Biomechanical adaptations enable phoretic mite species to occupy distinct spatial niches on host burying beetles.

Niche theory predicts that ecologically similar species coexist by minimizing interspecific competition through niche partitioning. Therefore, understanding the mechanisms of niche partitioning is essential for predicting interactions and coexistence between competing organisms. Here, we study two phoretic mite species, Poecilochirus carabi and Macrocheles nataliae that coexist on the same host burying beetle Nicrophorus vespilloides and use it to 'hitchhike' between reproductive sites. Field observations revealed clear spatial partitioning between species in distinct host body parts. Poecilochirus carabi preferred the ventral side of the thorax, whereas M. nataliae were exclusively found ventrally at the hairy base of the abdomen. Experimental manipulations of mite density showed that each species preferred these body parts, largely regardless of the density of the other mite species on the host beetle. Force measurements indicated that this spatial distribution is mediated by biomechanical adaptations, because each mite species required more force to be removed from their preferred location on the beetle. While P. carabi attached with large adhesive pads to the smooth thorax cuticle, M. nataliae gripped abdominal setae with their chelicerae. Our results show that specialist biomechanical adaptations for attachment can mediate spatial niche partitioning among species sharing the same host.

Froghoppers jump from smooth plant surfaces by piercing them with sharp spines.

Attachment mechanisms used by climbing animals facilitate their interactions with complex 3D environments and have inspired novel types of synthetic adhesives. Here we investigate one of the most dynamic forms of attachment, used by jumping insects living on plants. Froghopper insects can perform explosive jumps with some of the highest accelerations known among animals. As many plant surfaces are smooth, we studied whether Philaenus spumarius froghoppers are able to take off from such substrates. When attempting to jump from smooth glass, the insects' hind legs slipped, resulting in weak, uncontrolled jumps with a rapid forward spin. By contrast, on smooth ivy leaves and smooth epoxy surfaces, Philaenus froghoppers performed strong jumps without any slipping. We discovered that the insects produced traction during the acceleration phase by piercing these substrates with sharp spines of their tibia and tarsus. High-speed microscopy recordings of hind legs during the acceleration phase of jumps revealed that the spine tips indented and plastically deformed the substrate. On ivy leaves, the spines of jumping froghoppers perforated the cuticle and epidermal cell walls, and wounds could be visualized after the jumps by methylene blue staining and scanning electron microscopy. Improving attachment performance by indenting or piercing plant surfaces with sharp spines may represent a widespread but previously unrecognized strategy utilized by plant-living insects. This attachment mechanism may also provide inspiration for the design of robotic grippers.

Role of legs and foot adhesion in salticid spiders jumping from smooth surfaces.

Many spiders and insects can perform rapid jumps from smooth plant surfaces. Here, we investigate how jumping spiders (Pseudeuophrys lanigera and Sitticus pubescens) avoid slipping when accelerating. Both species differed in the relative contribution of leg pairs to the jump. P. lanigera accelerated mainly with their long third legs, whereas their short fourth legs detached earlier. In contrast, S. pubescens accelerated mainly with their long fourth legs, and their short third legs detached earlier. Because of the different orientation (fourth-leg tip pointing backward, third-leg tip pointing forward), the fourth-leg tarsus pushed, whereas the third-leg tarsus pulled. High-speed video recordings showed that pushing and pulling was achieved by different attachment structures. In P. lanigera, third-leg feet made surface contact with setae on their distal or lateral claw tuft, whereas fourth-leg feet engaged the proximal claw tuft, and the distal tuft was raised off the ground. S. pubescens showed the same division of labour between proximal and distal claw tuft for pushing and pulling, but the claw tuft contact lasted longer and was more visible in the fourth than in the third legs. Experimental ablation of claw tufts caused accelerating spiders to slip, confirming that adhesion is essential for jumps from smooth substrates.

Shear-sensitive adhesion enables size-independent adhesive performance in stick insects.

The ability to climb with adhesive pads conveys significant advantages and is widespread in the animal kingdom. The physics of adhesion predict that attachment is more challenging for large animals, whereas detachment is harder for small animals, due to the difference in surface-to-volume ratios. Here, we use stick insects to show that this problem is solved at both ends of the scale by linking adhesion to the applied shear force. Adhesive forces of individual insect pads, measured with perpendicular pull-offs, increased approximately in proportion to a linear pad dimension across instars. In sharp contrast, whole-body force measurements suggested area scaling of adhesion. This discrepancy is explained by the presence of shear forces during whole-body measurements, as confirmed in experiments with pads sheared prior to detachment. When we applied shear forces proportional to either pad area or body weight, pad adhesion also scaled approximately with area or mass, respectively, providing a mechanism that can compensate for the size-related loss of adhesive performance predicted by isometry. We demonstrate that the adhesion-enhancing effect of shear forces is linked to pad sliding, which increased the maximum adhesive force per area sustainable by the pads. As shear forces in natural conditions are expected to scale with mass, sliding is more frequent and extensive in large animals, thus ensuring that large animals can attach safely, while small animals can still detach their pads effortlessly. Our results therefore help to explain how nature's climbers maintain a dynamic attachment performance across seven orders of magnitude in body weight.

Extreme positive allometry of animal adhesive pads and the size limits of adhesion-based climbing.

Organismal functions are size-dependent whenever body surfaces supply body volumes. Larger organisms can develop strongly folded internal surfaces for enhanced diffusion, but in many cases areas cannot be folded so that their enlargement is constrained by anatomy, presenting a problem for larger animals. Here, we study the allometry of adhesive pad area in 225 climbing animal species, covering more than seven orders of magnitude in weight. Across all taxa, adhesive pad area showed extreme positive allometry and scaled with weight, implying a 200-fold increase of relative pad area from mites to geckos. However, allometric scaling coefficients for pad area systematically decreased with taxonomic level and were close to isometry when evolutionary history was accounted for, indicating that the substantial anatomical changes required to achieve this increase in relative pad area are limited by phylogenetic constraints. Using a comparative phylogenetic approach, we found that the departure from isometry is almost exclusively caused by large differences in size-corrected pad area between arthropods and vertebrates. To mitigate the expected decrease of weight-specific adhesion within closely related taxa where pad area scaled close to isometry, data for several taxa suggest that the pads' adhesive strength increased for larger animals. The combination of adjustments in relative pad area for distantly related taxa and changes in adhesive strength for closely related groups helps explain how climbing with adhesive pads has evolved in animals varying over seven orders of magnitude in body weight. Our results illustrate the size limits of adhesion-based climbing, with profound implications for large-scale bio-inspired adhesives.

Scaling of claw sharpness: mechanical constraints reduce attachment performance in larger insects.

Claws are the most widespread attachment devices in animals, but comparatively little is known about the mechanics of claw attachment. A key morphological parameter in determining attachment ability is claw sharpness; however, there is a conflict between sharpness and fracture resistance. Sharper claws can interlock on more surfaces but are more likely to break. Body size interacts with this conflict such that larger animals should have much blunter claws and consequently poorer attachment ability than smaller animals. This expected size-induced reduction in attachment performance has not previously been investigated, and it is unclear how animals deal with this effect, and whether it indeed exists. We explored the scaling of claw sharpness with body size using four insect species (Nauphoeta cinerea, Gromphadorhina portentosa, Atta cephalotes and Carausius morosus) each covering a large size range. The scaling of claw sharpness varied significantly between species, suggesting that they face different pressures regarding claw function. Attachment forces were measured for A. cephalotes and G. portentosa (which had different scaling of claw sharpness) on several rough surfaces using a centrifuge setup. As expected, attachment performance was poorer in larger animals. Firstly, larger animals were more likely to slip, although this effect depended on the scaling of claw sharpness. Secondly, when they gripped, they attached with smaller forces relative to their weight. This size-induced reduction in attachment performance has significant implications for the attachment ability of larger animals on rough surfaces.

Coping with the climate: cuticular hydrocarbon acclimation of ants under constant and fluctuating conditions.

Terrestrial arthropods achieve waterproofing by a layer of cuticular hydrocarbons (CHCs). At the same time, CHCs also serve as communication signals. To maintain waterproofing under different climate conditions, insects adjust the chemical composition of their CHC layer, but this may affect the communication via CHCs. The detailed acclimatory changes of CHCs and how these influence their physical properties are still unknown. Here, we studied acclimation in two closely related ant species with distinct CHC profiles, Myrmica rubra and Myrmica ruginodis, in response to constant or fluctuating temperature and humidity regimes. We measured how acclimation affected CHC composition and viscosity, and the ants' drought survival. In both species, CHC composition showed strong, predictable responses to temperature regimes. Warm-acclimated individuals had higher proportions of linear alkanes, and less methyl-branched or unsaturated CHCs. These changes coincided with higher solid content and viscosity of CHCs in warm-acclimated ants. Temperature fluctuation caused effects similar to those observed under constant-cool conditions in Mrubra, but led to entirely different profiles in Mruginodis, suggesting that fluctuating and constant conditions pose very different challenges. Acclimation to dry conditions led to higher absolute amounts of CHCs, which increased the ants' drought survival, whereas temperature acclimation did not. Hence, the temperature-induced CHC changes cannot be explained by the need for waterproofing alone. Although these changes could be non-adaptive, we propose that they serve to maintain a constant CHC viscosity, which may be essential for communication and other functions.

Mechanotransduction: use the force(s).

Mechanotransduction - how cells sense physical forces and translate them into biochemical and biological responses - is a vibrant and rapidly-progressing field, and is important for a broad range of biological phenomena. This forum explores the role of mechanotransduction in a variety of cellular activities and highlights intriguing questions that deserve further attention.

How to catch more prey with less effective traps: explaining the evolution of temporarily inactive traps in carnivorous pitcher plants.

Carnivorous Nepenthes pitcher plants capture arthropods with specialized slippery surfaces. The key trapping surface, the pitcher rim (peristome), is highly slippery when wetted by rain, nectar or condensation, but not when dry. As natural selection should favour adaptations that maximize prey intake, the evolution of temporarily inactive traps seems paradoxical. Here, we show that intermittent trap deactivation promotes 'batch captures' of ants. Prey surveys revealed that N. rafflesiana pitchers sporadically capture large numbers of ants from the same species. Continuous experimental wetting of the peristome increased the number of non-recruiting prey, but decreased the number of captured ants and shifted their trapping mode from batch to individual capture events. Ant recruitment was also lower to continuously wetted pitchers. Our experimental data fit a simple model that predicts that intermittent, wetness-based trap activation should allow safe access for 'scout' ants under dry conditions, thereby promoting recruitment and ultimately higher prey numbers. The peristome trapping mechanism may therefore represent an adaptation for capturing ants. The relatively rare batch capture events may particularly benefit larger plants with many pitchers. This explains why young plants of many Nepenthes species additionally employ wetness-independent, waxy trapping surfaces.

Effect of shear forces and ageing on the compliance of adhesive pads in adult cockroaches.

The flexibility of insect adhesive pads is crucial for their ability to attach on rough surfaces. Here, we used transparent substrates with micropillars to test in adult cockroaches (Nauphoeta cinerea) whether and how the stiffness of smooth adhesive pads changes when shear forces are applied, and whether the insect's age has any influence. We found that during pulls towards the body, the pad's ability to conform to the surface microstructures was improved in comparison to a contact without shear, suggesting that shear forces make the pad more compliant. The mechanism underlying this shear-dependent increase in compliance is still unclear. The effect was not explained by viscoelastic creep, changes in normal pressure, or shear-induced pad rolling, which brings new areas of cuticle into surface contact. Adhesive pads were significantly stiffer in older cockroaches. Stiffness increased most rapidly in cockroaches aged between 2.5 and 4 months. This increase is probably based on wear and repair of the delicate adhesive cuticle. Recent wear (visualised by Methylene Blue staining) was not age dependent, whereas permanent damage (visible as brown scars) accumulated with age, reducing the pads' flexibility.

Rate-dependence of 'wet' biological adhesives and the function of the pad secretion in insects.

Many insects use soft adhesive footpads for climbing. The surface contact of these organs is mediated by small volumes of a liquid secretion, which forms thin films in the contact zone. Here, we investigate the role of viscous dissipation by this secretion and the 'bulk' pad cuticle by quantifying the rate-dependence of the adhesive force of individual pads. Adhesion increased with retraction speed, but this effect was independent of the amount of pad secretion present in the contact zone, suggesting that the secretion's viscosity did not play a significant role. Instead, the rate-dependence can be explained by relating the strain energy release rate to the speed of crack propagation, using an established empirical power law. The 'wet' pads' behaviour was akin to that of 'dry' elastomers, with an equilibrium energy release rate close to that of dry van-der-Waals contacts. We suggest that the secretion mainly serves as a 'release layer', minimising viscous dissipation and thereby reducing the time- and 'loading-history'-dependence of the adhesive pads. In contrast to many commercial adhesives which derive much of their strength from viscous dissipation, we show that the major modulator of adhesive strength in 'wet' biological adhesive pads is friction, exhibiting a much larger effect than retraction speed. A comparison between 'wet' and 'dry' biological adhesives, using both results from this study and the literature, revealed a striking lack of differences in attachment performance under varying experimental conditions. Together, these results suggest that 'wet' and 'dry' biological adhesives may be more similar than previously thought.

Rapid preflexes in smooth adhesive pads of insects prevent sudden detachment.

Many insects possess adhesive organs that can produce extreme attachment forces of more than 100 times body weight but they can rapidly release adhesion to allow locomotion. During walking, weaver ants (Oecophylla smaragdina) use only a fraction of their maximally available contact area, even upside-down on a smooth surface. To test whether the reduced contact area makes the ants more susceptible to sudden and unexpected detachment forces, for example, by rain or wind gusts, we investigated the reaction of untethered ants to rapid horizontal displacements of the substrate. High-speed video recordings revealed that the pad's contact area could more than double within the first millisecond after the perturbation. This contact area expansion is much faster than any neuromuscular reflex and therefore represents a passive 'preflex', resulting from the mechanical properties and geometrical arrangement of the (pre-)tarsus. This preflex reaction protects ants effectively against unexpected detachment, and allows them to use less contact area during locomotion. Contact area expanded most strongly when the substrate displacement generated a pull along the axis of the tarsus, showing that the ants' preflex is direction-dependent. The preflex may be based on the ability of Hymenopteran adhesive pads to unfold when pulled towards the body. We tested Indian stick insects (Carausius morosus), which have smooth pads that lack this motility. Similar to the ants, they showed a rapid and direction-dependent expansion of the contact area mainly in the lateral direction. We propose that the preflex reaction in stick insects is based on the reorientation of internal cuticle fibrils in a constant-volume system, whereas the ants' pad cuticle is probably not a hydrostat, and pad extension is achieved by the arcus, an endoscelerite of the arolium.

'Insect aquaplaning' on a superhydrophilic hairy surface: how Heliamphora nutans Benth. pitcher plants capture prey.

Trichomes are a common feature of plants and perform important and diverse functions. Here, we show that the inward-pointing hairs on the inner wall of insect-trapping Heliamphora nutans pitchers are highly wettable, causing water droplets to spread rapidly across the surface. Wetting strongly enhanced the slipperiness and increased the capture rate for ants from 29 to 88 per cent. Force measurements and tarsal ablation experiments revealed that wetting affected the insects' adhesive pads but not the claws, similar to the 'aquaplaning' mechanism of (unrelated) Asian Nepenthes pitcher plants. The inward-pointing trichomes provided much higher traction when insects were pulled outwards. The wetness-dependent capture mechanisms of H. nutans and Nepenthes pitchers present a striking case of functional convergence, whereas the use of wettable trichomes constitutes a previously unknown mechanism to make plant surfaces slippery.

Bumblebees negotiate a trade-off between nectar quality and floral biomechanics.

How and why pollinators choose which flowers to visit are fundamental, multifaceted questions in pollination biology, yet most studies of floral traits measure simple relative preferences. Here, we used vertically and horizontally oriented slippery-surfaced artificial flowers to test whether bumblebees could make a trade-off between floral handling difficulty and nectar sucrose concentration. We quantified foraging energetics, thereby resolving the rationale behind the bees' foraging decisions. The bees chose flowers with either a high handling cost or low sucrose concentration, depending on which was the energetically favorable option. Their behavior agreed with the critical currency being the rate of energy return (net energy collected per unit time), not energetic efficiency (net energy collected per unit energy spent). This suggests that bumblebees prioritize immediate carbohydrate flow to the nest rather than energy gain over the working lifespan of each bee. Trade-off paradigms like these are a powerful approach for quantifying pollinator trait preferences.

Ants swimming in pitcher plants: kinematics of aquatic and terrestrial locomotion in Camponotus schmitzi.

Camponotus schmitzi ants live in symbiosis with the Bornean pitcher plant Nepenthes bicalcarata. Unique among ants, the workers regularly dive and swim in the pitcher's digestive fluid to forage for food. High-speed motion analysis revealed that C. schmitzi ants swim at the surface with all legs submerged, with an alternating tripod pattern. Compared to running, swimming involves lower stepping frequencies and larger phase delays within the legs of each tripod. Swimming ants move front and middle legs faster and keep them more extended during the power stroke than during the return stroke. Thrust estimates calculated from three-dimensional leg kinematics using a blade-element approach confirmed that forward propulsion is mainly achieved by the front and middle legs. The hind legs move much less, suggesting that they mainly serve for steering. Experiments with tethered C. schmitzi ants showed that characteristic swimming movements can be triggered by submersion in water. This reaction was absent in another Camponotus species investigated. Our study demonstrates how insects can use the same locomotory system and similar gait patterns for moving on land and in water. We discuss insect adaptations for aquatic/amphibious lifestyles and the special adaptations of C. schmitzi to living on an insect-trapping pitcher plant.

The energetics of running stability: costs of transport in grass-cutting ants depend on fragment shape.

Grass-cutting ants (Atta vollenweideri) carry fragments that can be many times heavier and longer than the ants themselves and it is important for them to avoid falling over during load transport. To investigate whether the energetic costs of transport are affected by the need to maintain stability, the rate of CO(2) production was measured in both unladen workers and workers carrying standardized paper fragments of different size and shape. We tested: (1) the effect of mass by comparing workers carrying either light or heavy fragments of the same size, and (2) the effect of shape by comparing short and long fragments of the same mass. Consistent with previous studies, metabolic rate increased but running speed remained constant when ants carried heavier fragments. The net cost of transport (normalized to the total mass of ant and fragment) was the same for heavy and light fragments, and did not differ from the costs of carrying a unit body mass. Ants carrying long fragments showed similar metabolic rates but ran significantly slower than ants carrying short fragments. As a consequence, net cost of transport was significantly higher for long fragments than for short ones, and higher than the costs of carrying a unit body mass. The observed reduction in running speed is likely a result of the ants' need to maintain stability. When the absolute costs of transport were compared, smaller ants required more energy to carry heavier and longer fragments than larger workers, but the opposite was found for lighter and shorter fragments. The absolute costs of transport per unit fragment mass suggest that it is energetically advantageous for a colony to allocate smaller workers for the transport of small fragments and larger workers for large fragments. The present results underline the importance of biomechanical factors for the understanding of leaf-cutting ant foraging strategies.

Evidence for alternative trapping strategies in two forms of the pitcher plant, Nepenthes rafflesiana.

Nepenthes pitchers are specialized leaves that function as insect traps. Several pitcher components may contribute to trapping, including the pitcher fluid, slippery wax crystals and downward-pointing epidermal cells on the inner pitcher wall, and the wetness-dependent pitcher rim (peristome), but the relative importance of these traits is unclear. Mechanisms of prey capture and retention in the field were investigated by quantifying the effect of 'knock-out' manipulations of individual pitcher structures, and by testing the ability of pitcher fluids and water to retain insects. Two forms of Nepenthes rafflesiana Jack ('elongate' and 'typical') with contrasting combinations of pitcher traits were compared. Wax crystals on the inner pitcher wall were found to be the most important trapping structure in the elongate form, whereas the typical form relied primarily on the peristome. The pitcher fluids of both forms, differing markedly in the degree of viscoelasticity, retained significantly more ants than water. The present results show that pitcher plants utilize several mechanisms for prey capture and retention, varying in efficiency and relative importance between forms. It is proposed that these differences represent alternative prey capture strategies that may provide a mechanism to reduce competition and facilitate species co-existence in nutrient-limited habitats.

Beetle adhesive hairs differ in stiffness and stickiness: in vivo adhesion measurements on individual setae.

Leaf beetles are able to climb on smooth and rough surfaces using arrays of micron-sized adhesive hairs (setae) of varying morphology. We report the first in vivo adhesive force measurements of individual setae in the beetle Gastrophysa viridula, using a smooth polystyrene substrate attached to a glass capillary micro-cantilever. The beetles possess three distinct adhesive pads on each leg which differ in function and setal morphology. Visualisation of pull-offs allowed forces to be measured for each tarsal hair type. Male discoidal hairs adhered with the highest forces (919 ± 104 nN, mean ± SE), followed by spatulate (582 ± 59 nN) and pointed (127 ± 19 nN) hairs. Discoidal hairs were stiffer in the normal direction (0.693 ± 0.111 N m(-1)) than spatulate (0.364 ± 0.039 N m(-1)) or pointed (0.192 ± 0.044 N m(-1)) hairs. The greater adhesion on smooth surfaces and the higher stability of discoidal hairs help male beetles to achieve strong adhesion on the elytra of females during copulation. A comparison of pull-off forces measured for single setae and whole pads (arrays) revealed comparable levels of adhesive stress. This suggests that beetles are able to achieve equal load sharing across their adhesive pads so that detachment through peeling is prevented.

Disentangling the role of surface topography and intrinsic wettability in the prey capture mechanism of Nepenthes pitcher plants.

Nepenthes pitcher plants capture prey with leaves specialised as pitfall traps. Insects are trapped when they 'aquaplane' on the pitcher rim (peristome), a surface structured with macroscopic and microscopic radial ridges. What is the functional significance of this hierarchical surface topography? Here, we use insect pad friction measurements, photolithography, wetting experiments and physical modelling to demonstrate that the ridges enhance the trap's efficacy by satisfying two functional demands on prey capture: Macroscopic ridges restrict lateral but enhance radial spreading of water, thereby creating continuous slippery tracks which facilitate prey capture when little water is present. Microscopic ridges, in turn, ensure that the water film between insect pad and peristome remains stable, causing insects to aquaplane. In combination, the hierarchical ridge structure hence renders the peristome wettable, and water films continuous, so avoiding the need for a strongly hydrophilic surface chemistry, which would compromise resistance to desiccation and attract detrimental contamination.

How a sticky fluid facilitates prey retention in a carnivorous pitcher plant (Nepenthes rafflesiana).

Nepenthes pitcher plants grow in nutrient-poor soils and produce large pitfall traps to obtain additional nutrients from animal prey. Previous research has shown that the digestive secretion in N. rafflesiana is a sticky viscoelastic fluid that retains insects much more effectively than water, even after significant dilution. Although the retention of prey is known to depend on the fluid's physical properties, the details of how the fluid interacts with insect cuticle and how its sticky nature affects struggling insects are unclear. In this study, we investigated the mechanisms behind the efficient prey retention in N. rafflesiana pitcher fluid. By measuring the attractive forces on insect body parts moved in and out of test fluids, we show that it costs insects more energy to free themselves from pitcher fluid than from water. Moreover, both the maximum force and the energy required for retraction increased after the first contact with the pitcher fluid. We found that insects sink more easily into pitcher fluid than water and, accordingly, the surface tension of N. rafflesiana pitcher fluid was lower than that of water (60.2 vs. 72.3 mN/m). By analysing the pitcher fluid's wetting behaviour, we demonstrate that it strongly resists dewetting from all surfaces tested, leaving behind residual films and filaments that can facilitate re-wetting. This inhibition of dewetting may be a further consequence of the fluid's viscoelastic nature and likely represents a key mechanism underlying prey retention in Nepenthes pitcher plants. STATEMENT OF SIGNIFICANCE: Carnivorous Nepenthes pitcher plants secrete sticky viscoelastic fluids that prevent insects from escaping after falling into the pitcher. What physical mechanisms are responsible for the fluid's retentive function? First, insects sink and drown more readily in N. rafflesiana pitcher fluid due to its reduced surface tension. Second, once within the fluid, our force measurements show that it costs more energy to separate insects from pitcher fluid than from water. Third, the fluid strongly resists dewetting, making it harder for insects to extract themselves and covering their cuticle with residues that facilitate re-wetting. Such striking inhibition of dewetting may represent a previously unrecognised mechanism of prey retention by Nepenthes. Pitcher fluid fulfils a well-defined biological function and may serve as a model for studying the mechanics of complex fluids.