Tarsal Hairs Research Articles

Habituation of Sugar-Induced Proboscis Extension Reflex and Yeast-Induced Habituation Override in Drosophila melanogaster.

Habituation, the process by which animals learn to ignore insignificant stimuli, facilitates engagement with salient features of the environment. However, neural mechanisms underlying habituation also allow responses to familiar stimuli to be reinstated when such stimuli become potentially significant. Thus, the habituated state must allow a mechanism for habituation override. The remarkably precise knowledge of cell identity, connectivity, and information coding in Drosophila sensory circuits, as well as the availability of tools to genetically target these cells, makes Drosophila a valuable and important organism for analysis of habituation and habituation-override mechanisms. Studies of olfactory and gustatory habituation in Drosophila suggest that potentiation of GABAergic neurons underlies certain timescales of habituation and have specified some elements of a gustatory habituation-override pathway. More detailed understanding of gustatory habituation and habituation-override mechanisms will benefit from access to robust behavioral assays for (a) the proboscis extension reflex (PER) elicited by a sweet stimulus, (b) exposure paradigms that result in PER habituation, and, most critically, (c) manipulations that result in PER-habituation override. Here, we describe simple protocols for persistent sucrose exposure of tarsal hairs that lead to habituation of proboscis extension and for presentation of a novel appetitive stimuli that reinstate robust PER to habituated flies. This detailed protocol of gustatory habituation provides (a) a simple method to induce habituation by continuous exposure of the flies to sucrose for 10 min without leading to ingestion and (b) a novel method to override habituation by presenting yeast to the proboscis. Key features • A protocol for stimulation of Drosophila's taste (sugar) sensory neurons that induces gustatory habituation without satiation due to ingestion. • A chemical (yeast) stimulation protocol that rapidly induces habituation override/dishabituation in sugar-habituated Drosophila.

Mechanisms of detachment in fibrillar adhesive systems

Several creatures can climb on smooth surfaces with the help of hairy adhesive pads on their legs. A rapid change from strong attachment to effortless detachment of the leg is enabled by the asymmetric geometry of the tarsal hairs. In this study, we propose mechanisms by which the hairy pad can be easily detached, even when the hairs possess no asymmetry. Here, we examine the possible function of the tibia-tarsus leg joint and the claws. Based on a spring-based model, we consider three modes of detachment: vertically pulling the pad while maintaining either a (1) fixed or a (2) free joint, or by (3) flexing the pad about the claw. We show that in all cases, the adhesion force can be significantly reduced due to elastic forces when the hairs deform non-uniformly across the array. Our proposed model illustrates the design advantage of such fibrillar adhesive systems, that not only provide strong adhesion, but also allow easy detachment, making them suitable as organs for fast locomotion and reliable hold. The presented approaches can be potentially used to switch the adhesion state in bio-inspired fibrillar adhesives, by incorporating artificial joints and claws into their design, without the need of asymmetric or stimuli-responsive fibrillar structures.

A Drosophila Circuit for Habituation Override.

Habituated animals retain a latent capacity for robust engagement with familiar stimuli. In most instances, the ability to override habituation is best explained by postulating that habituation arises from the potentiation of inhibitory inputs onto stimulus-encoding assemblies and that habituation override occurs through disinhibition. Previous work has shown that inhibitory plasticity contributes to specific forms of olfactory and gustatory habituation in Drosophila Here, we analyze how exposure to a novel stimulus causes override of gustatory (proboscis extension reflex; PER) habituation. While brief sucrose contact with tarsal hairs causes naive Drosophila to extend their proboscis, persistent exposure reduces PER to subsequent sucrose stimuli. We show that in so habituated animals, either brief exposure of the proboscis to yeast or direct thermogenetic activation of sensory neurons restores PER response to tarsal sucrose stimulation. Similar override of PER habituation can also be induced by brief thermogenetic activation of a population of tyrosine hydroxylase (TH)-positive neurons, a subset of which send projections to the subesophageal zone (SEZ). Significantly, sensory-neuron induced habituation override requires transmitter release from these TH-positive cells. Treatments that cause override specifically influence the habituated state, with no effect on the naive sucrose response across a range of concentrations. Taken together with other findings, these observations in female flies are consistent with a model in which novel taste stimuli trigger activity in dopaminergic neurons which, directly or indirectly, inhibit GABAergic cells that drive PER habituation. The implications of these findings for general mechanisms of attentional and sensory override of habituation are discussed.SIGNIFICANCE STATEMENT Habituation can be overcome when a new context requires an enhanced response to a familiar stimulus. However, the underlying mechanisms remain incompletely understood. Previous studies have provided evidence that habituation of the sucrose-induced proboscis extension reflex (PER) in Drosophila occurs through potentiation of inhibition onto the PER pathway. This work defines controlled protocols for override of PER habituation and uses them to outline the underlying circuit mechanisms. The results presented support a model in which novel taste stimuli cause dishabituation by activating a subset of tyrosine hydroxylase (TH)-expressing neurons that inhibit GABAergic neurons whose potentiation underlies PER habituation. At a general level, these findings further highlight a central role for inhibition and disinhibition in the control of behavioral flexibility.

Are trichobothria used in terrestrial prey capture by the yellow scorpion Tityus serrulatus Lutz & Mello, 1922 (Buthidae)?

Many arachnids rely on substrate-borne vibrations and air displacement to detect prey. Air-flow stimuli may be detected by long setae called trichobothria, which occur on scorpion pedipalps, but seldom have their functions been addressed in these animals. We tested the hypothesis that trichobothria on scorpion pedipalps are important for capturing terrestrial prey in the scorpion Tityus serrulatus. We predicted that scorpions with trichobothria experimentally removed would be less successful in capturing terrestrial prey than the control groups. We also predicted that scorpions without trichobothria would have a higher number of capture attempts, that the latency to detect prey and to the first capture attempts would be higher, and the number of times that scorpions oriented their body towards the prey would be lower. We used an experimental subject and a cricket in an arena with a paper sheet as substrate. We did not find differences in the measured variables between the groups. Other sensory organs, such as basitarsal compound slit sensilla and tarsal hairs would enable scorpions to detect prey by substrate-borne vibrations, compensating for the lack of trichobothria. Our results suggest that the trichobothria of T. serrulatus may not be essential to capture terrestrial prey.

Gripping ease in southern green stink bugsNezara viridulaL. (Heteroptera: Pentatomidae): Coping with geometry, orientation and surface wettability of substrate

AbstractThe southern green stink bugNezara viridulaL. (Heteroptera, Pentatomidae) is highly polyphagous, preferring apically situated seeds and fruits on more than 150 plant species belonging to over 30 plant families all over the world. This forces them to move over highly variable terrains, including plant stems, leaves, pods and buds, which requires efficient attachment. Stink bugs have long slender legs and feet (tarsi) equipped with paired curved claws, paired soft adhesive pads (pulvilli), and flattened lanceolate hairs (setae), which arise ventrally on the first and second foot segments (tarsomeres). To characterize their attachment abilities on well‐defined test substrates, here we comparatively measured and analyzed the traction forces of bugs walking horizontally and vertically on hydrophilic (water attractive) and hydrophobic (water repellent) glass plates and rods. The latter correspond to the geometry of preferred feeding sites of stink bugs in the field. The results show a clear contribution of tarsal flattened lanceolate hairs to the stink bug's attachment. Higher traction forces are generated on a glass rod than on a glass plate, corresponding to up to individual maximum of 43 times the stink bug's body weight. Substrate hydrophobicity promotes the attachment, while the measured forces are up to eight times lower when tarsal hairs are disabled. The combination of smooth and hairy tarsal pads results in a remarkable attachment ability, which enablesN. viridulato climb unstable apical plant parts, and supports their invasive behavior and global dispersion.

On Heels and Toes: How Ants Climb with Adhesive Pads and Tarsal Friction Hair Arrays.

Ants are able to climb effortlessly on vertical and inverted smooth surfaces. When climbing, their feet touch the substrate not only with their pretarsal adhesive pads but also with dense arrays of fine hairs on the ventral side of the 3rd and 4th tarsal segments. To understand what role these different attachment structures play during locomotion, we analysed leg kinematics and recorded single-leg ground reaction forces in Weaver ants (Oecophylla smaragdina) climbing vertically on a smooth glass substrate. We found that the ants engaged different attachment structures depending on whether their feet were above or below their Centre of Mass (CoM). Legs above the CoM pulled and engaged the arolia (‘toes’), whereas legs below the CoM pushed with the 3rd and 4th tarsomeres (‘heels’) in surface contact. Legs above the CoM carried a significantly larger proportion of the body weight than legs below the CoM. Force measurements on individual ant tarsi showed that friction increased with normal load as a result of the bending and increasing side contact of the tarsal hairs. On a rough sandpaper substrate, the tarsal hairs generated higher friction forces in the pushing than in the pulling direction, whereas the reverse effect was found on the smooth substrate. When the tarsal hairs were pushed, buckling was observed for forces exceeding the shear forces found in climbing ants. Adhesion forces were small but not negligible, and higher on the smooth substrate. Our results indicate that the dense tarsal hair arrays produce friction forces when pressed against the substrate, and help the ants to push outwards during horizontal and vertical walking.

Beetle adhesive hairs differ in stiffness and stickiness: in vivo adhesion measurements on individual setae

Leaf beetles are able to climb on smooth and rough surfaces using arrays of micron-sized adhesive hairs (setae) of varying morphology. We report the first in vivo adhesive force measurements of individual setae in the beetle Gastrophysa viridula, using a smooth polystyrene substrate attached to a glass capillary micro-cantilever. The beetles possess three distinct adhesive pads on each leg which differ in function and setal morphology. Visualisation of pull-offs allowed forces to be measured for each tarsal hair type. Male discoidal hairs adhered with the highest forces (919 ± 104nN, mean ± SE), followed by spatulate (582 ± 59nN) and pointed (127 ± 19nN) hairs. Discoidal hairs were stiffer in the normal direction (0.693 ± 0.111N m(-1)) than spatulate (0.364 ± 0.039N m(-1)) or pointed (0.192 ± 0.044N m(-1)) hairs. The greater adhesion on smooth surfaces and the higher stability of discoidal hairs help male beetles to achieve strong adhesion on the elytra of females during copulation. A comparison of pull-off forces measured for single setae and whole pads (arrays) revealed comparable levels of adhesive stress. This suggests that beetles are able to achieve equal load sharing across their adhesive pads so that detachment through peeling is prevented.

Bimodal Pollination by Wasps and Beetles in the African Milkweed Xysmalobium undulatum

ABSTRACTIt has been suggested that flowers of some plants are specialized for pollination by two unrelated species (or functional groups) of pollinators. However, evidence for ‘bimodal pollination systems’ has been extremely limited. Studies of the milkweed Xysmalobium undulatum in South Africa showed that its flowers are visited by a range of different insects (representing 18 families), but only two groups, represented by the chafer beetle Atrichelaphinis tigrina and pompilid wasps in the genus Hemipepsis, effect pollination. Experiments showed that both these pollinator groups are effective in removing and inserting pollinia. Pollinia are attached to clypeal hairs and mouthparts on the wasps and tarsal hairs and spines on the beetles. Although considerably less abundant than the beetles, Hemipepsis spp. wasps move more quickly among flowers and appeared to be more effective pollinators overall. Experimental hand‐pollinations conducted in the field showed that X. undulatum is genetically self‐incompatible and thus completely reliant on pollinators for reproduction. We conclude that X. undulatum has a bimodal pollination system, specialized for pollination by Hemipepsis pompilid wasps and the chafer beetle A. tigrina.

Comb-hairs on the fourth tarsi in pholcid spiders (Araneae, Pholcidae)

Comb-hairs on the fourth tarsi of males and females are a classical theridioid character, but they also occur in pholcids. Previous studies on Pholcus phalangioides (Fuesslin 1775) have shown that in this species the comb-hairs function in the context of sticky silk wrap attack just as in theridiids. Here we investigate pholcid comb-hairs in a comparative way, studying the tarsal hairs of representatives of 42 pholcid genera with the SEM. We found two principal morphologies, a simple and a complex type of comb-hair. We found two principal types of comb-hair distribution on the tarsus: in distal patches or in ventral rows, but intermediate types also occur. Character mapping suggests that simple comb-hairs are derived from complex ones, and that distal patches are plesiomorphic, ventral rows derived. We speculate that pholcid comb-hairs may be derived from hairs (the ''accessory claws'') that grasp silk in functional correlation with the median claw. In a female shock-frozen during wrap attack, the silk line passed through the notch of a comb-hair, but several functional details (silk grasping and releasing, function of different hair branches) remain unanswered.

Pollinator‐mediated isolation in sympatric milkweeds (Asclepias): do floral morphology and insect behavior influence species boundaries?

Summary •We explored whether mechanical or ethological differences provide pollinator-mediated floral isolation capable of reinforcing existing species barriers among sympatric Asclepias with divergent floral morphologies: A. incarnata, A. verticiallata and A. syriaca. •In a common garden, we quantified pollinator visitation and flight patterns, differences in corporal attachment of pollinia to insects, and the potential outcome of putative floral barriers for interspecific pollination and fruit set. •We detected significant variation in the importance, constancy, and behavior of major pollinators on sympatric asclepiads, including Bombus, Xylocopa and large sphecid wasps. Pollinia attach differentially to the arolium on insect legs for A. syriaca, but to the tarsal hairs in other asclepiads. Fruit-set was lower in mixed than unispecific patches of Asclepias. •We detected mechanical isolation between A. syriaca and its congeners and a tendency toward wasp pollination in A. verticillata. All three species appear to show some specialization for long-tongued hymenoptera and lepidopterans. Pre–mating barriers provide a potentially effective means of reducing interspecific pollination, but more study is needed in species visited by generalists.

Reflex modulation in locusts walking on a treadwheel intracellular recordings from motoneurons

In locusts (Locusta migratoria) walking on a treadwheel, afferents of tarsal hair sensilla were stimulated via chronically implanted hook electrodes (Fig. 1). Stimuli applied to the middle leg tarsus elicited avoidance reflexes (Fig. 2). In quiescent animals, the leg was lifted off the ground and the femur adducted. In walking locusts, the response was phase-dependent. During the stance phase, no reaction was observed except occasional, premature triggering of swing movements; stimuli applied near the end of the swing phase were able to elicit an additional, short leg protraction.

Pollen-Feeding in Poecilognathus punctipennis (Diptera: Bombyliidae)

Females of the bombyliid fly Poecilognathus punctipennis (Walker) feed avidly on pollen of Commelina erecta L. and Tradescantia roseolens Small (Commelinaceae). The front tarsi rapidly rake pollen from slits in the sides of the anther and transfer the pollen to the tip of the proboscis. Specialized tarsal hairs may assist in pollen collection. Pollen appears to be mixed with a liquid as it is transported the length of the proboscis. The stomach of pollen-collecting flies is distended with pollen. Pollen was also found in stomachs of females of Geron sp. Several types of evidence suggest that P. punctipennis females are specialized to exploit pollen of Commelinaceae, especially T. roseolens. There is no evidence that the plants have a coevolved symbiosis with the flies.

SPECIALIZED TARSAL HAIRS ON ADULT MALE COLORADO POTATO BEETLES, LEPTINOTARSA DECEMLINEATA (SAY), HAMPER ITS LOCOMOTION ON SMOOTH SURFACES

AbstractTarsi of male Colorado potato beetles adhere to glass and plastic surfaces limiting locomotion greatly. This is not observed with females. Scoop-like tarsal hairs present only in males are responsible for the adherence. The effect of this morphological difference on toxicological or behavioral research conducted in glass or plastic cages is discussed.

The morphology of a population of thoracic intersegmental interneurones in the locust.

A population of intersegmental interneurones with axons extending from the meso- to the metathoracic ganglion of the locust is described. They receive specific mechanosensory inputs from one mesothoracic leg. Their cell bodies are in group at the posterior of the mesothoracic ganglion, lying over the lateral base of each connective, and their primary neurites emerge in one of four bundles. Their mesothoracic branches are ipsilateral to the cell bodies and the leg from which they receive inputs. Each interneurone has two to six mesothoracic secondary neurites that divide and form a dense field of arborizations in specific regions of the neuropil so that each individual interneurone has a characteristic shape that is an elaboration of a basic and common plan. An interneurone excited by tibial campaniform sensilla and tarsal hair afferents branches in the intermediate neuropil and the ventral association center where the afferents from these receptors also project. An interneurone excited by proprioceptive inputs from the tarsus arborizes in the dorsal and intermediate neuropils, lateral to the ventral intermediate and ventral median tracts, in the same area as the proprioceptors afferents. An interneurone inhibited by proprioceptive inputs from the tibia (and wing) arborizes only in the dorsal neuropil, where there are no afferent projections. Some interneurones have one to three axonal branches with sparse and varicose side branches in the mesothoracic ganglion, which resemble the metathoracic axonal branches. The metathoracic axonal branches are mostly restricted to the dorsal neuropil and the dorsal part of the intermediate neuropil where local non-spiking interneurones and motor neurones controlling movements of the hind leg also project. The overlap between the branches of the sensory afferents and the intersegmental interneurones in the mesothoracic ganglion and between those of the nonspiking local interneurones or motor neurones and intersegmental interneurones in the metathoracic ganglion suggest that these interneurones are responsible for transferring information about the action of one leg to an adjacent leg.

The effects of behaviourally relevant temperatures on mechanosensory neurones of the grasshopper, Schistocerca americana.

Grasshopper mechanosensory hair neurones respond to displacement of their associated hairs in a temperature sensitive manner: comparable increases in the number of spikes per stimulus result from increases in temperature with constant stimulus strengths and from increasing stimulus strengths at constant temperature. It is therefore not obvious that neurones in the CNS which receive inputs from mechanosensory hairs would be able to distinguish between these two parameters. The temperatures which populations of mechanosensory hairs on the thorax, head and tarsus experienced were measured in freely moving animals. Animals in thermally heterogeneous environments spent 90% of the accounted time in locations where thoracic temperatures of 32-44 degrees C were maintained (the behaviourally 'preferred' range). Head temperatures covered a wider range, and tarsal temperatures the widest. Different populations of mechanosensory hair neurones exhibited different sensitivities to temperature. Thoracic hair neurones were significantly more temperature sensitive than one of the two populations of head hairs studied, and tarsal hairs exhibited a pronounced temperature compensation in the behaviourally 'preferred' range. Wind sensitive head hairs, however, showed exceptionally high temperature sensitivities. There is a negative correlation between the temperature sensitivity of a population of mechanosensory hair neurones and the temperature variability to which those neurones are normally exposed. Implications of this correlation for the central interpretation of mechanosensory input are considered.

Influence of feeding conditions on wing, labellar and tarsal hair resistance inPhormia regina (Meig.)

Feeding enhances resitance of wing, tarsal and labellar hairs ofPhormia regina Meig. The observed increase in resistance might be related to variations in the secretory function of the accessory cells at the hair sockets. The importance of this fact in feeding control is discussed.

Gustatory mechanisms and sugar‐feeding in the mosquito, Culiseta inornata

ABSTRACT. Gustatory hairs on the legs and mouthparts of the mosquito, Culiseta inornata, were stimulated with sucrose solutions to determine their role in the finding and consuming of nectar by females. Stimulation of tarsi initiated probing, which continued without subsequent stimulation of tarsal hairs. Turning in response to tarsal stimulation depended on which leg was stimulated. Once gustatory hairs on the labella were stimulated, turning and probing were discontinued. Stimulation of the hairs on the external surface of the labella apparently initiates the labellar opening response, while stimulation of hairs on the oral surface of the labella maintains the labellar response. Electrophysiologically recorded activity of cibarial and pharyngeal pumps was used to assess the influence of the five relevant sets of gustatory hairs on initiation of sucking. None of the sets alone were capable of initiating sucking. Sucking was initiated when the hairs on the oral surface of the labella were stimulated simultaneously with sensory hairs on the tip of the labrum. The gustatory hairs on the oral surface of the labella exerted considerable influence in determining the amount of sugar or water imbibed.

Osmetrichia: specialized scent hair in black-tailed deer

Black-tailed deer ( Odocoileus hemionus columbianus ) possess a conspicuous tarsal hair tuft covering the tarsal gland which is located on the inside of the hock. The central hairs of that tuft carry a strong smelling mixture of sebaceous and urinary components. These central hairs are short and stiff in comparison to the outer hair of the tuft and the deer's other body hair. These “scent hairs” have large chambers between the cuticular scales, and the scales have comb-like group of ridges. Lipids, in which volatiles are trapped, are held on the hair by these two features. The term “osmetrichia” is proposed for the specialized scent hair. No comparable features were found on hair covering the metatarsal gland of black-tailed deer, the tarsal gland of white-tailed deer ( O. virginianus borealis ); the subauricular gland of pronghorn ( Antilocapra americana ); on scalp, axillary, and pubic hair of Homo sapiens ; or the ventral gland hair of Mongolian gerbils ( Meriones unguiculatus ). SEM pictures of the trough-like osmetrichia of the Mongolian gerbil are presented.

The proboscis extention response and tarsal and labellar chemosensory hairs in the blowfly

Four types of tarsal chemosensory hairs proposed by Grabowski and Dethier (1954) in the blowfly,Phormia regina, were reclassified into the following six types:A-,B1-,B2-,B3-,C- andD-type, based on the electrophysiological results. As for the labellar hairs, the results obtained by Wilczek (1967) agreed well with those in this work. The concentration-response curves of sugar receptors inB2-, andD-type of tarsal hairs and all types of labellar hairs for sugar stimulation were compared in relation to the regression of the acceptance threshold in the proboscis extention response of the blowflies starved for twenty four hours. The initial step of this response could be considered to be triggered mainly by about twelve impulses of every sugar receptor unD-type hairs during initial 0.1 sec after stimulus.

Differential sensitivity of insect chemoreceptors to alkali cations

A technique is described which makes it possible to record—at constant temperature and humidity—the electric responses from taste cells in tarsal as well as labellar hairs of intact, living Calliphora vicina. Upon stimulation of taste hairs of the fly with 0·25 M concentrations of NaCl and KCl, and 0·5 M concentrations of LiCl, NaCl, KCl, RbCl, and CsCl impulses of no more than three different size classes appear. The activities of the primary receptor cells giving rise to these impulses are either positively, or negatively, or not correlated with salt concentration. On stimulation with 0·5 M alkali chlorides in tarsal hairs, no more than one type of impulse is fired by cells positively sensitive to salt concentration, but in labellar hairs two of these cells are active in about 15 per cent of the stimulations. The order of increasing stimulating effectiveness of the alkali cations appears to be irregular in that it does not correspond to their atomic numbers. For cells positively responsive to salt concentration the order is: Li +<Na +≤Cs +<Rb +<K +. For cells not or negatively sensitive to salt concentration it is impossible at present to rank all five alkali cations in a consecutive order, but it is clear that in these cells as well lithium, sodium, and rubidium generally are less stimulating than potassium. It is argued that irregular sequences of alkali and alkaline earth cations—of which many examples may be found in the literature—are indicative of a reaction of these cations with highly polarizable negative groups—probably phosphate groups—in the taste cell membranes.