Ultrastructure and function of the adhesion–capture apparatus of Stenus species (Coleoptera, Staphylinidae)

 The elongated labium of rove beetles of the genus Stenus forms an adhesion–capture apparatus that enables the animal to catch fast fleeing prey, for example, collemboles. Structural details of this labium have been reinvestigated by using transmission electron microscopy, and the functional model of the capture mechanism has been refined. The openings of glandular ductules have been found to be located at the outer margin of the sticky cushions formed by the paraglossae. These cushions can be expanded by hemolymph pressure and are compressed when the tip of the protrusible labium hits the prey. Endocuticular fibers stabilize the cushions internally and determine the shape of the cushions in both the expanded and the compressed state. Within the membranous connecting tube that connects the prementum with the head capsule, the existence of an extra inner membrane has been confirmed. It is formed by a portion of the epidermis that has become detached from the cuticle. The most important part of the functional model of the protrusion of the labium is that the membranous connecting tube turns itself inside out distally, but the extra inner membrane does so proximally. During protrusion of the labium by hemolymph pressure, the prementum is accelerated during the initial phase of the process, and the nerves, muscles, tracheae, and glandular ductules that are attached to it are passively drawn into the labium. The mechanoreceptive function of setae at the distal end of the prementum has been confirmed on the basis of their ultrastructural characteristics. Accepted: 4 September 1998     

The role of adhesion in prey capture and predator defence in arthropods

Adhesive devices are used by arthropods not only in terrestrial locomotion but also in prey capture and predator defence. We argue that the physical mechanisms involved in both these contexts must mainly be capillarity and the viscosity of an adhesive secretion, whereas other mechanisms, such as friction or intermolecular forces, are of minor importance. Adhesive prey-capture devices might function as passive devices or might be actively extended toward the prey, sometimes in a very rapid manner. Adhesive mechanisms used for predator defence might involve firm adhesion to the substratum or the discharge of a sticky secretion to immobilize the appendages of the opponent. We review the occurrence of adhesive devices as employed in both functional contexts across the Arthropoda and argue that these mechanisms are of particular importance for slow-moving and relatively clumsy life forms. We discuss three case studies in more detail. (1) Loricera larvae (Carabidae) use galeae with an extremely flexible cuticle in combination with an adhesive secretion. (2) Adult Stenus species (Staphylinidae) employ two highly flexible paraglossae that are covered by an adhesive emulsion of lipid droplets dispersed in an aqueous proteinaceous liquid. (3) Springtails often adhere to the mouthparts, the antennae, the legs, or other parts of the integument of Stenus larvae before being captured with the mandibles.     

Adhesive performance of the stick-capture apparatus of rove beetles of the genus Stenus (Coleoptera, Staphylinidae) toward various surfaces

Rove beetles of the genus Stenus possess a unique adhesive prey-capture apparatus that enables them to catch elusive prey such as springtails over a distance of several millimeters. The prey-capture device combines the hierarchically organized morphology of dry adhesive systems with the properties of wet ones, since an adhesive secretion is released into the contact zone. We hypothesize that this combination enables Stenus species successfully to capture prey possessing a wide range of surface structures and chemistries. We have investigated the influence of both surface energy and roughness of the substrate on the adhesive performance of the prey-capture apparatus in two Stenus species. Force transducers have been used to measure both the compressive and adhesive forces generated during the predatory strike of the beetles on (1) epoxy resin surfaces with defined roughness values (smooth versus rough with asperity diameters ranging from 0.3 to 12 μm) and (2) hydrophobic versus hydrophilic glass surfaces. Our experiments show that neither the surface roughness nor the surface energy significantly influences the attachment ability of the prey-capture apparatus. Thus, in contrast to the performance of locomotory adhesive systems in geckos, beetles, and flies, no critical surface roughness exists that might impede adhesion of the prey-capture apparatus of Stenus beetles. The prey-capture apparatus of Stenus beetles is therefore well adapted to adhere to the various unpredictable surfaces with diverse roughness and surface energy occurring in a wide range of potential prey.     

Functional morphology and adhesive performance of the stick-capture apparatus of the rove beetles Stenus spp. (Coleoptera, Staphylinidae)

The adhesive prey-capture apparatus of the representatives of the rove beetle genus Stenus (Coleoptera, Staphylinidae) is an outstanding example of biological adhesive systems. This unique prey-capture device is used for catching elusive prey by combining (i) hierarchically structured adhesive outgrowths, (ii) an adhesive secretion, and (iii) a network of cuticular fibres within the pad. The outgrowths arise from a pad-like cuticle and are completely immersed within the secretion. To date, the forces generated during the predatory strike of these beetles have only been estimated theoretically. In the present study, we used force transducers to measure both the compressive and adhesive forces during the predatory strike of two Stenus species. The experiments revealed that the compressive forces are low, ranging from 0.10 mN (Stenus bimaculatus) to 0.18 mN (Stenus juno), whereas the corresponding adhesive forces attain up to 1.0 mN in S. juno and 1.08 mN in S. bimaculatus. The tenacity or adhesive strength (adhesive force per apparent unit area) amounts to 51.9 kPa (S. bimaculatus) and 69.7 kPa (S. juno). S. juno beetles possess significantly smaller pad surface areas than S. bimaculatus but seem to compensate for this disadvantage by generating higher compressive forces. Consequently, S. juno beetles reach almost identical adhesive properties and an equal prey-capture success in attacks on larger prey. The possible functions of the various parts of the adhesive system during the adhesive prey-capture process are discussed in detail.     

New species of Desoria (Collembola: Isotomidae) from Korea

A new species, Desoria mulyeongariensis, shares some characters with D. choi (Lee), such as the number of setae on retinaculum and apical setae on manubrium. However, it could be easily distinguished from D. choi by the number of ommatidia. This species is also well characterized by having long and thickened smooth macrosetae on the body, and 6 basomedian setae on labium.     

Sticky predators: a comparative study of sticky glands in harpactorine assassin bugs (Insecta: Hemiptera: Reduviidae)

Zhang, G. and Weirauch, C. 2011. Sticky predators: a comparative study of sticky glands in harpactorine assassin bugs (Insecta: Hemiptera: Reduviidae). —Acta Zoologica (Stockholm) 00 : 1–10. For more than 50 years, specialized dermal glands that secrete sticky substances and specialized setae have been known from the legs of New World assassin bugs in the genus Zelus Fabricius (Reduviidae: Harpactorinae). The gland secretions and specialized ‘sundew setae’ are involved in enhancing predation success. We here refer to this predation strategy as ‘sticky trap predation’ and the specialized dermal glands as ‘sticky glands’. To determine how widespread sticky trap predation is among Reduviidae, we investigated taxonomic distribution of sticky glands and sundew setae using compound light microscopical and scanning electron microscopical techniques and sampling 67 species of Reduviidae that represent 50 genera of Harpactorini. We found sticky glands in 12 genera of Harpactorini and thus show that sticky trap predation is much more widespread than previously suspected. The sticky glands vary in shape, size and density, but are always located in a dorsolateral position on the fore tibia. Sundew setae are present in all taxa with sticky glands with the exception of Heza that instead possesses unique lamellate setae. The sticky trap predation taxa are restricted to the New World, suggesting a New World origin of this unique predation strategy.     

Wrap attack of the spider <Emphasis Type="Italic">Achaearanea tepidariorum</Emphasis> (Araneae: Theridiidae) by preying on mealybugs <Emphasis Type="Italic">Planococcus citri</Emphasis> (Homoptera: Pseudococcidae)

Predation by Achaearanea tepidariorum (Koch 1841) on mealybugs Planococcus citri (Risso 1813) is facilitated by the design of its web, which features a tangle of sticky gumfooted lines, and wrap attacks as well as the ability to handle the prey, whose body is covered with a waxy secretion, via silk. Crawling, i.e., wingless, mealybugs (in particular those in the nymphal stages and adult females and, to a lesser extent, winged males) are caught by means of the gumfooted lines, covered with globules of an adhesive secretion. The process of wrap attack and subsequent handling of the captured prey is a series of the following consecutive events: (1) confining and immobilising the mealybugs with sticky silk; (2) biting with chelicerae and paralyzing the prey with a toxin; (3) detaching the confined prey, attached to the tense threads, from the plant surface and catapulting it toward the central section of the web; (4) wrapping the catapulted prey in viscid silk emitted by the spinning apparatus; (5) transporting the wrapped prey to the central section of the web; (6) wrapping the prey in the central section of the web in nonsticky silk, whose tufts are present in this part of the web even before the attack; (7) filling the prey with digestive fluid; (8) sucking the prey empty; and (9) cleaning the chelicerae and mouth parts. The process of silk tuft wrapping was described for the first time. The described ability to hunt mealybugs implies the possibility of using A. tepidariorum spiders for biological control of these pests.     

Structure of the tarsi in some Stenus species (Coleoptera,Staphylinidae): external morphology,ultrastructure, and tarsal secretion

SEM studies show that the differentiation among Stenus species with respect to the formation of the tarsi (wide bilobed vs. slender tarsomeres) takes place with a considerable augmentation of tarsal ventral setae in wide bilobed tarsomeres. The structural diversity of ventral tarsal setae among and within species is discussed with respect to 1) their different roles as mechanosensilla and tenent setae, respectively, and 2) the different selection pressures in terms of adhesive requirements along the longitudinal tarsus axis. The tarsi are provided with four groups of tarsal mechanosensilla, comprising hair and bristle sensilla, campaniform sensilla, and scolopidia. The tarsus wall is supported by an epidermis, which forms three different types of glands pouring their secretion via different exit paths onto the outer cuticle. The organization and ultrastructure of each of these glands is described. Only one (unicellular) gland is directly associated with the ventral tenent setae and is thus considered to form the main part of the adhesive secretion. The beetles appear to release the tarsal secretion through mediation of the tenent setae, which contains a lipid and a proteinaceous fraction. I propose that the secretion is discharged to the outside via a system of very fine pore canals in the wall of the setal shaft. Gas chromatography and infrared spectroscopy revealed that the lipid fraction of the secretion is a mixture of unsaturated fatty acid glycerides and aliphatic hydrocarbons whose spectra are similar to those of extractions of the superficial lipid coating of the body surface.     

Comparative studies on the structure and adhesion of setae in <Emphasis Type="Italic">G. gecko</Emphasis> and <Emphasis Type="Italic">G. swinhonis</Emphasis>

Scanning electron microscopy (SEM) and histological techniques were used to observe and study the setae structures of two gecko species (G. gecko and G. swinhonis) and the relationships between these structures and the adhesive forces. The SEM results showed that the setae of these two species were densely distributed in an orderly fashion, and branched with curved tips. The setae of G. gecko had cluster structures, each cluster containing 4–6 setae whose terminal branches curved towards the center of the toes at ∼ 10°, the tips of the branches like spatulae and densely arrayed at an interval of less than 0.2–0.3 μm. On the contrary, the branch tips in the setae of G. swinhonis were curled, and the terminal parts of setae curved towards the center of the toes at various angles. Usually the setae of these gecko species branch twice at the top at intervals greater than that of G. gecko. The histological observation found that inside the setae of these two species there were plenty of unevenly distributed contents, such as epithelia, fat cells, pigmental cells and muscle tissue, but no gland cells existed. The results of functional experiments suggested that modifying the structure of gecko’s setae could reduce its adhesive ability dramatically, demonstrating the positive correlation between the structure of the gecko’s setae and its adhesive ability. The above results provide important information in designing bio-mimic setae and bio-gecko robots.     

Comparative studies on the structure and adhesion of setae in G. gecko and G. swinhonis

Scanning electron microscopy (SEM) and histological techniques were used to observe and study the setae structures of two gecko species (G. gecko and G. swinhonis) and the relationships between these structures and the adhesive forces. The SEM results showed that the setae of these two species were densely distributed in an orderly fashion, and branched with curved tips. The setae of G. gecko had cluster structures, each cluster containing 4-6 setae whose terminal branches curved towards the center of the toes at ~ 10o, the tips of the branches like spatulae and densely arrayed at an interval of less than 0.2―0.3 μm. On the contrary, the branch tips in the setae of G. swinhonis were curled, and the terminal parts of setae curved towards the center of the toes at various angles. Usually the setae of these gecko species branch twice at the top at intervals greater than that of G. gecko. The histological observation found that inside the setae of these two species there were plenty of unevenly distributed contents, such as epithelia, fat cells, pigmental cells and muscle tissue, but no gland cells existed. The results of functional experiments suggested that modifying the structure of gecko's setae could reduce its adhesive ability dramatically, demonstrating the positive correlation between the structure of the gecko's setae and its adhesive ability. The above results provide important information in designing bio-mimic setae and bio-gecko robots.     

Subdigital and subcaudal microornamentation in chamaeleonidae—A comparative study

Locomotion on horizontal and vertical substrates requires effective attachment systems. In three clades of arboreal and rupicolous Iguanidae, Gekkota and Scincidae adhesive systems consisting of microscopic hair‐like structures (setae) have been evolved independently. Also the substrate contacting sites on toes and tails of chameleons (Chamaeleonidae) are covered with setae. In the present comparative scanning electron microscopy study, we show that representatives from the chamaeleonid genera Calumma, Chamaeleo, Furcifer, and Trioceros feature highly developed setae that are species‐specific and similar on their feet and tail. These 10 μm long, unbranched setae rather resemble those in anoline and scincid lizards than the larger and branched setae of certain gecko species. In contrast to the thin triangular tips of other lizards, all examined species of the genera Furcifer and Calumma and one of the five examined species of the genus Trioceros have spatulate tips. All other examined species of genera Trioceros and Chamaeleo bear setae with narrowed, fibrous tips. Unlike the setae of other lizards, chamaeleonid setal tips do not show any orientation along the axis of the toes, but they are flexible to bend in any direction. With these differences, the chameleon's unique microstructures on the zygodactylous feet and prehensile tail rather increase friction for arboreal locomotion than being a shear‐induced adhesive system as setal pads of other lizards. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

The oral apparatus of tadpoles of Rana dalmatina, Bombina variegata, Bufo bufo, and Bufo viridis (Anura)

The morphology and development of the larval oral apparatus of Rana dalmatina, Bombina variegata, Bufo bufo, and Bufo viridis are described and compared using scanning electron microscopy. The species show different arrangements of the mouthparts. The small oral apparatus of R. dalmatina larvae has three labial tooth rows on the upper labium, while there are four tooth rows on the lower labium with a medial gap in row proximal to the mouth. The margins of the oral apparatus are defined by papillae that encircle the lower labium. B. variegata tadpoles have two upper labial tooth rows and three lower labial tooth rows that are uninterrupted, unlike the ones of R. dalmatina. The mouth is encircled by papillae that are larger than those of R. dalmatina. The oral discs of tadpoles of both B. bufo and B. viridis are similar. They are defined by two upper labial tooth rows (the second of which is interrupted by a medial gap) and by three lower tooth rows that differ in lengths in the two Bufo species. Both species develop papillae on the mouth angles and in two rows on the upper labium. Some morphological differences among the oral discs of R. dalmatina, B. variegata, B. bufo, and B. viridis tadpoles can be attributed to phylogenetic differences, but most can be related to their varying feeding habits and/or to their dietary specializations.     

Mechanical functions of setae from the mouth apparatus of seven species of decapod crustaceans

The mouthpart setae of seven species of decapods were examined with macro-video recordings and scanning electron microscopy. The general mechanical (nonsensory) functions of the different mouthparts are described and an account of their setation is given. This offers the possibility to determine the mechanical functions of the different types of setae. Pappose setae do not participate in food handling but in general make setal barriers. Plumose setae likewise do not contact food objects but assist in current generation. Papposerrate setae are rare but they were seen to assist in pushing food particles into the mouth. Serrulate setae are very common and mainly participate in gentle food handling and grooming. Serrate setae are used for more rough food manipulation and grooming. The roughest shredding, tearing, and manipulation of prey items are handled by the cuspidate setae. Simple setae seem to be divided into two populations with very different functions. On the maxillipeds of Panulirus argus they are used for shredding, tearing, and holding the food objects, but on the basis of maxilla 2 of three other species they appear to have very little mechanical influence and only when handling small prey items. The functional scheme seems to be consistent within the Decapoda.     

Prey Detection and Prey Capture in Copepod Nauplii

Copepod nauplii are either ambush feeders that feed on motile prey or they produce a feeding current that entrains prey cells. It is unclear how ambush and feeding-current feeding nauplii perceive and capture prey. Attack jumps in ambush feeding nauplii should not be feasible at low Reynolds numbers due to the thick viscous boundary layer surrounding the attacking nauplius. We use high-speed video to describe the detection and capture of phytoplankton prey by the nauplii of two ambush feeding species (Acartia tonsa and Oithona davisae) and by the nauplii of one feeding-current feeding species (Temora longicornis). We demonstrate that the ambush feeders both detect motile prey remotely. Prey detection elicits an attack jump, but the jump is not directly towards the prey, such as has been described for adult copepods. Rather, the nauplius jumps past the prey and sets up an intermittent feeding current that pulls in the prey from behind towards the mouth. The feeding-current feeding nauplius detects prey arriving in the feeding current but only when the prey is intercepted by the setae on the feeding appendages. This elicits an altered motion pattern of the feeding appendages that draws in the prey.     

Unusual sensory setae of the raptorial Branchinecta gigas (Branchiopoda: Anostraca)

In many vernal pools, visibility is very poor because of the turbidity from suspended clay particles. For predatory species like Branchinecta gigas, these conditions can be detrimental to successful prey capture. In vernal lakes in central California, B. gigashave developed specialized hunting modes to capture anostracan prey in pools of low visibility. The position of their body, the kinematics of their locomotion, and their reduced eye size suggested the possibility of novel sensory structures on their antennae and/or their cercopods designed to enhance their prey capture abilities. Using Scanning Electron Microscopy, we investigated the presence and design of sensory setae on the antennae and cercopods of B. gigas. On both males and females, there are dense patches of sensilla along the length of the antennae. They are oriented ventrally and slightly anteriorly. These antennal setae appear to be chemosensory in structure and position; they resemble antennal setae of other branchiopods. However, the setae of the cercopods are unusual in their morphology and location on the appendage. The cercopods, which are bent over the head in the hunting position, have a linear arrangement of specialized setae on their ventral side. They are jointed setae with an anterior crown of protective spines. The setal joint only permits limited abduction either toward the head in the hunting position or ventrally when swimming. These setae appear to be mechanosensory in function and may be adaptations to a raptorial lifestyle. They correlate well with the behavioral components of hunting in B. gigasand their complex prey capture mechanism.     

The roles of visual and proprioceptive information during motor program choice in frogs

Previous studies have shown that leopard frogs, Rana pipiens, use tongue prehension to capture small prey and jaw prehension to capture large prey. After hypoglossal nerve transection, the frogs fail to open their mouths when attempting to feed on small prey, but open their mouths and capture large prey. Here, we investigate how visual information about the prey and proprioceptive information from the tongue interact to influence the motor program choice. Using pieces of earthworm of various sizes, we found that Rana exhibits two different behavior patterns based on prey size. The frogs captured the 1.5-cm prey using tongue prehension, whereas 2.0-cm and larger prey were captured using jaw prehension. After hypoglossal transection, the frogs never opened their mouths when they tried to feed on 1.5-cm prey. When feeding on 3.0-cm and larger prey after transection, they always opened their mouths and captured the prey using jaw prehension. When offered 2.0-cm prey, they alternated randomly between opening and not opening the mouth. Therefore, deafferentation changed the pattern of motor program choice at the behavioral border. This implies that afferents from the tongue interact with visual input to influence motor program choice.     

Quantification of flow during suction feeding in bluegill sunfish

Nearly all aquatic-feeding vertebrates use some amount of suction to capture prey items. Suction prey capture occurs by accelerating a volume of water into the mouth and taking a prey item along with it. Yet, until recently, we lacked the necessary techniques and analytical tools to quantify the flow regime generated by feeding fish. We used a new approach; Digital Particle Image Velocimetery (DPIV) to measure several attributes of the flow generated by feeding bluegill sunfish. We found that the temporal pattern of flow was notably compressed during prey capture. Flow velocity increased rapidly to its peak within 20 ms of the onset of the strike, and this peak corresponded to the time that the prey entered the mouth during capture. The rapid acceleration and deceleration of water suggests that timing is critical for the predator in positioning itself relative to the prey so that it can be drawn into the mouth along with the water. We also found that the volume of water affected by suction was spatially limited. Only rarely did we measure significant flow beyond 1.75 cm of the mouth aperture (in 20 cm fish), further emphasizing the importance of mechanisms, like locomotion, that place the fish mouth in close proximity to the prey. We found that the highest flows towards the mouth along the fish midline were generated not immediately in front of the open mouth, but approximately 0.5 cm anterior to the mouth opening. Away from the midline the peak in flow was closer to the mouth. We propose that this pattern indicates the presence of a bow wave created by the locomotor efforts of the fish. In this scheme, the bow wave acts antagonistically to the flow of water generated by suction, the net effect being to push the region of peak flow away from the open mouth. The peak was located farther from the mouth opening in strikes accompanied by faster locomotion, suggesting faster fish created larger bow waves.     

Coordination of Behavioral Sequences Between Individuals During Prey Capture in a Social Spider, Anelosimus eximius

The analysis of collaborative predation sequences performed by groups of 10 individuals (females) in a nonterritorial permanent-social spider, A. eximius, shows that prey-captures are organized in successive steps. Spiders begin by throwing sticky silk, which hinders the prey in the web; they then throw dry silk, which completes the immobilization of the prey. The third step is characterized by bites that paralyze the prey that will be then carried. A concordance test reveals a coordination of the individual's acts that explains the collaborative prey-capture efficiency. No individual specialization in one type of act has been shown. On the contrary, by using living preys or artificially dead vibrated preys, we show that all individuals have equipotential behaviors. Furthermore, each spider is able to adjust its behavior to the state of the prey. Individuals already involved in prey transportation can again display bites or sticky silk throwing if the prey is artificially vibrated. This mechanism, which corresponds to stimergic processes responsible for self-organized phenomena, already described in social insects, permits a coordination of individual acts without the recourse of direct communication. These results permit us to understand better how individuals coordinate their acts and lead us to support the hypothesis that the transition between solitary species and social species in spiders could have been sudden.     

The influence of oral anatomy on prey selection during the ontogeny of two percoid fishes,Lagodon rhomboides and Centropomus undecimalis

Synopsis Ontogenetic increases in mouth size and changes in dentition of percoid fishes may affect the size and species of prey selected, thus influencing the fundamental trophic niche. To examine the influence of oral anatomy on prey selectivity by pinfish, Lagodon rhomboides, and snook, Centropomus undecimalis, two co-occurring percoid fishes with contrasting mouth morphologies, the mouth size, dentition, stomach contents, and available prey during ontogeny were quantified. Based on the presence of prey fragments in stomach contents and direct behavioral observation, prey were categorized by the feeding mode used during capture (suction/ramfeeding or biting). Centropomus has a larger size-specific gape than Lagodon during all ontogenetic stages. Although both feeding modes were used by Lagodon during ontogeny, the amount of prey captured using suction/ram-feeding declined and the amount of prey captured by biting increased with standard length. This change in feeding mode was associated with a change in incisor shape and width: Lagodon < 39 mm SL possessed narrow, pointed incisors and strongly selected amphipods, which are captured using suction/ram-feeding; Lagodon> 40 mm SL possessed wide, flat-topped incisors and significantly increased their selectivity for polychaetes, which are captured by biting. Centropomus used ram-feeding to capture prey at all ontogenetic stages. Size-selective feeding by Centropomus was apparent but could not be due to gape-limitation alone, because average prey body depth was only 45% of gape and was not proportional to absolute mouth size increase during ontogeny. Dietary diversity was greatest during the transition from suction/ram-feeding to biting in Lagodon. Lagodon had a higher dietary diversity at all ontogenetic stages than Centropomus, due in part to Lagodon's use of multiple feeding modes.