Finite element modeling of arachnid slit sensilla—I. The mechanical significance of different slit arrays

Arachnid strain sensitive slit sensilla are elongated openings in the cuticle with aspect ratios (slit length l / slit width b) of up to 100. Planar Finite Element (FE) models are used to calculate the relative slit face displacements, D _c, at the centers of single slits and of arrangements of mechanically interacting slits under uni-axial compressive far-field loads. Our main objective is to quantitatively study the role of the following geometrical parameters in stimulus transformation: aspect ratio, slit shape, geometry of the slits‘ centerlines, load direction, lateral distance S, longitudinal shift λ, and difference in slit length Δl between neighboring slits. Slit face displacements are primarily sensitive to slit length and load direction but little affected by aspect ratios between 20 and 100. In stacks of five parallel slits at lateral distances typical of lyriform organs (S = 0.03 l) the longitudinal shift λ substantially influences slit compression. A change of λ from 0 to 0.85 l causes changes of up to 420% in D _c. Even minor morphological variations in the arrangements can substantially influence the stimulus transformation. The site of transduction in real slit sensilla does not always coincide with the position of maximum slit compression predicted by simplified models. An erratum to this article can be found at     

Finite element modeling of arachnid slit sensilla: II. Actual lyriform organs and the face deformations of the individual slits

Arachnid slit sensilla respond to minute strains in the exoskeleton. After having applied Finite Element (FE) analysis to simplified arrays of five straight slits (Hößl et al. J Comp Physiol A 193:445–459, 2007) we now present a computational study of the effects of more subtle natural variations in geometry, number and arrangement of slits on the slit face deformations. Our simulations show that even minor variations in these parameters can substantially influence a slit’s directional response. Using white-light interferometric measurements of the surface deformations of a lyriform organ, it is shown that planar FE models are capable of predicting the principal characteristics of the mechanical responses. The magnitudes of the measured and calculated slit face deformations are in good agreement. At threshold, they measure between 1.7 and 43 nm. In a lyriform organ and a closely positioned loose group of slits, the detectable range of loads increases to approximately 3.5 times the range of the lyriform organ alone. Stress concentration factors (up to ca. 29) found in the vicinity of the slits were evaluated from the models. They are mitigated due to local thickening of the exocuticle and the arrangement of the chitinous microfibers that prevents the formation of cracks under physiological loading conditions.     

Model studies on the mechanical significance of grouping in compound spider slit sensilla (Chelicerata,Araneida)

Summary The mechanical implications of various types of slit arrangements found among the strain-sensitive slit sensilla in the arachnid exoskeleton (Fig. 3) were studied by measuring the deformation of model slits, cut into plastic discs, under static load applied in the plane of the disc and from varying directions (Figs. 1, 2).1. Close parallel, lyriform arrangements. Compression of slits (adequate stimulus) reaches much higher values than dilatation. It is highest with the load direction at right angle to the slit axes. Also, in the majority of slits the range of load angles resulting in compression is considerably larger than that leading to dilatation. Length distribution and lateral shift of slits in the models have a pronounced effect on slit deformability (Figs. 4-5): (a) In the oblique bar arrangement with slits of equal length and regular lateral shift (Fig. 4A) deformation of all slits is very similar at all load directions. In all slits compression results from a range of load angles larger than 120°. (b) In arrangements with a regular increase in slit length and a triangular outline shape deformability differs greatly among the slits at all load angles (Fig. 4B). (c) The slit configuration with a heartshaped outline (Fig. 4C) is peculiar for the large spread of load angles at which the compression of the different slits is highest. — These properties recommend different arrangements for the solution of different strain measuring problems, with for instance, the particular need of a wide angular working range (arrangement a), of a large spectrum of absolute sensitivities (b), or of the analysis of load direction (c).2. Angle and distance between slits. Due to the mechanical directionality inherent in an elongated slit the divergence of slit axes within a group of slits is likely to indicate the importance of the analysis of strain direction (Fig. 6). The mechanical interaction between closely neighbouring slits decreases with their distance from each other. In a parallel arrangement of equally long slits it disappears if the distance is about 1.5 times the slit length (Fig. 7).3. Aiming towards a mechanical model which would explain the complex deformation found in a lyriform organ, we consider the outline of the organ as a hole traversed by beams of material. Slit deformation can be calculated from the elastic lines of the beams which separate the slits and information drawn from photoelastic experiments (Figs. 8-11).     

Slit sense organs on the scorpion leg (Androctonus australis L., Buthidae)

As in other arthropods the exoskeleton of arachnids is subjected to loads generated by external stimuli and behavioral activities. Far from being mere by-products of various activities such loads act as signals for mechanoreceptors capable of detecting minute displacements caused by them in the cuticle. In arachnids the slit sense organs serve in this capacity. Spiders have the most elaborate system of slit sense organs. Our previous studies clearly pointed to a functional significance of their specific location and orientation, as well as degree and type of aggregation (isolated, grouped, compound or lyriform) on respective body parts. The present study extends our work to the slit sense organs of scorpions. It gives a detailed account of the topography of the organs on the walking legs. In general slits are less orderly arranged on the legs of scorpions than on those of spiders. In the scorpion they never aggregate to form lyriform organs. Instead there are groups at comparable locations forming much more irregular, but still specific patterns. Isolated slits are more numerous on the scorpion leg, but are also less regularly distrubuted there. A common feature of the majority of slits on both the spider and the scorpion leg is their position on the lateral surfaces and their orientation roughly parallel to the long axis of the leg.     

Ein atlas der spaltsinnesorgane von Cupiennius salei keys. Chelicerata (Araneae)

To facilitate further physiological investigation, a survey was undertaken of all the slit sense organs to be found on the body of the spider Cupiennius salei. We counted and mapped more than 3 000 sensory slits in the cuticle about half of which are combined to small groups of up to 29 slits forming compound or lyriform organs.     

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.     

Central nervous projections of mechanoreceptors in the spider Cupiennius salei Keys.

Summary The basic organization of sensory projections in the suboesophageal central nervous system of a spider (Cupiennius salei Keys.) was analyzed with anterograde cobalt fills and a modified Golgi rapid method. The projections of three lyriform slit sense organs and of tactile hairs located proximally on the legs are described and related to central nerve tracts. There are five main longitudinal sensory tracts in the central region of the suboesophageal nervous mass arranged one above the other. Whereas the three dorsal ones contain fibers from the lyriform organs, the two ventral ones contain axons from the hair receptors. Axons from all three lyriform organs have typical shapes and widely arborizing ipsilateral intersegmental branches and a few contralateral ones. The terminal branches of the afferent projections from identical lyriform organs on each leg form characteristic longitudinal pathways, typical of each organ: U-shaped, O-shaped, or two parallel bundles. The terminations of the hair sensilla are ipsilateral and intersegmental. Two large bilaterally arranged longitudinal sensory association tracts receive inputs from all legs including the dense arborizations from tactile hairs, lyriform organs, and other sense organs. These tracts may serve as important integrating neuropils of the suboesophageal central nervous system.     

The sensory equipment of a spider – A morphological survey of different types of sensillum in both sexes of Argiope bruennichi (Araneae,Araneidae)

Spiders show a wide range of sensory capabilities as evidenced by behavioural observations. Accordingly, spiders possess diverse sensory structures like mechano-, hygro-, thermo- or chemoreceptive sensilla. As to chemoreceptive structures, only trichoid tip-pore sensilla were found so far that were tested for gustation. That spiders are also able to receive airborne signals is corroborated by numerous behavioural experiments but the responsible structures have not been determined yet. Here, we provide sensilla distribution maps of pedipalps and walking legs of both sexes of the wasp spider Argiope bruennichi whose biology and mating system is well explored. By means of scanning electron microscopy, we scrutinized whether there is in fact only one type of trichoid pore sensillum and if so, if there are deviations in the outer structure of the tip-pore sensilla depending on their position on the body. We also describe the external structure and distribution of slit sense organs, trichobothria and tarsal organs. Our study shows that all four sensillum types occur on pedipalps and walking legs of both sexes. As to chemosensory organs, only tip-pore sensilla were found, suggesting that this sensillum type is used for both gustation and olfaction. The highest numbers of tip-pore sensilla were observed on metatarsi and tarsi of the first two walking legs. Mechanosensitive slit sense organs occur as single slit sensilla in rows along all podomers or as lyriform organs next to the joints. The mechanosensitive trichobothria occur on the basal part of tibiae and metatarsi. Tarsal organs occur on the dorsal side of all tarsi and the male cymbium. The distribution maps of the sensilla are the starting point for further exploration of internal, morphological differences of the sensilla from different regions on the body. Cryptic anatomical differences might be linked to functional differences that can be explored in combination with electrophysiological analyses. Consequently, the maps will help to elucidate the sensory world of spiders.     

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.     

Atomistic Monte Carlo Simulations of Liquids of Chain Molecules Confined by Solid Surfaces: Methods and Recent Results

Abstract

The molecular arrangements of liquid tridecane near solid surfaces and in narrow slits have been studied by atomistic Monte Carlo computer simulations. A single surface perturbs the liquid over a distance of 1.5 nm, inducing the formation of progressively less dense and ordered layers of thickness 0.4 nm. Chains with atoms in the first layer tend to run parallel to the surface. The tendency to form layer structures is maintained or destroyed in narrow slits, depending on the slit thickness. For instance, it is slighly increased in slits of thickness 1.2 nm, while it is practically destroyed when the slit thickness is reduced to 1.0 nm. When added in small amounts, shorter-chain components are preferentially adsorbed at the solid surface, making the first layer of liquid in contact with these surfaces much less ordered.     

Intracellular recording from a spider vibration receptor

The present study introduces a new preparation of a spider vibration receptor that allows intracellular recording of responses to natural mechanical or electrical stimulation of the associated mechanoreceptor cells. The spider vibration receptor is a lyriform slit sense organ made up of 21 cuticular slits located on the distal end of the metatarsus of each walking leg. The organ is stimulated when the tarsus receives substrate vibrations, which it transmits to the organ’s cuticular structures, reducing the displacement to about one tenth due to geometrical reasons. Current clamp recording was used to record action potentials generated by electrical or mechanical stimuli. Square pulse stimulation identified two groups of sensory cells, the first being single-spike cells which generated only one or two action potentials and the second being multi-spike cells which produced bursts of action potentials. When the more natural mechanical sinusoidal stimulation was applied, differences in adaptation rate between the two cell types remained. In agreement with prior extracellular recordings, both cell types showed a decrease in the threshold tarsus deflection with increasing stimulus frequency. Off-responses to mechanical stimuli have also been seen in the metatarsal organ for the first time.     

Proprioceptor distribution and control of a muscle reflex in the tibia of spider legs

In spiders, retrograde cobalt staining was used to clarify the distribution and detailed innervation of the three types of proprioceptors in the tibio-metatarsal leg joint: internal joint receptors, lyriform slit sense organs, and cuticular spines and hairs. The axons of all these receptors run in just two lateral, ascending nerves, which had previously been associated only with the internal receptors. Each nerve contains several hundred axons ranging in diameter from 0.1 micron to ca. 10 micron. Each slit of the four tibial lyriform organs is innervated by two bipolar sensory neurons. The lateral nerves are entirely sensory and run just beneath the cuticle, a convenient site for electrophysiological recording. We demonstrate simultaneous nerve and muscle recordings from intact spiders; these, in combination with selective sensory ablations, show that a resistance reflex in the flexor metatarsi muscles is elicited by internal joint-receptor units.     

Acetylcholine and histamine are transmitter candidates in identifiable mechanosensitive neurons of the spider Cupiennius salei: an immunocytochemical study

Histochemical and indirect immunocytochemical techniques were used to search for neuroactive substances and transmitter candidates in identified sensory neurons of two types of cuticular mechanoreceptors in the spider Cupiennius salei Keys.: (1) in lyriform slit-sense organ VS-3 (comprising 7-8 cuticular slits each innervated by 2 bipolar neurons), and (2) in tactile hairs (each supplied by 3 bipolar sensory cells). All neurons are mechanosensitive. A polyclonal antibody against choline acetyltransferase (ChAT) strongly labeled all cell bodies and afferent fibers of both mechanoreceptor types. Western blot analysis using the same antibody against samples of spider sensory hypodermis and against samples from the central nervous system demonstrated a clear band at 65 kDa, corresponding to the molecular mass of ChAT in insects. Moreover, staining for acetylcholine esterase (AChE) revealed AChE activity in one neuron of each mechanoreceptor type. Incubation with a polyclonal antibody against histamine clearly labeled one neuron in each set of sensilla, whereas activity in the remaining one or two cells was near background. All mechanoreceptor preparations treated with a polyclonal antiserum against serotonin tested negative, whereas sections through the central nervous system of the same spiders were clearly labeled for serotonin. The presence of ChAT-like immunoreactivity and AChE implicates acetylcholine as a transmitter candidate in the two mechanoreceptive organs. We assume that histamine serves as a mechanosensory co-transmitter in the central nervous system and may also act at peripheral synapses that exist in these sensilla. Received: 15 July 1996 / Accepted: 26 August 1996     

Changes in distribution and abundance of antennal sensilla during growth of Locusta migratoria L. (Orthoptera : Acrididae)

The antenna of Locusta migratoria (Orthoptera : Acrididae) increases in length by the production of new annuli proximally and by elongation of existing annuli. The most distal annuli are fully differentiated at the time of hatching and no new olfactory sensilla are added to them at subsequent molts. More proximally, the differentiation of trichoid contact chemoreceptors precedes the development of olfactory sensilla. Sensillum differentiation proceeds from distal to proximal along the antenna and more distal annuli attain full development at each molt. The biggest increase in numbers of olfactory sensilla occurs at the final molt. On any one annulus, most olfactory sensilla are restricted to sensory fields on the anterior and posterior faces. Their spacing within these fields is consistent with the existence of separate but interacting chaetogens regulating the differentiation of basiconic and coeloconic sensilla.     

POROUS SUBSTRUCTURE OF THE GLOMERULAR SLIT DIAPHRAGM IN THE RAT AND MOUSE

The highly ordered, isoporous substructure of the glomerular slit diaphragm was revealed in rat and mouse kidneys fixed by perfusion with tannic acid and glutaraldehyde. The slit diaphragm was similar in both animal species and appeared as a continuous junctional band, 300–450 Å wide, consistently present within all slits formed by the epithelial foot processes. The diaphragm exhibited a zipper-like substructure with alternating, periodic cross bridges extending from the podocyte plasma membranes to a central filament which ran parallel to and equidistant from the cell membranes. The dimensions and spacing of the cross bridges defined a uniform population of rectangular pores approximately 40 by 140 Å in cross section and 70 Å in length. The total area of the pores was calculated to be about 2–3% of the total surface area of the glomerular capillaries. Physiological data indicate that the glomerular filter functions as if it were an isoporous membrane which excludes proteins larger than serum albumin. The similarity between the dimensions of the pores in the slit diaphragm and estimates for the size and shape of serum albumin supports the conclusion from tracer experiments that the slit diaphragm may serve as the principal filtration barrier to plasma proteins in the kidney.     

Detection of vibrations in sand by tarsal sense organs of the nocturnal scorpion,Paruroctonus mesaensis

Summary The scorpionParuroctonus mesaensis locates prey by orienting to substrate vibrations produced by movements of the prey in sand. At the end of each walking leg of this scorpion there are two sense organs, the basitarsal compound slit sensillum and tarsal sensory hairs (Figs. 1, 3) that are excited by substrate vibrations conducted through sand. The slit sensilla appear to be most sensitive to surface (Rayleigh) waves while the tarsal sensory hairs respond best to compressional waves (Fig. 7). Both mechanoreceptors were activated by nearby disturbances of the substrate (Fig. 6) but only the slit sensilla responded to insects moving more than 15 cm away. Both receptors are highly sensitive to small amplitude (less than 10 Å) mechanical stimuli applied to the tarsus (Fig. 5).Behavioral studies of scorpions with ablated sense organs (Fig. 2) indicate that the basitarsal compound slit sensilla are necessary for determining vibration source direction.Abbreviation BCSS basitarsal compound slit sensillum (a) Supported by PHS Environmental Science and Regents Intern Fellowships (PB), and by intramural research funds from the University of California (RDF)     

Structural correlates of mechanosensory transduction and adaptation in identified neurons of spider slit sensilla

We used isolated but functionally intact preparations of the lyriform slit-sense organ VS-3 from the leg of the spider, Cupiennius salei Keys, to examine the role of prominent fine-structural elements for mechanosensory transduction and adaptation. Slit sensilla act as strain sensors in the cuticular exoskeleton; each slit is innervated by two mechanosensitive neurons. Punctate mechanical deformation at four points along the dendrites demonstrated that mechanical excitability is confined to membrane sites at the extreme dendrite tips that are enclosed by cuticular slit structures. Depletion of microtubules in VS-3 neurons by prolonged mechanical stimulation and application of 5 mmol l(-1) colchicine did not disrupt the generation of a receptor potential. Hence, putative gating mechanisms of the mechanically activated membrane channels at the dendrite tips appear to be largely independent of microtubular structures. The discrete adaptation pattern in each of the two partner neurons, rapidly adapting versus slowly adapting, did not depend on the distinct mode of dendrite attachment to cuticular slit structures, and even persisted in isolated neurons after their dendrite tips and auxiliary structures were lost. We suggest that the two discrete adaptation patterns are based on intrinsic differences in the action potential encoding process rather than differences in stimulus transformation or mechanotransduction.     

Slit sense organs and kinesthetic orientation

Summary In the hunting spider Cupiennius salei Keys, kinesthetic orientation towards a catching site from which it has previously been chased away is observed. This ability strongly depends on the lyriform slit sense organs found on femur and tibia of the walking legs. The animals miss the original catching site, if these organs are destroyed on all legs. The mean angular deviation of the starting angles of the returns increases significantly as compared with intact spiders (P<0.005). Also, the directions of the mean vectors of the starting angles change (P<0.05).Supported by a grant of the Deutsche Forschungsgemeinschaft.     

Scanning electron microscoscopy of the second-instar larva of Gasterophilus nasalis

The second-instar larva of the bot fly Gasterophilus nasalis (L.) (Diptera: Gasterophilidae) is described for the first time, based on scanning electron microscope (SEM) studies. On the pseudocephalum the larva bears an antenomaxillary sensory complex formed by the antenna (coeloconic sensilla) and the maxillary palp with a set of six coeloconic sensilla and four basiconica sensilla. The oral opening is latero-posteriorly limited by small spines, and exhibits strongly ornamented maxillae and mandibles. The thoracic and abdominal segments are circled by two bands, each with two rows (except the last segment that has one row) of backwardly pointed spines, and have cuticular depressions. Trichoid and campaniform sensilla surround the larval segments. The anterior spiracular opening is a small aperture. The terminal end of the eighth abdominal segment shows a spiracular cavity, lateral tubercles, eight basiconic and two trichoid sensilla. Each spiracular plate has two slightly curved slits, each with a serrated rima. There is a probable ecdysial scar. The findings of this ultrastructural study are compared with those other of larval flies.     

In search of differences between the two types of sensory cells innervating spider slit sensilla (<Emphasis Type="Italic">Cupiennius salei</Emphasis> Keys.)

The metatarsal lyriform organ of the spider Cupiennius salei is a vibration detector consisting of 21 cuticular slits supplied by two sensory cells each, one ending in the outer and the other at the inner slit membrane. In search of functional differences between the two cell types due to differences in stimulus transmission, we analyzed (1) the adaptation of responses to electrical stimulation, (2) the thresholds for mechanical stimulation and (3) the representation of male courtship vibrations using intracellular recording and staining techniques. Single- and multi-spiking receptor neurons were found among both cell types, which showed high-pass filter characteristics. Below 100-Hz threshold, tarsal deflections were between 1° and 10°. At higher frequencies, they decreased down to values as small as 0.05°, corresponding to 4.5-nm tarsal deflection in the most sensitive cases. Different slits in the organ and receptor cells with slow or fast adaptation did not differ in this regard. When stimulated with male courtship vibrations, both types of receptor cells again did not differ significantly regarding number of action potentials, latency and synchronization coefficients. Surprisingly, the differences in dendrite coupling were not reflected by the physiological responses of the two cell types innervating the slits.