Sensing the Plant Surface Prior to Feeding and Oviposition: Differences in External Ultrastructure and Function Among Tarsi of <Emphasis Type="Italic">Heliconius erato</Emphasis>

Adult foretarsi of Heliconius erato Linnaeus (Lepidoptera, Nymphalidae) are reduced in size and are not used for walking. Foretarsi of the female have specialized sensilla that are presumably used to identify the host plant, by drumming. The mid- and hind tarsi also bear sensilla in both sexes, but these have not been described in detail, nor has their chemosensory function been determined. We described and compared the tarsi of H. erato under light and scanning electron microscopy. Behavioral experiments showed that differences in the shape, number, and size of sensilla were related to feeding and oviposition behaviors. Two types of sensillum (chaeticum and trichodeum) were found in similar numbers and size on the mid- and hind tarsi of both sexes. Sensilla on the female foretarsi act in host-plant site selection, strongly affecting oviposition rates when isolated. Male foretarsi lack sensilla, which may have been selected against due to the absence of function and thus lost. Sensilla on the mid- and hind tarsi are involved in sugar detection in both sexes, responding to an effective dose of sucrose (ED₅₀) near 0.01 M, and therefore might be used to identify food resources when the butterflies settle on flowers.     

Behavioural and chemosensory responses of the turnip root fly (Delia floralis) to glucosinolates

This study investigates the behavioural and neural mechanisms involved in the oviposition behaviour of the turnip root fly,Delia floralis (Fallen). Behavioural studies showed that glucosinolates modulated the oviposition behaviour of the flies on artificial leaves as well as the number of eggs laid in the soil at the base of these leaves. Electrophysiological responses to glucosinolates were obtained from type A and type D sensilla on the prothoracic and mesothoracic tarsi, as well as from the long contact sensilla on the labellum. The neural responses from these sensilla were positively correlated with the oviposition behaviour of the flies and with the number of eggs laid. Of the eleven glucosinolates tested in the behavioural and electrophysiological tests, the flies were most responsive to glucobrassicanapin, gluconapin and glucobrassicin. The type D tarsal sensilla were more responsive to the glucosinolates than either the type A tarsal sensilla or the labellar sensilla. The structure-activity investigations showed that slight modifications to the chemical composition of the glucosinolates resulted in changes in neural activity.     

Sexual dimorphism of antennal,tarsal and ovipositor chemosensilla in the African stemborer,Busseola fusca (Fuller) (Lepidoptera: Noctuidae)

The number and distribution of chemosensilla located on different organs of Busseola fusca (Fuller) (Lepidoptera: Noctuidae) males and females are described based on observations using scanning electron microscopy, selective staining with silver nitrate, and gustatory electrophysiological recording. The antennae and the fifth tarsomere of the prothoracic legs of both sexes bear chemosensilla: uniporous chaetica and multiporous trichoidea sensilla. However, there is a sexual dimorphism in the number and size of sensilla on these organs. The distal part of the ovipositor has uniporous gustatory chemosensilla of the chaetica type. The involvement of these sensilla in oviposition site selection by B. fusca is discussed.     

Morphological and electrophysiological mapping of tarsal chemoreceptors of oviposition-deterring pheromone in Rhagoletis pomonella flies

Light microscopy and S.E.M. observations revealed that Rhagoletis pomonella female tarsi, bearing the principal receptors of oviposition-deterring fruit marking pheromone (ODP), have 3 types of chemosensilla: B, C and D. Using electrophysiological hair tip-recording techniques, we found that D chemosensilla located in pairs on distal ventrolateral portions of the 2nd, 3rd and 4th tarsomeres of each leg were highly sensitive to stimulation by the pheromone. D chemosensilla located in pairs on the 5th tarsomere of each leg were moderately sensitive to the pheromone, while the B and C chemosensilla of all tarsi were nearly or completely insensitive to it. For reasons discussed, the D chemosensilla on the prothoracic tarsi may be the most important in providing sensory input eliciting oviposition deterrence.     

Time course of the Houseflies' landing response

The landing response of stationary flying houseflies Musca domestica has been recorded on video tape. The leg movements were quantitatively evaluated. It could be demonstrated that:

1. only the first two pairs of legs are involved in the reaction (Fig. 1). Prothoracic tarsi are lifted beyond the head, mesothoracic tarsi are lowered and moved sidewards (Fig. 2a and b).
2. the movement of the tarsal tips is mainly due to an opening of one single joint per leg, i.e. the femurtibia joint of the prothoracic leg (Fig. 2c), and the coxa-femur joint of the mesothoracic leg.
3. the landing reaction is a fixed action pattern which does not seem to require further sensory input once it is released (Fig. 4d).
4. the landing responses to a light-off stimulus and to expanding patterns with different angular velocities are indistinguishable (compare Fig. 3a-c with Fig. 2a-c). The only parameter that is obviously dependent on the stimulus conditions, is the latency of the reaction (Fig. 4a-c).

     

Tarsal contact chemoreceptor response to glucosinolates and cardenolides mediating oviposition in Pieris rape

Abstract. Water-soluble extracts of a host crucifer (Brassica oleracea L.) and non-host crucifer (Erysimum cheiranthoides L.) and isolated pure cardenolides and glucosinolates were tested on Pieris rapae L. (Lepidoptera: Pieridae) butterflies in oviposition assays and by electrophysiological recordings from the contact-chemoreceptor sensilla of the prothoracic tarsi. Ten different glucosinolates stimulated oviposition to varying degree when put on non-host plant leaves. The most active compounds were glucobrassiein and gluconasturtiin (methylindole and phenylethyl aglycone), whereas glucocapparin, sinalbin. glucotropaeolin, sinigrin and glucoalyssinin had intermediate activity. Glucocheirolin, glucoerucin and glucoiberin (sulphur-containing aglycone) were significantly less active. Of eight cardenolides applied to host-plant leaves (100 μg each), four glycosides deterred oviposition strongly (erysimoside, erychroside, cymarin and K-strophanthin-β). Erycordin, helveticoside, digitoxin and strophanthidin had little or no deterrent activity. Sensilla located laterally on the prothoracic tarsi of female butterflies contained one receptor cell sensitive to sucrose. None of the tested extracts or pure compounds stimulated any cell in these sensilla. In contrast, the cells in the medial sensilla showed little or no sensitivity to sucrose. One cell was found to be sensitive to cardenolide glycosides. The threshold for one of the most active compounds, erychroside, was about 0.1 μg/ml (1.5 times 10^-7 M). Two receptor cells, characterized by spikes of differing amplitude, were sensitive to glucosinolates. One of these, with larger amplitude spikes, seemed to be the same as the cell sensitive to cardenolides. The threshold for the most active glucosinolates, glucobrassicin and gluconasturtiin was estimated to be below 0.1 mg/ml (2 times 10^-4 M). The neural activity of both classes of compounds, cardenolides and glucosinolates, was significantly correlated with their behavioural activity as deterrents or stimulants.     

The problem of the number of tarsomeres in the regenerated cockroach leg.

There are 5 tarsomeres in the normal cockroach leg, but this number is often reduced in regenerated legs. In order to examine this complicated situation, fore-, mid-, and hindlegs of German cockroaches were amputated at 11 different tarsal levels and at 18 different times during the last instar. When tarsi were amputated at or proximal to the 3rd tarsomere, 4-segmented tarsi regenerated. When legs were amputated distal to the 3rd tarsomere, the regenerated tarsi had 5 segments. Three-segmented tarsi rarely regenerated when legs were amputated proximal to 3rd tarsomere and in the latter half of the instar period. The lengths of all tarsomeres of regenerated tarsi were measured together with those of unoperated contralateral tarsomeres, and the ratios of the former to the latter were calculated. The ratios ranged from 28 to 138% for the various tarsomeres and levels of amputation. From a comparison of the ratios and morphological observations, it was suggested that the 3rd tarsomere of the normal 5-segmented tarsus has disappeared in the regenerated 4-segmented tarsus. Pads and disto-lateral spines of tarsomeres were observed on unoperated and regenerated tarsi. It was of interest that double spines were often found on the 4-segmented tarsi, mostly on the 2nd tarsomere, just proximal to the position of the missing 3rd tarsomere. This observation supported the idea that the 3rd tarsomere has not simply disappeared, but has probably fused with the 2nd tarsomere.     

Reproductive strategies and parasitization behavior of Ageniaspis citricola, a parasitoid of the citrus leafminer Phyllocnistis citrella

We describe the number, distribution, and function of sensilla located on different organs of Lobesia botrana (Lepidoptera: Tortricidae) females using scanning electron microscopy, selective staining, and contact electrophysiology. The tarsi of the prothoracic legs bear contact chemo‐mechanoreceptor sensilla chaetica (5–13 per tarsomere), arranged in rings mainly concentrated on ventral surfaces, and different mechanosensory structures (sensilla chaetica, sensilla squamiformia, sensilla campaniformia, and spines). A single contact chemo‐mechanoreceptor sensillum chaeticum is present between the claws on the pretarsus. The ventral surface of the ovipositor lobes is covered with numerous mechanosensory sensilla chaetica of different types, out of which 10 have a contact chemosensory function. Putative contact chemo‐mechanoreceptor sensilla were also observed on the proboscis and antenna. Longitudinal rows of alternated sensilla styloconica and basiconica are present on the distal part of the proboscis, and rings of sensilla chaetica are present at the antennal tip. The sensilla on these body parts may play different roles in the selection of an oviposition site.     

Kinematics and motor activity during tethered walking and turning in the cockroach, <Emphasis Type="Italic">Blaberus discoidalis</Emphasis>

When insects turn from walking straight, their legs have to follow different motor patterns. In order to examine such pattern change precisely, we stimulated single antenna of an insect, thereby initiating its turning behavior, tethered over a lightly oiled glass plate. The resulting behavior included asymmetrical movements of prothoracic and mesothoracic legs. The mesothoracic leg on the inside of the turn (in the apparent direction of turning) extended the coxa-trochanter and femur-tibia joints during swing rather than during stance as in walking, while the outside mesothoracic leg kept a slow walking pattern. Electromyograms in mesothoracic legs revealed consistent changes in the motor neuron activity controlling extension of the coxa-trochanter and femur-tibia joints. In tethered walking, depressor trochanter activity consistently preceded slow extensor tibia activity. This pattern was reversed in the inside mesothoracic leg during turning. Also for turning, extensor and depressor motor neurons of the inside legs were activated in swing phase instead of stance. Turning was also examined in free ranging animals. Although more variable, some trials resembled the pattern generated by tethered animals. The distinct inter-joint and inter-leg coordination between tethered turning and walking, therefore, provides a good model to further study the neural control of changing locomotion patterns.     

Contact chemoreception related to host selection and oviposition behaviour in the monarch butterfly, Danaus plexippus

Abstract. Behavioural events during host selection by ovipositing monarch butterflies (Danaus plexippus (L.), Danainae, Nymphalidae) include tapping the leaf surface with fore-tarsi and touching this surface with mid-tarsi (‘drumming’) and antennae. Flavonoids identified from host plant extracts are known to stimulate oviposition. Scanning electron microscopy revealed the presence of contact-chemoreceptor sensilla on all appendages that contact the leaf surface. This electrophysiological study was conducted to identify the contact chemoreceptors that are sensitive to the known oviposition stimuli and are therefore probably involved in host recognition. Receptor cells of conspicuous sensilla grouped in clusters on fore-tarsi of females were sensitive to the behaviourally active butanol fraction of host plant (Asclepias curassavica) extract. However, these receptors generally had low sensitivity to three oviposition-stimulating flavonoids identified from this fraction, but they were also sensitive to the butanol fraction of a non-host (Brassica oleracea). Chemoreceptors in sensilla of the tarsomers 2–4 of the mid-legs also responded to the behaviourally active fraction of host plant extract and showed some sensitivity to two of the flavonoids that stimulate oviposition. Similar results were obtained from receptor cells in sensilla on the tip of the antennae. Most of these sensilla had cells responding to the butanol fraction of A. curassavica extract but only 25% of them were also sensitive to one of the behaviourally active flavonoids. These electrophysiological results, in combination with behavioural observations, suggest that host selection in monarch butterflies relies on a complex pattern of peripheral sensory information from several types of tarsal and antennal contact chemoreceptors.     

Morphology and distribution of sensilia on the cephalic appendages,tarsi and ovipositor of the European sunflower moth,Homoeosoma nebulella Den. & Schiff. (Lepidoptera : Pyralidae)

Sensilla on male and female antennae, mouthparts, tarsi and on the ovipositor of the European sunflower moth, Homoeosoma nebulella (Lepidoptera : Pyralidae) have been investigated by means of scanning electron microscope. The antennal flagellum bears multiporous sensilla (trichodea, basiconica, auricillica, coeloconica) and uniporous sensilla (chaetica, styloconica). A sexual dimorphism is found in the numbers of sensilla trichodea (8300 in males and 6000 in females) and sensilla basiconica (1150 in females and 650 in males). The proboscis has uniporous s. styloconica, multiporous s. basiconica (described for the first time in Lepidoptera), aporous s. chaetica, and some rare uniporous s. basiconica in the food channel. The labial palp-pit organ houses multiporous s. coeloconica, while the maxillary palps have aporous sensilla. Tarsi of both sexes possess one type of aporous s. chaetica and 2 types of uniporous s. chaetica. There is no significant difference in the distribution of tarsal sensilla between males and females. The surface of each lobe of the ovipositor is covered by 3 types of aporous s. trichodea of different lengths and about 60 multiporous s. basiconica, sensilla unusual on the ovipositor of Lepidoptera. The role of sensilla in the oviposition site selection is discussed.     

Sexually dimorphic legs in a neotropical harvestman (Arachnida,Opiliones): Ornament or weapon?

The evolution of sexually dimorphic traits has been the focus of much theoretical work, but empirical approaches to this topic have not been equally prolific. Males of the neotropical family Gonyleptidae usually present a strong fourth pair of legs armed with spines, but their functional significance is unknown. We investigated the putative functions of the leg armature in the harvestman Neosadocus maximus. Being a non-visual species, the spines on male legs can only be perceived by females through physical contact. Thus, we could expect females to touch the armature on the legs of their mates if they were to evaluate it. However, we found no support for this hypothesis. We did show that (1) leg armature is used as a weapon in contests between males and (2) spines and associated sensilla are sexually dimorphic structures involved in "nipping behavior", during which a winner emerged in most fights. Finally, we demonstrate that five body structures directly involved in male-male fights show positive allometry in males, presenting slopes higher than 1, whereas the same structures show either no or negative allometry in the case of females. In conclusion, leg armature in male harvestmen is clearly used as a device in intrasexual contests.     

Sensilla on antennae,ovipositor and tarsi of the larval parasitoids,Cotesia sesamiae (Cameron 1906) and Cotesia flavipes Cameron 1891 (Hymenoptera: Braconidae): a comparative scanning electron microscopy study

Two braconid parasitoids of cereal stemborers in eastern Africa, Cotesia sesamiae and Cotesia flavipes, have been shown to display a similar hierarchy of behavioural events during host recognition and acceptance. In order to understand the mechanisms underlying host recognition and acceptance, the morphology of antennal sensilla on the last antennomeres, on the ovipositor, and on the fifth tarsomere and pretarsus of the prothoracic legs tarsi were studied using scanning electron microscopy followed by selective silver nitrate staining. It appeared that female C. sesamiae and C. flavipes shared the same types and distribution of sensory receptors, which enable them to detect volatiles and contact chemical stimuli from their hosts. In both parasitoids, four types of sensilla were identified on the three terminal antennomeres: (i) non-porous sensilla trichodea likely to be involved in mechanoreception, (ii) uniporous sensilla chaetica with porous tips that have gustatory functions, (iii) multiporous sensilla placodea, which are likely to have olfactory function, and (iv) sensilla coeloconica known to have thermo-hygroreceptive function. The tarsi of both parasitoids possessed a few uniporous sensilla chaetica with porous tips, which may have gustatory functions. The distal end of the ovipositor bore numerous dome-shaped sensilla. However, there were no sensilla coeloconica or styloconica, known to have gustatory function in other parasitoid species, on the ovipositors of the two braconid wasps.     

Ultrastructure of chemoreceptive tarsal sensilla in an armored harvestman and evidence of olfaction across Laniatores (Arachnida,Opiliones)

Harvestmen (Arachnida, Opiliones) are especially dependent on chemical cues and are often regarded as animals that rely mainly on contact chemoreception. Information on harvestman sensilla is scarce when compared to other arachnid orders, especially concerning internal morphology. Using scanning (SEM) and transmission (TEM) electron microscopy, we investigated tarsal sensilla on the distal tarsomeres (DT) of all leg pairs in Heteromitobates discolor (Laniatores, Gonyleptidae). Furthermore, we explored the typological diversity of sensilla present on the DT I and II in members of the suborder Laniatores, which include two thirds of the formally described opilionid fauna, using species from 17 families representing all main laniatorian lineages. Our data revealed that DT I and II of H. discolor are equipped with wall-pored falciform hairs (two types), wall-pored sensilla chaetica (two types) and tip-pored sensilla chaetica, while DT III and IV are mainly covered with trichomes (non-sensory) and tip-pored sensilla chaetica. The ultrastructural characteristics support an olfactory function for all wall-pored sensilla and a dual gustatory/mechanoreceptive function for tip-pored sensilla chaetica. Based on our comparative SEM survey, we show that wall-pored sensilla occur in all investigated Laniatores, demonstrating their widespread occurrence in the suborder and highlighting the importance of both legs I and II as the sensory appendages of laniatorean harvestmen. Our results provide the first morphological evidence for olfactory receptors in Laniatores and suggest that olfaction is more important for harvestmen than previously thought.     

Obstacle perception by insect antennae during terrestrial locomotion

Abstract. Insect antennae bear several types of sensilla including chemo-receptors, hygroreceptors, thermoreceptors and mechanoreceptors. A large proportion of sensilla is chemoreceptors, providing olfactory function. Pro-prioreceptors located on the antennae provide information on the position of these organs and are used in flight control. This type of sensillum is present in most insects and might serve other functions. We tested the hypothesis that antennae are used to perceive obstacles in the path of walking beetles. When adult Colorado potato beetles, Leptinotarsa decemlineata (Say), touch an obstacle with their antennae during terrestrial locomotion, they modify the angle of their body to allow the tarsi of one prothoracic leg to reach the top of the obstacle. Our results demonstrate that antennae, by their movements and their position ahead of the beetle, provide information on the presence of the obstacle necessary to initiate step-up behaviour. Furthermore, the change in the body angle needed to increase the reach of the prothoracic leg and step on the obstacle, is proportional to the height of the obstacle. Since the eyes are not involved in the process, normal behaviour can be performed in the dark.     

Variation in the ontogenetic allometry of horn length in bovids along a body mass continuum

Allometric relationships describe the proportional covariation between morphological, physiological, or life‐history traits and the size of the organisms. Evolutionary allometries estimated among species are expected to result from species differences in ontogenetic allometry, but it remains uncertain whether ontogenetic allometric parameters and particularly the ontogenetic slope can evolve. In bovids, the nonlinear evolutionary allometry between horn length and body mass in males suggests systematic changes in ontogenetic allometry with increasing species body mass. To test this hypothesis, we estimated ontogenetic allometry between horn length and body mass in males and females of 19 bovid species ranging from ca. 5 to 700 kg. Ontogenetic allometry changed systematically with species body mass from steep ontogenetic allometries over a short period of horn growth in small species to shallow allometry with the growth period of horns matching the period of body mass increase in the largest species. Intermediate species displayed steep allometry over long period of horn growth. Females tended to display shallower ontogenetic allometry with longer horn growth compared to males, but these differences were weak and highly variable. These findings show that ontogenetic allometric slope evolved across species possibly as a response to size‐related changes in the selection pressures acting on horn length and body mass.     

Sexual dimorphism in Diabrotica speciosa and Diabrotica viridula (Coleoptera: Chrysomelidae)

Diabrotica speciosa (Germar) and Diabrotica viridula F. (Coleoptera: Chrysomelidae) are the two most abundant species of the genus in South America, and belong to the fucata and virgifera groups, respectively. Here, we characterize the dimorphism of the setae present on the basitarsi of males and females of these species. Dimorphism was confirmed in both species, and it was related to the presence of adhesive setae exclusively in males, which possess these structures on the basal tarsomeres of the pro- and mesothoracic legs.     

Central projections of sensory cells of the midleg of the locust,Schistocerca gregaria

The central projections of trichoid hairs and of some scolopidial organs of the mesothoracic leg of the locust Schistocerca gregaria were studied by using nickel chloride backfilling and single cell recording. Trichoid hair sensilla on different parts of the legs project somatotopically in the ventral part of the ipsilateral neuropile of the mesothoracic ganglion. Generally, distally located receptors have their terminal arborizations in ventro-lateral areas of the neuropile, and proximally located receptors in ventro-medial areas. The axons of the subgenual organ and tarsal chordotonal organs project into the intermediate neuropile.     

Sexual Selection,Ontogenetic Acceleration,and Hypermorphosis Generates Male Trimorphism in Wellington Tree Weta

Strong sex-specific selection on traits common to both sexes typically results in sexual dimorphism. Here we find that Wellington tree weta (Hemideina crassidens) are sexually dimorphic in both head shape and size due to differential selection pressures on the sexes: males use their heads in male-male combat and feeding whereas females use theirs for feeding only. Remarkably, the sexes share a common ontogenetic trajectory with respect to head growth. Male head shape allometry is an extension of the female’s trajectory despite maturing two instars earlier, a feat achieved through ontogenetic acceleration and hypermorphosis. Strong sexual selection also favours the evolution of alternative reproductive strategies in which some males produce morphologically different weapons. Wild-caught male H. crassidens are trimorphic with regard to weapon size, a rare phenomenon in nature, and weapon shape is related to each morph’s putative mating strategy.