Evidence for air movement signals in the agonistic behaviour of a nocturnal arachnid (order Amblypygi)

Many arthropods possess filiform hair sensilla (termed trichobothria in arachnids), which are extremely sensitive detectors of medium particle displacement. Electrophysiological evidence in some taxa suggests that these sensilla can detect air particle displacements resulting from intraspecific communication signals. However, it has not yet been shown for any species that the air particle displacements detected by the filiform hairs are themselves perceived as a 'signal' (i.e. that individuals make behavioural decisions based upon the responses of these organs to the displays of conspecifics). We investigate the agonistic behaviour of the whip spider Phrynus marginemaculatus and the role of its trichobothria in receiving agonistic signals. Whip spiders have extremely elongated 'antenniform' first legs, which they vibrate close to their opponents during agonistic interactions, inducing air movements that excite their opponents' trichobothria. We find that ablation of the trichobothria causes significant increases in: (I) contest duration, and (II) the probability of contest escalation past aggressive displays to physical fighting. Therefore, in the absence of air movement-sensitive sensilla, contest assessment is impaired. This suggests that whip spiders exploit true air movement signals during agonistic interactions, and that these are received by the trichobothria. Furthermore, these results indicate that, in whip spiders, such signals help mitigate the cost of agonistic interaction.     

Tactile learning by a whip spider, <Emphasis Type="Italic">Phrynus marginemaculatus</Emphasis> C.L. Koch (Arachnida,Amblypygi)

The ability of animals to learn and remember underpins many behavioural actions and can be crucial for survival in certain contexts, for example in finding and recognising a habitual refuge. The sensory cues that an animal learns in such situations are to an extent determined by its own sensory specialisations. Whip spiders (Arachnida, Amblypygi) are nocturnal and possess uniquely specialised sensory systems that include elongated ‘antenniform’ forelegs specialised for use as chemo- and mechanosensory feelers. We tested the tactile learning abilities of the whip spider Phrynus marginemaculatus in a maze learning task with two tactile cues of different texture—one associated with an accessible refuge, and the other with an inaccessible refuge. Over ten training trials, whip spiders got faster and more accurate at finding the accessible refuge. During a subsequent test trial where both refuges were inaccessible, whip spiders searched for significantly longer at the tactile cue previously associated with the accessible refuge. Using high-speed cinematography, we describe three distinct antenniform leg movements used by whip spiders during tactile examination. We discuss the potential importance of tactile learning in whip spider behaviour and a possible role for their unique giant sensory neurons in accessing tactile information.     

广西近捕鸟蛛体表结构扫描电镜观察

对广西近捕鸟蛛Plesiophrictus guangxiensis进行扫描电镜观察,观察其螯肢、颚叶、跗节、生殖球、生殖沟、书肺、感觉器官、发音器及纺器等若干体表结构,为进一步研究蜘蛛的形态结构提供基础资料.     

Spider mechanoreceptors

Spiders have highly developed mechanosensory systems, some of which provide access to forms of stimulation alien to our own sensations. Studies of hair-shaped air movement detectors (trichobothria) and tactile sensors have uncovered an outstanding refinement of the processes of stimulus uptake and stimulus transformation, which reflect details of both stimulus physics and behavioral significance. They also emphasize the potential contained in the seemingly simple Bauplan of arthropod cuticular hairs. Embedded into the spider exoskeleton are several thousands of strain detectors (slit sensilla) measuring compressive exoskeletal strains induced by various forms of loads and forces. A compound slit sensillum (lyriform organ) on the leg has become an important model system for studies of mechanoreceptor primary processes at the cellular and membrane level.     

Mechanics of trichobothria in orb-weaving spiders (Agelenidae,Araneae)

Summary When a fly is humming at a distance of about one centimetre from an orb-weaving spider (Agelenidae) the trichobothria on the spider's extremities are deflected by air streams and air vibrations. Frequency analysis of the hum of the two prey animals,Drosophila andMusca, shows that the effective sound velocities of the harmonics with frequencies inferior to some five hundred Hz exceeds that of higher frequencies by a factor of at least 5. Biologically relevant resonances would, therefore, have to be looked for in the range of a few hundred Hz. Frequency response diagrams show that single hairs have no resonance between a few Hz and approximately 2 kHz. The maximal relative amplitude of hairs of different lengths shifts from the longer to the shorter hairs with increasing frequency. As this is only a minor effect, however, it appears that there is no frequency discrimination by the mechanical apparatus. Constant air streams with a velocity of 40 mm/s cause hair deflection of about 10 degrees (the hair's bend is neglibible). Similarly, near-field particle velocity of sound fields up to a few hundred Hz is well transmitted. The mechanical directional sensitivity does not depend on the azimuthal angle of deflection. Thus, information about direction and velocity of stationary and near-field air movements is transmitted without deformation by the mechanical apparatus. This is well matched with the fact that the hair is multiply innervated.Supported by grants of the Deutsche Forschungsmeinschaft in the field of the Schwerpunktprogramm Rezeptorphysiologie     

Acetylcholine receptors in spider peripheral mechanosensilla

Peripherally located parts of spider mechanosensory neurons are modulated by several neurotransmitters released from apposed efferent fibers. Activities of acetylcholine (ACh) synthesizing enzyme choline acetyltransferase (ChAT) and ACh degrading enzyme acetylcholine esterase (AChE) were previously found in some efferent fibers. ChAT activity was also present in all the mechanosensory neurons, while AChE activity was only found in some. We show that spider mechanosensory neurons and probably some efferent neurons are immunoreactive to a monoclonal antibody against muscarinic ACh receptors (mAChRs). However, application of muscarinic agonists did not change the physiological responses or membrane potentials of neurons in the lyriform organ VS-3. Similarly, the sensitivities of the neurons of trichobothria (filiform hairs) remained unchanged after application of these agonists. Therefore, activation of mAChRs may only modulate the function of spider mechanosensory neurons indirectly, for example, by affecting the release of other transmitter(s). However, a subgroup of VS-3 neurons was inhibited by ACh, which also depolarized the membrane similar to these neurons’ responses to GABA, suggesting that ACh activates anion channels in these neurons. Interestingly, all of the neurons responding to ACh were the rapidly adapting Type A neurons that were previously shown to express AChE activity.     

Central nervous projection patterns of trichobothria and other cuticular sensilla in the wandering spider Cupiennius salei (Arachnida,Araneae)

Summary Central projections of mechano-and chemoreceptors on the legs and pedipalps of the wandering spider Cupiennius salei were traced by anterograde cobalt fills. The primary afferent fibres from trichobothria, tactile hairs, lyriform organs and contact chemoreceptive hairs enter the leg ganglia and pedipalpal ganglia ventrally. On their way through these ganglia there is very little arborization. The main areas of arborization are in the sensory longitudinal tracts in the suboesophageal nervous mass. The central projections of all mechano-and chemoreceptors examined show somatotopic organization. Sensilla located proximally on the legs are represented in dorsally located sensory longitudinal tracts, whereas those located on distal leg segments enter more ventral tracts. The afferent fibres of receptors of identifical modality on a specific segment of all legs and of the pedipalps overlap in the same tracts. No indication for a tonotopic arrangement of the trichobothrial afferences was found, which might have been associated with the mechanical frequency tuning of the trichobothria known from other experiments. The convergence of the projections of different types of receptors in the sensory longitudinal tracts is considered to be an anatomical basis for their functional interaction in behaviour. Both the convergence of the projections of receptors from the same segment of different legs and the somatotopy are connectivity patterns possibly associated with the orientation of the spiders towards mechanical or chemical cues.     

Assassin bug uses aggressive mimicry to lure spider prey

Assassin bugs (Stenolemus bituberus) hunt web-building spiders by invading the web and plucking the silk to generate vibrations that lure the resident spider into striking range. To test whether vibrations generated by bugs aggressively mimic the vibrations generated by insect prey, we compared the responses of spiders to bugs with how they responded to prey, courting male spiders and leaves falling into the web. We also analysed the associated vibrations. Similar spider orientation and approach behaviours were observed in response to vibrations from bugs and prey, whereas different behaviours were observed in response to vibrations from male spiders and leaves. Peak frequency and duration of vibrations generated by bugs were similar to those generated by prey and courting males. Further, vibrations from bugs had a temporal structure and amplitude that were similar to vibrations generated by leg and body movements of prey and distinctly different to vibrations from courting males or leaves, or prey beating their wings. To be an effective predator, bugs do not need to mimic the full range of prey vibrations. Instead bugs are general mimics of a subset of prey vibrations that fall within the range of vibrations classified by spiders as 'prey'.     

Low-frequency airborne vibrations generated by crickets during singing and aggression

When crickets (Gryllus bimaculatus) produce their calling, courtship and rivalry songs, they generate, in addition to the audible stridulatory sound, low-frequency air oscillations associated with the inward and outward movements of the forewings. The frequencies of these oscillations are below ca 70 Hz, with a major component at 30 Hz, the syllable repetition rate. In the courtship song, single oscillations are also produced. Jerking movements of the whole body, which often occur in the presence of rivals, cause considerable air currents. In all these cases the air vibrations are sufficient to be perceived both by the individual generating them and by conspecifics (and perhaps by other insects) via air-flow receptors, in crickets the cercal filiform hairs.     

Modeling arthropod filiform hair motion using the penalty immersed boundary method

Crickets are able to sense their surrounding environment through about 2000 filiform hairs located on a pair of abdominal cerci. The mechanism by which the cricket is able to sense a wide range of input signals using these filiform hairs of different length and orientation is of great interest. Most of the previous filiform hair models have focused on a single, rigid hair in an idealized air field. Here, we present a model of the cercus and filiform hairs that are mechanically coupled to the surrounding air, and the model equations are based on the penalty immersed boundary method. The key difference between the penalty immersed boundary method and the traditional immersed boundary method is the addition of forces to account for density differences between the immersed solid (the filiform hairs) and the surrounding fluid (air). The model is validated by comparing the model predictions to experimental results, and then the model is used to examine the interactions between multiple hairs. With multiple hairs, there is little interaction when the hairs are separated by more than 1mm, and, as they move closer, they interact through viscous coupling, which reduces the deflection of the hairs due to the air movement. We also examine the computational scalability of the algorithm and show that the computational costs grow linearly with the number of hairs being modeled.     

虎纹捕鸟蛛体表扫描电镜观察

对虎纹捕岛蛛(Ornithoctonus husoena)的眼、生殖球、颚叶、听毛、触毛、琴形器、跗节器、发音器、幼蛛及成蛛的纺绩器和螯肢等结构进行了扫描电镜观察。     

Hunting Without a Web: How Lycosoid Spiders Subdue their Prey

More than half of all spider species hunt prey without a web. To successfully subdue their prey, they use adapted capture behaviour and efficient grasping mechanisms to interrupt the prey's locomotion, and to restrain it from escaping during the subsequent handling for final envenomation. In this study, we investigated how the prey capture behaviour of different lycosoid spider species is related to leg morphology and venom efficiency; using high speed videography, feeding experiments, stereomicroscopy, scanning electron microscopy and LD₅₀ venom bioassays. We found that different species employed different techniques when grasping their prey and these differences strongly correlate with the distribution and size of hairy adhesive leg pads (so‐called scopulae on pro‐ and retrolateral parts of legs) and erectable spines, which act in a complementary way. Our results indicate that the grasping and handling behaviour and leg morphology is crucial in restricting the prey's movements. However, none of these traits is directly related with venom efficiency.     

Wind-sensitive interneurones in the spider CNS (Cupiennius salei ): directional information processing of sensory inputs from trichobothria on the walking legs

Spiders can use air particle movements to localize moving prey. We studied the responses of 32 wind-sensitive interneurones in the hunting spider Cupiennius salei to prey stimuli. Stimulation with a tethered flying fly or with artificial air pulses activated plurisegmental interneurones that responded to changes in air movement velocity and were thus well suited to represent the highly fluctuating air stream typical of prey stimuli. In most interneurones (n = 18) the responses to the stimulation of different legs were not significantly different from each other. Different interneurones had different response characteristics and their latencies largely overlapped suggesting that there is parallel processing of the signals by populations of interneurones with different response characteristics. In two interneurones the number of spikes and the spiking pattern elicited by stimulation of each of the eight legs markedly differed depending on the leg stimulated. These neurones may play an important role in directional information processing. Stimulation of the adjacent legs from front to back or from back to front revealed two interneurones sensitive to the direction of successive stimulation of the legs. These neurones may be able to detect the motion of an air movement source in a preferred direction and thus act as nearfield motion detectors to localize a moving prey item. Accepted: 28 September 1996     

Kampf,Paarungsverhalten, Spermatophorenmorphologie und weibliche Genitalien bei neotropischen Geißelspinnen (Amblypygi,Arachnida)

Zusammenfassung Agonistisches Verhalten, Samenübertragung und Spermatophorenmorphologie vonTarantula (Phrynus) palmata (Herbst) undHeterophrynus alces Pocock sind ähnlich wie bei anderen Arten der Familie Tarantulidae (Phrynidae). Anders ist das agonistische Verhalten vonTrichodamon froesi Mello Leitao. Die Palpen tragen an ihren Spitzen kleine Scheren und sind beim Männchen stark verlängert. Beim Kampf versucht jeder, die Tibien des 3. Beinpaares des Gegners zu ergreifen und dann nach hinten und hochzustemmen. Die Balz besteht aus Serien von vibrierenden und trillernden Bewegungen der Fühlerbeine und gelegent lichen Eingreifen des Weibchens; das Weibchen antwortet darauf mit charakteristischen Fühlerbeinbewegungen. Die komplizierte Spermatophore wird dadurch entleert, daß das Weibchen auf zwei Hebel drückt und dadurch die Samenpakete hochschnellen läßt. Diese werden dann in die Receptacula eingeführt und mit den hakenartigen Strukturen an den Gonopoden ergriffen und abgerissen. Ein Vergleich der bisher untersuchten Arten zeigt, daß das Paarungsverhalten keine charakteristischen Unterschiede bei verschiedenen Familien oder Gattungen zeigt. Aber die Spermatophoren zeigen familientypische Baueigenschaften.

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Agonistic and mating behaviour, spermatophore morphology, and female genitalia in neotropical whip spiders (Amblypygi, Arachnida)

Summary Agonistic and mating beaviour and Spermatophore morphology ofTarantula (Phrynus) palmata (Herbst) andHeterophrynus alces Pocock are similar to those of other species of the Tarantulidae (Phrynidae). Males ofTrichodamon froesi Mello Leitao perform a different agonistic behaviour. Their pedipalps bear small apical chelae and are extremely elongate. During fighting, each male grasps the tibiae of the opponent's third legs and pushes them upward and backward. During mating, the male performs vibrating and tapping movements with its antenniform legs and occasionally grasps the female. The female responds by performing characteristic movements of her antenniform legs. The spermatophore is a complicated structure. It is emptied by the female's pressing down two levers which causes two sperm packages to become elevated. These are then grasped by the female's seminal receptacles and by two hook-like structures of her gonopods and finally pulled off the spermatophore. Comparison of the species so far studied shows that the mating behaviour, although it varies in different species, does not exhibit differences useful for taxonomic research. But the different spermatophores show family characteristic structural properties.

     

Anatomical and physiological observations on the organization of mechanoreceptors and local interneurons in the central nervous system of the wandering spider Cupiennius salei

Summary In the wandering spider Cupiennius salei, the functional neuroanatomy of leg mechanosensory receptor neurons and interneurons associated with a single leg neumere was investigated by combined intracellular recording and Lucifer yellow ionophoresis. Trichobothria axons that selectively respond to air currents and to low-frequency airborne vibrations have arborizations restricted to ventral regions of the appropriate leg neuromere. Receptor afferents that respond selectively to substrateborne vibrations are distributed ventrally in the corresponding leg neuromere and extend into certain interganglionic tract neuropiles. Golgi impregnation and intracellular dye filling show that local interneurons originate in ventral sensory neuropiles of leg neuromeres and ascend dorsally to terminate amongst dendrites of motor neurons. Local interneurons generally show higher thresholds for vibration stimuli than do receptors. Local interneurons typically receive inputs from one or several types of receptors. Some respond to stimulation of a single leg, others respond to stimulation of several legs on the same side of the body. The functional morphology of the receptor afferents is correlated with known physiological characteristics of slit sensilla and trichobothria. Structure and activity of the local interneurons are compared with analogous interneurons in other arthropods.     

Interaction between arthropod filiform hairs in a fluid environment

Many arthropods use filiform hairs as mechanoreceptors to detect air motion. In common house crickets (Acheta domestica) the hairs cover two antenna-like appendages called cerci at the rear of the abdomen. The biomechanical stimulus-response properties of individual filiform hairs have been investigated and modeled extensively in several earlier studies. However, only a few previous studies have considered viscosity-mediated coupling between pairs of hairs, and only in particular configurations. Here, we present a model capable of calculating hair-to-hair coupling in arbitrary configurations. We simulate the coupled motion of a small group of mechanosensory hairs on a cylindrical section of cercus. We have found that the coupling effects are non-negligible, and likely constrain the operational characteristics of the cercal sensory array.     

Proprioceptors and sensory nerves in the legs of a spider,Cupiennius salei (Arachnida,Araneida)

Summary Retrograde CoS-impregnation was used to trace and map the course of sensory nerves and the distribution and innervation of the various proprioceptor types in all leg segments of Cupiennius salei, a Ctenid spider.1. Sensory nerve branches. In both the tibia and femur, axons of all proprioceptor types ascend in just two lateral nerves which do not merge with the main leg nerve until they reach the next proximal joint region. In the short segments — coxa, trochanter, patella, and tarsus — axons of the internal joint receptors often run separately from those of the other sensilla. Axons of the large lyriform slit sense organ at the dorsal metatarsus and of the trichobothria join with only a few hair axons and form their own nerve branches (Figs. 1, 2, 3).2. Proprioceptors. Each of the seven leg joints is supplied with at least one set of the well-known internal joint receptors, slit sensilla (single slits and lyriform organs), and long cuticular hairs. In addition, we found previously unnoticed hair plates on both sides of the coxa, near the prosoma/coxa joint; they are deflected by the articular membrane during joint movements (Fig. 4).3. Sensory cells and innervation. CoS-impregnation shows that each slit of the slit sense organs — be it a single slit or several slits in a lyriform organ — is innervated by two bipolar sensory cells (Fig. 6). We also confirm previous reports of multiple innervation in the internal joint receptors and in the long joint hairs and cuticular spines.Most of the ascending nerve branches run just beneath the cuticle for at least a short distance (Fig. 5); hence they are convenient sites for electrophysiological recordings of sensory activity even in freely walking spiders.     

The formation of the antenna sensory apparatus in some bug (Heteroptera) species in the course of their postembryonic development

In the antenna sensory apparatus of bugs Coreus marginatus, Cimex lectularius, and Rhodnius prolixus sensilla of the four main types are identified: chaetica, trichodea, basiconica, and coeloconica. Chaetoid sensilla are differentiated into two subtypes: sensilla with cogged cuticles and those with smooth ones; trichoid sensilla were divided into long pointed and short ones with blunt tips. In larvae and adults of R. prolixus trichobothria (long filiform hairs) were found on the medial side of pedicellum. The postembryonic changes in the quantitative and qualitative composition of the antenna sensory apparatus were assessed using biometric analysis. The greatest increase of sensory organs was observed upon the nymphal ecdysis from the 5th instar to adult.     

The giant fiber system in the forelegs (whips) of the whip spider Heterophrynus elaphus Pocock (Arachnida: Amblypygi)

Summary The front legs of the whip spider H. elaphus are strongly modified to serve sensory functions. They contain several afferent nerve fibers which are so large that their action potentials can be recorded externally through the cuticle. In recordings from the tarsus 7 different types of afferent spikes were identified; 6 additional types of afferent spikes were discriminated in recordings from the tibia and femur. Most of the recorded potentials could be attributed to identifiable neurons serving different functions. These neurons include giant interneurons and giant fibers from diverse mechanoreceptors such as slit sense organs, trichobothria, and a joint receptor. In the present report these neurons are characterized using electrophysiological and histological methods. Their functions are discussed in the context of the animal's behavior.Abbreviations GN giant neuron - S segment     

Relative contributions of organ shape and receptor arrangement to the design of cricket’s cercal system

Understanding the relative contributions of the shape of a sensory organ and the arrangement of receptors to the overall performance of the organ has long been a challenge for sensory biologists. We tackled this issue using the wind-sensing system of crickets, the cerci, two conical abdominal appendages covered with arrays of filiform hairs. Scanning electron microscopy coupled with 3D reconstruction methods were used for mapping of all cercal filiform hairs. The hairs are arranged according to their diameter in a way that avoids collisions with neighbours during hair deflection: long hairs are regularly spaced, whereas short hairs are both randomly and densely distributed. Particle image velocimetry showed that the variation in diameter of the cercus along its length modifies the pattern of fluid velocities. Hairs are subject to higher air flow amplitudes at the base than at the apex of the cercus. The relative importance of interactions between receptors and the air flow around the organ may explain the performance of the cricket's cercal system: it is characterised by a high density of statistically non-interacting short hairs located at the base of the cercus where sensitivity to air currents is the highest.