bioRxiv Science⌕ Search

Biology subjects

Federle, W.

Publications and source records attributed to Federle, W..

9 recordsLinked to original sources

Regulation of pitcher fluid volume and properties in six ecologically distinct Bornean Nepenthes species

Carnivorous Nepenthes plants capture and digest prey in fluid-filled pitchers, whose fluid level is subject to fluctuations caused by rain and evaporation. It was found that N. rafflesiana pitchers can reduce these fluctuations by regulating their fluid volume and composition. Here, we investigate whether and to what extent this ability occurs in other Nepenthes species varying in morphology, trapping mechanisms, habitat, lifespan and nutrient sources. We hypothesised that species more exposed to fluid level fluctuations or relying more on fluid for prey capture would exhibit more intensive regulation. In six Bornean Nepenthes species, we quantified the effect of pitcher fluid level on prey-capture efficiency, the natural fluctuations in fluid volume, and the plants response to manipulations of the fluids volume, concentration and pH. The prey capture of Nepenthes species depended to varying degrees on the pitcher fluid level: in species with waxy inner walls, capture efficiency decreased at high fluid levels, as prey could escape easily. In contrast, species with wax-free walls and steep peristomes retained prey efficiently, regardless of fluid level. Although all Nepenthes species were able to secrete and absorb water and electrolytes, the regulation rate varied considerably. The rates of the various secretion and absorption processes (concentration/volume-dependent rates of electrolyte/water transport) were positively correlated with one another, suggesting that they all depend on the activity of the pitcher glandular epithelium. While differences and similarities in fluid regulation may be partly due to phylogeny, the observed species differences can also be explained by the pitchers trapping mechanisms and ecological factors. We found weaker regulation in Nepenthes species growing in sheltered understorey habitats, and in species utilising alternative nutrient sources, which may reduce their reliance on pitcher fluid. Our study highlights the diversity of ecological strategies in pitcher plants and demonstrates how these are influenced by environmental conditions. Lay SummaryNepenthes pitcher plants have fluid-filled pitchers to capture and digest prey. Can they control the volume and composition of their fluids? We found that all six species studied regulated their fluids, but to varying degrees. Species differences can be explained by the plants habitat, pitcher morphology and nutrient acquisition strategies.

Plant Biology↗

Caterpillar counter-adaptations to hooked trichomes: does the coevolutionary arms race continue?

Plants protect themselves against herbivory with diverse chemical and physical defences, and many herbivores have evolved counter-adaptations against these defences. So far, little is known about herbivore counter-adaptations to physical plant defences and their underlying mechanisms. Here, we investigated how specialised Heliconiini caterpillars are able to cope with the hooked trichomes of Passiflora adenopoda vines. P. adenopoda trichomes have sharp tips reinforced with silica, in contrast to simpler trichomes of other Passiflora that do not deter Heliconiini larvae. While Heliconius melpomene and H. erato caterpillars placed on P. adenopoda leaves were arrested and their soft cuticle was pierced by the sharp hooked trichomes, H. charithonia and Dryas iulia caterpillars of all sizes could move easily over the leaves without any injury. The superior performance of these two species on trichome-bearing leaves can be explained by their thicker and more puncture-resistant cuticle. Morphological and penetrometry measurements showed that the relevant cuticle regions in H. charithonia and D. iulia caterpillars are significantly thicker and more puncture-resistant than in H. melpomene and H. erato. When we tested the ability of the caterpillars to feed on P. adenopoda leaves with hooked trichomes, only H. charithonia survived, indicating the existence of further, previously unknown post-ingestive adaptations. Understanding insect counter-adaptations to physical plant defences is essential for studying the evolutionary arms-race between plants and insect herbivores.

evolutionary biology↗

Arms race of physical defences: Hooked trichomes of Macaranga ant-plants kill lycaenid caterpillars, but one specialist has a counter-defence

The co-evolution of insects and chemical plant defences has been described as an arms-race, but it is unclear if physical plant defences can produce similar outcomes. Here we report a previously unknown interaction from the mutualism between ants and Macaranga trees. Although Macaranga trees are well protected against herbivory by aggressive ants, caterpillars of the genus Arhopala (Lepidoptera: Lycaenidae) can feed on the leaves by appeasing the ants with nectar-like secretions. One ant-plant species, M. trachyphylla, bears hooked trichomes on its green surfaces. When placed on M. trachyphylla stems or petioles, Arhopala caterpillars associated with other Macaranga species (A. major, A. dajagaka and A. zylda) were quickly arrested by the sharp trichomes which pierced their cuticle, resulting in rapid loss of blood and death. In striking contrast, A. amphimuta caterpillars, which occur naturally on M. trachyphylla, could easily walk over the hooked trichomes without any injury. As hooked trichomes are a novel trait within Macaranga, this interaction provides an example of de novo evolution of a physical plant defence, which in turn has been overcome by a specialist herbivore. Our study suggests that physical plant defences can lead to evolutionary arms races similar to those for chemical defences.

zoology↗

Adult diet strongly affects cuticle thickness and its injury resistance in the insect Narnia femorata (Hemiptera: Coreidae)

Arthropods are the most diverse phylum on earth, accounting for up to 90% of animal species. The cuticular exoskeleton has played a vital role in their evolutionary success, but we know surprisingly little about the factors influencing its development, structure, and biomechanical properties. In this study, we examined whether and how nutrition affects the cuticle after an insect has completed its final molt into the adult stage. We found that a high-quality adult diet provided to the leaf-footed cactus bug, Narnia femorata (Hemiptera: Coreidae), over three weeks led to 4.1-times thicker cuticle with 3.7-times greater injury resistance relative to those that consumed a poor, but still ecologically relevant, diet. We further discovered that a high-quality adult diet allowed compensation for a sub-optimal juvenile diet. The cuticle of males was more injury resistant than that of females, as expected due to the aggressive male competition in this species. Altogether, our results show that, even after the final molt, nutrition can strongly influence the development and properties of the arthropod cuticle, a phenomenon that likely has drastic fitness-related consequences for locomotion, predator-prey interactions, and resource acquisition.

zoology↗

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

Nepenthes pitcher plants live 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 is much more effective at retaining insects than water, even after significant dilution. Although the physical properties of the fluid are important for its retentive function, it is unclear how the fluid interacts with insect cuticle and how its sticky nature affects struggling insects. In this study, we investigated the mechanisms behind the efficient prey retention in N. rafflesiana pitcher fluid. By measuring the attractive forces exerted on insect body parts moving in and out of test fluids, we show that it costs insects significantly more energy to separate from pitcher fluid than from water. Moreover, both the maximum force and the energy required for retraction increase 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 significantly lower than that of water (60.2 vs. 72.3 mN/m). By analysing the pitcher fluid dewetting 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 fluids viscoelastic nature and likely represents a key mechanism underlying prey retention in Nepenthes pitcher plants.

plant biology↗

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 traps 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.

plant biology↗

Extreme suction attachment performance from specialised insects living in mountain streams (Diptera: Blephariceridae)

Suction is widely used by animals for strong controllable underwater adhesion but is less well understood than adhesion of terrestrial climbing animals. Here we investigate the attachment of an aquatic insect larva (Blephariceridae), which clings to rocks in torrential streams using the only known muscle-actuated suction organs in insects. We measured their attachment forces on well-defined rough substrates and found their adhesion was much less reduced by micro-roughness than terrestrial climbing insects. In vivo visualisation of the suction organs in contact with microstructured substrates revealed that they can mould around large asperities to form a seal. Moreover, we showed that spine-like microtrichia on the organ are stiff cuticular structures that only make tip contact on smooth and microstructured substrates. Our results highlight the performance and versatility of blepharicerid suction organs and introduce a new study system to explore biological suction.

ecology↗

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

The ability to climb with adhesive pads conveys significant advantages, and is hence 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 natures climbers maintain a dynamic attachment performance across seven orders of magnitude in body weight.

zoology↗

Sophisticated suction organs from insects living in raging torrents: Morphology and ultrastructure of the attachment devices of net-winged midge larvae (Diptera: Blephariceridae)

2.Suction organs provide powerful yet dynamic attachments for many aquatic animals, including octopus, squid, remora, and clingfish. While the functional morphology of suction organs from various cephalopods and fishes has been investigated in detail, there are only few studies on such attachment devices in insects. Here we characterise the morphology, ultrastructure, and in vivo movements of the suction attachment organs of net-winged midge larvae (genus Liponeura) - aquatic insects that live on rocks in rapid alpine waterways where flow rates can reach 3 m s-1 - using scanning electron microscopy, laser confocal scanning microscopy, and X-ray computed micro-tomography (micro-CT). We identified structural adaptations important for the function of the suction attachment organs from L. cinerascens and L. cordata. First, a dense array of spine-like microtrichia covering each suction disc comes into contact with the substrate upon attachment. Similar hairy structures have been found on the contact zones of suction organs from octopus, clingfish, and remora fish. These structures are thought to contribute to the seal and to provide increased shear force resistance in high-drag environments. Second, specialised rim microtrichia at the suction disc periphery form a continuous ring in close contact with a surface and may serve as a seal on a variety of surfaces. Third, a V-shaped cut on the suction disc (the V-notch) is actively peeled open via two cuticular apodemes inserting into its flanks. The apodemes are attached to dedicated V-notch opening muscles, thereby providing a unique detachment mechanism. The complex cuticular design of the suction organs, along with specialised muscles that attach to them, allows blepharicerid larvae to generate powerful attachments which can withstand strong hydrodynamic forces and quickly detach for locomotion. Our findings could be applied to bio-inspired attachment devices that perform well on a wide range of surfaces.

zoology↗