fortunately, the fundamental physics of suction and friction are mechanically conserved. Therefore, a morphologically relevant bioinspired model can be used to examine performance of hypothetical evolutionary intermediates. Using a bioinspired remora disc, we experimentally investigated the performance of increased lamellar number on shear adhesion. Herein, we translated fundamental biological principles into engineering design rules and show that a passive model system can autonomously achieve adhesive forces measured in live remoras in any environment. Our experimental results show that an increase in lamellar number resulted in an increase in shear adhesive performance, supporting the phylogenetic trend observed in extant remoras. The greatest pull-off forces measured for our model were on surface roughness on the order of shark skin and exceeded those measured for live remoras attached to shark skin by almost 60%. Overall, relative to fossil remoras and their closest ancestor, extant remoras exhibit a morphology indicative of selection for enhanced shear adhesive performance.

Going Out on a Limb: How Investigation of the Anoline Adhesive System Can Enhance Our Understanding of Fibrillar Adhesion.

The remarkable ability of geckos to adhere to a wide-variety of surfaces has served as an inspiration for hundreds of studies spanning the disciplines of biomechanics, functional morphology, ecology, evolution, materials science, chemistry, and physics. The multifunctional properties (e.g., self-cleaning, controlled releasability, reversibility) and adhesive performance of the gekkotan adhesive system have motivated researchers to design and fabricate gecko-inspired synthetic adhesives of various materials and properties. However, many challenges remain in our attempts to replicate the properties and performance of this complex, hierarchical fibrillar adhesive system, stemming from fundamental, but unanswered, questions about how fibrillar adhesion operates. Such questions involve the role of fibril morphology in adhesive performance and how the gekkotan adhesive apparatus is utilized in nature. Similar fibrillar adhesive systems have, however, evolved independently in two other lineages of lizards (anoles and skinks) and potentially provide alternate avenues for addressing these fundamental questions. Anoles are the most promising group because they have been the subject of intensive ecological and evolutionary study for several decades, are highly speciose, and indeed are advocated as squamate model organisms. Surprisingly, however, comparatively little is known about the morphology, performance, and properties of their convergently-evolved adhesive arrays. Although many researchers consider the performance of the adhesive system of Anolis lizards to be less accomplished than its gekkotan counterpart, we argue here that Anolis lizards are prime candidates for exploring the fundamentals of fibrillar adhesion. Studying the less complex morphology of the anoline adhesive system has the potential to enhance our understanding of fibril morphology and its relationship to the multifunctional performance of fibrillar adhesive systems. Furthermore, the abundance of existing data on the ecology and evolution of anoles provides an excellent framework for testing hypotheses about the influence of habitat microstructure on the performance, behavior, and evolution of lizards with subdigital adhesive pads.