Facing the Green Threat: A Water Flea's Defenses against a Carnivorous Plant.

Every ecosystem shows multiple levels of species interactions, which are often difficult to isolate and to classify regarding their specific nature. For most of the observed interactions, it comes down to either competition or consumption. The modes of consumption are various and defined by the nature of the consumed organism, e.g., carnivory, herbivory, as well as the extent of the consumption, e.g., grazing, parasitism. While the majority of consumers are animals, carnivorous plants can also pose a threat to arthropods. Water fleas of the family Daphniidae are keystone species in many lentic ecosystems. As most abundant filter feeders, they link the primary production to higher trophic levels. As a response to the high predatory pressures, water fleas have evolved various inducible defenses against animal predators. Here we show the first example, to our knowledge, in Ceriodaphnia dubia of such inducible defenses of an animal against a coexisting plant predator, i.e., the carnivorous bladderwort (Utricularia x neglecta Lehm, Lentibulariaceae). When the bladderwort is present, C. dubia shows changes in morphology, life history and behavior. While the morphological and behavioral adaptations improve C. dubia's survival rate in the presence of this predator, the life-history parameters likely reflect trade-offs for the defense.

Structural gradients and anisotropic hydraulic conductivity in the enigmatic eel traps of carnivorous corkscrew plants (Genlisea spp.).

PREMISE: Among the sophisticated trap types in carnivorous plants, the underground eel traps of corkskrew plants (Genlisea spp., Lentibulariaceae) are probably the least understood in terms of their functional principle. Here, we provide a detailed analysis of structural and hydraulic features of G. hispidula traps, contributing to the ongoing debate on whether these traps can actively generate water streams to promote prey capture. METHODS: Anatomical and hydraulic traits of detached traps, including inner trap diameters, chamber line element, hair length, glandular pattern, and hydraulic conductivity, were investigated quantitatively using light and electron microscopy, x-ray microtomography, and hydraulic measurements. RESULTS: Hydraulic resistivity in the neck of the trap, from the trap mouth toward the vesicle (digestive chamber) was 10 times lower than in the opposite direction. The comparison of measured and theoretical flow rates suggests that the retrorse hairs inside trap necks also provide considerable resistance against movement of matter toward the vesicle. Hairs showed a gradient in length along the neck, with the shortest hairs near the vesicle. Co-occurrence of quadrifid and bifid glands was limited to a small part of the neck, with quadrifids near the vesicle and bifids toward the trap mouth. CONCLUSIONS: The combination of structural gradients with hydraulic anisotropy suggests the trap is a highly fine-tuned system based on likely trade-offs between efficient prey movement in the trap interior toward the vesicle, prey retention, and spatial digestion capacities and is not counter to the generation of water streams.

Functional-morphological analyses of the delicate snap-traps of the aquatic carnivorous waterwheel plant (Aldrovanda vesiculosa) with 2D and 3D imaging techniques.

BACKGROUND AND AIMS: The endangered aquatic carnivorous waterwheel plant (Aldrovanda vesiculosa) catches prey with 3-5-mm-long underwater snap-traps. Trapping lasts 10-20 ms, which is 10-fold faster than in its famous sister, the terrestrial Venus flytrap (Dionaea muscipula). After successful capture, the trap narrows further and forms a 'stomach' for the digestion of prey, the so-called 'sickle-shaped cavity'. To date, knowledge is very scarce regarding the deformation process during narrowing and consequent functional morphology of the trap. METHODS: We performed comparative analyses of virtual 3D histology using computed tomography (CT) and conventional 2D histology. For 3D histology we established a contrasting agent-based preparation protocol tailored for delicate underwater plant tissues. KEY RESULTS: Our analyses reveal new structural insights into the adaptive architecture of the complex A. vesiculosa snap-trap. In particular, we discuss in detail the arrangement of sensitive trigger hairs inside the trap and present actual 3D representations of traps with prey. In addition, we provide trap volume calculations at different narrowing stages. Furthermore, the motile zone close to the trap midrib, which is thought to promote not only the fast trap closure by hydraulics but also the subsequent trap narrowing and trap reopening, is described and discussed for the first time in its entirety. CONCLUSIONS: Our research contributes to the understanding of a complex, fast and reversible underwater plant movement and supplements preparation protocols for CT analyses of other non-lignified and sensitive plant structures.

Snapping mechanics of the Venus flytrap (Dionaea muscipula).

The mechanical principles for fast snapping in the iconic Venus flytrap are not yet fully understood. In this study, we obtained time-resolved strain distributions via three-dimensional digital image correlation (DIC) for the outer and inner trap-lobe surfaces throughout the closing motion. In combination with finite element models, the various possible contributions of the trap tissue layers were investigated with respect to the trap's movement behavior and the amount of strain required for snapping. Supported by in vivo experiments, we show that full trap turgescence is a mechanical-physiological prerequisite for successful (fast and geometrically correct) snapping, driven by differential tissue changes (swelling, shrinking, or no contribution). These are probably the result of the previous accumulation of internal hydrostatic pressure (prestress), which is released after trap triggering. Our research leads to an in-depth mechanical understanding of a complex plant movement incorporating various actuation principles.

4D pine scale: biomimetic 4D printed autonomous scale and flap structures capable of multi-phase movement.

We developed biomimetic hygro-responsive composite polymer scales inspired by the reversible shape-changes of Bhutan pine (Pinus wallichiana) cone seed scales. The synthetic kinematic response is made possible through novel four-dimensional (4D) printing techniques with anisotropic material use, namely copolymers with embedded cellulose fibrils and ABS polymer. Multi-phase motion like the subsequent transversal and longitudinal bending deformation during desiccation of a natural pinecone scale can be structurally programmed into such printed hygromorphs. Both the natural concept generator (Bhutan pinecone scale) and the biomimetic technical structure (4D printed scale) were comparatively investigated as to their displacement and strain over time via three-dimensional digital image correlation methods. Our bioinspired prototypes can be the basis for tailored autonomous and self-sufficient flap and scale structures performing complex consecutive motions for technical applications, e.g. in architecture and soft robotics. This article is part of the theme issue 'Bioinspired materials and surfaces for green science and technology (part 3)'.

Prey capture analyses in the carnivorous aquatic waterwheel plant (Aldrovanda vesiculosa L., Droseraceae).

We investigated the predator-prey interactions between an Australian ecotype of the carnivorous waterwheel plant (Aldrovanda vesiculosa, Droseraceae) and its potential natural prey, the water flea Daphnia longicephala (Daphniidae), which also occurs in Australia. A. vesiculosa develops snap-traps, which close within ~10-100 ms after mechanical triggering by zooplankton prey. Prey capture attempts (PCAs) were recorded via high-speed cinematography in the laboratory. From 14 recorded PCAs, nine were successful for the plant (the prey was caught), and five were unsuccessful (prey could escape), resulting in a capture rate of ~64%. The prey animals' locomotion behaviour (antenna beat frequency and movement type) in trap vicinity or inside the open traps is very variable. Traps were mainly triggered with the second antennae. During trap closure, the animals moved only very little actively. A flight response in reaction to an initiated trap closure was not observed. However, several animals could escape, either by having a "lucky" starting position already outside the triggered trap, by freeing themselves after trap closure, or by being pressed out by the closing trap lobes. According to our observations in the successful PCAs, we hypothesize that the convex curvature of the two trap lobes (as seen from the outside) and the infolded trap rims are structural means supporting the capture and retention of prey. Our results are discussed in a broader biological context and promising aspects for future studies are proposed.

How the carnivorous waterwheel plant (Aldrovanda vesiculosa) snaps.

The fast motion of the snap-traps of the terrestrial Venus flytrap (Dionaea muscipula) have been intensively studied, in contrast to the tenfold faster underwater snap-traps of its phylogenetic sister, the waterwheel plant (Aldrovanda vesiculosa). Based on biomechanical and functional-morphological analyses and on a reverse biomimetic approach via mechanical modelling and computer simulations, we identify a combination of hydraulic turgor change and the release of prestress stored in the trap as essential for actuation. Our study is the first to identify and analyse in detail the motion principle of Aldrovanda, which not only leads to a deepened understanding of fast plant movements in general, but also contributes to the question of how snap-traps may have evolved and also allows for the development of novel biomimetic compliant mechanisms.

Trap diversity and character evolution in carnivorous bladderworts (Utricularia, Lentibulariaceae).

Bladderworts (Utricularia, Lentibulariaceae, Lamiales) constitute the largest genus of carnivorous plants but only aquatic species (about one fifth of the genus) have so far been thoroughly studied as to their suction trap functioning. In this study, we comparatively investigated trap biomechanics in 19 Utricularia species to examine correlations between life-forms, trapping mechanisms, and functional-morphological traits. Our investigations show the existence of two functional trap principles (passive trap in U. multifida vs. active suction traps), and - in active suction traps - three main trapdoor movement types (with several subtypes). The trapdoor movement types and their corresponding functional-morphological features most presumably represent adaptations to the respective habitat. We furthermore give insights into fluid dynamics during suction in three representatives of the main types of trapdoor movement. The results on functional morphology and trapdoor movement were mapped onto a new phylogenetic reconstruction of the genus, derived from the rapidly evolving chloroplast regions trnK, rps16 and trnQ-rps16 and a sampling of 105 Utricularia species in total. We discuss potential scenarios of trap character evolution and species radiation, highlighting possible key innovations that enable such a unique carnivorous lifestyle in different habitats.

Biomechanical analysis of prey capture in the carnivorous Southern bladderwort (Utricularia australis).

We recorded capture events (CEs) of the daphniid Ceriodaphnia dubia by the carnivorous Southern bladderwort with suction traps (Utricularia australis). Independent to orientation and behavior during trap triggering, the animals were successfully captured within 9 ms on average and sucked in with velocities of up to 4 m/s and accelerations of up to 2800 g. Phases of very high acceleration during onsets of suction were immediately followed by phases of similarly high deceleration (max.: -1900 g) inside the bladders, leading to immobilization of the prey which then dies. We found that traps perform a 'forward strike' during suction and that almost completely air-filled traps are still able to perform suction. The trigger hairs on the trapdoors can undergo strong bending deformation, which we interpret to be a safety feature to prevent fracture. Our results highlight the elaborate nature of the Utricularia suction traps which are functionally resilient and leave prey animals virtually no chance to escape.

Fastest predators in the plant kingdom: functional morphology and biomechanics of suction traps found in the largest genus of carnivorous plants.

Understanding the physics of plant movements, which describe the interplay between plant architecture, movement speed and actuation principles, is essential for the comprehension of important processes like plant morphogenesis. Recent investigations especially on rapid plant movements at the interface of biology, physics and engineering sciences highlight how such fast motions can be achieved without the presence of muscles, nerves and technical hinge analogies. The suction traps (bladders) of carnivorous bladderworts (Utricularia spp., Lentibulariaceae, Lamiales) are considered as some of the most elaborate moving structures in the plant kingdom. A complex interplay of morphological and physiological adaptations allows the traps to pump water out of their body and to store elastic energy in the deformed bladder walls. Mechanical stimulation by prey entails opening of the otherwise watertight trapdoor, followed by trap wall relaxation, sucking in of water and prey, and consecutive trapdoor closure. Suction can also occur spontaneously in non-stimulated traps. We review the current state of knowledge about the suction trap mechanism with a focus on architectonically homogeneous traps of aquatic bladderwort species from section Utricularia (the so-called 'Utricularia vulgaris trap type'). The functional morphology and biomechanics of the traps are described in detail. We discuss open questions and propose promising aspects for future studies on these sophisticated ultra-fast trapping devices.