Antennal Contact Research Articles

The regulation of ant colony foraging activity without spatial information.

Many dynamical networks, such as the ones that produce the collective behavior of social insects, operate without any central control, instead arising from local interactions among individuals. A well-studied example is the formation of recruitment trails in ant colonies, but many ant species do not use pheromone trails. We present a model of the regulation of foraging by harvester ant (Pogonomyrmex barbatus) colonies. This species forages for scattered seeds that one ant can retrieve on its own, so there is no need for spatial information such as pheromone trails that lead ants to specific locations. Previous work shows that colony foraging activity, the rate at which ants go out to search individually for seeds, is regulated in response to current food availability throughout the colony's foraging area. Ants use the rate of brief antennal contacts inside the nest between foragers returning with food and outgoing foragers available to leave the nest on the next foraging trip. Here we present a feedback-based algorithm that captures the main features of data from field experiments in which the rate of returning foragers was manipulated. The algorithm draws on our finding that the distribution of intervals between successive ants returning to the nest is a Poisson process. We fitted the parameter that estimates the effect of each returning forager on the rate at which outgoing foragers leave the nest. We found that correlations between observed rates of returning foragers and simulated rates of outgoing foragers, using our model, were similar to those in the data. Our simple stochastic model shows how the regulation of ant colony foraging can operate without spatial information, describing a process at the level of individual ants that predicts the overall foraging activity of the colony.

Learning Impairment in Honey Bees Caused by Agricultural Spray Adjuvants

BackgroundSpray adjuvants are often applied to crops in conjunction with agricultural pesticides in order to boost the efficacy of the active ingredient(s). The adjuvants themselves are largely assumed to be biologically inert and are therefore subject to minimal scrutiny and toxicological testing by regulatory agencies. Honey bees are exposed to a wide array of pesticides as they conduct normal foraging operations, meaning that they are likely exposed to spray adjuvants as well. It was previously unknown whether these agrochemicals have any deleterious effects on honey bee behavior.Methodology/Principal FindingsAn improved, automated version of the proboscis extension reflex (PER) assay with a high degree of trial-to-trial reproducibility was used to measure the olfactory learning ability of honey bees treated orally with sublethal doses of the most widely used spray adjuvants on almonds in the Central Valley of California. Three different adjuvant classes (nonionic surfactants, crop oil concentrates, and organosilicone surfactants) were investigated in this study. Learning was impaired after ingestion of 20 µg organosilicone surfactant, indicating harmful effects on honey bees caused by agrochemicals previously believed to be innocuous. Organosilicones were more active than the nonionic adjuvants, while the crop oil concentrates were inactive. Ingestion was required for the tested adjuvant to have an effect on learning, as exposure via antennal contact only induced no level of impairment.Conclusions/SignificanceA decrease in percent conditioned response after ingestion of organosilicone surfactants has been demonstrated here for the first time. Olfactory learning is important for foraging honey bees because it allows them to exploit the most productive floral resources in an area at any given time. Impairment of this learning ability may have serious implications for foraging efficiency at the colony level, as well as potentially many social interactions. Organosilicone spray adjuvants may therefore contribute to the ongoing global decline in honey bee health.

Why have long antennae? Exploring the function of antennal contact in snapping shrimp

Many organisms use antennae to gather tactile or chemical information from the environment. Crustaceans have two sets of antennae: short antennules (first antennae) and antennae posterior or lateral to them (second antennae) which are often much longer. While the function of crustacean antennae has received some attention, particularly the perception of dispersed chemical signals by the antennules, the role of direct antennal contact during social behavior is less well understood. We compared antennal contact in competitive and pairing interactions in two species of snapping shrimp: Alpheus angulosus and Alpheus heterochaelis. Conspecific interactions involve more antennal contact than heterospecific interactions. Alpheus heterochaelis perform more antennal contact than A. angulosus. Alpheus angulosus females perform more antennal contact in pairing than in competitions; however, A. heterochaelis females and males of both species use antennal contact equally in pairing and competitive interactions. Although antennal contact carries a risk of injury, such contact appears central to snapping shrimp social behavior.

Asymmetry in antennal contacts during trophallaxis in ants

Behavioural and brain left–right asymmetries are a common feature among the animal kingdom. Lateralization often manifests itself at the population-level with most individuals showing the same direction of lateral bias. Theoretical model based on evolutionary stable strategy predicts that lateralization at the population-level is more likely to characterize social rather than solitary species. Empirical data supporting this hypothesis has been recently obtained in Hymenoptera showing that eusocial honeybees present an asymmetrical use of the antennae: the right antenna is involved in olfactory learning and present more olfactory receptors. However, no evidences about the role of antennal asymmetries in social interactions have been provided so far. Highly social ant species belonging to Formica rufa group are a good model for investigating natural communication because they are able to pass exact information to their nest mates. We applied the “binary tree” experimental paradigm, which allowed us to observe different types of antennal contacts performed by ants out of their nest. To examine possible asymmetrical use of the right and left antenna, we focused on “feeding” (the simplest) contacts where a “donor” ant is exchanging food with a “receiver” ant through trophallaxis. We observed a population-level asymmetry, with the “receiver” ant using the right antenna significantly more often than the left antenna. This study provides the first evidence of lateralization in antennal contacts in ants, and seems to support the hypothesis of mathematical models on the evolution of lateralization suggesting that the alignment of lateralization at the population-level matters in social interactions.

Deciding Which Way to Go: How Do Insects Alter Movements to Negotiate Barriers?

Animals must routinely deal with barriers as they move through their natural environment. These challenges require directed changes in leg movements and posture performed in the context of ever changing internal and external conditions. In particular, cockroaches use a combination of tactile and visual information to evaluate objects in their path in order to effectively guide their movements in complex terrain. When encountering a large block, the insect uses its antennae to evaluate the object’s height then rears upward accordingly before climbing. A shelf presents a choice between climbing and tunneling that depends on how the antennae strike the shelf; tapping from above yields climbing, while tapping from below causes tunneling. However, ambient light conditions detected by the ocelli can bias that decision. Similarly, in a T-maze turning is determined by antennal contact but influenced by visual cues. These multi-sensory behaviors led us to look at the central complex as a center for sensori-motor integration within the insect brain. Visual and antennal tactile cues are processed within the central complex and, in tethered preparations, several central complex units changed firing rates in tandem with or prior to altered step frequency or turning, while stimulation through the implanted electrodes evoked these same behavioral changes. To further test for a central complex role in these decisions, we examined behavioral effects of brain lesions. Electrolytic lesions in restricted regions of the central complex generated site specific behavioral deficits. Similar changes were also found in reversible effects of procaine injections in the brain. Finally, we are examining these kinds of decisions made in a large arena that more closely matches the conditions under which cockroaches forage. Overall, our studies suggest that CC circuits may indeed influence the descending commands associated with navigational decisions, thereby making them more context dependent.

Neural activity in the central complex of the cockroach brain is linked to turning behaviors

An animal moving through complex terrain must consider sensory cues around it and alter its movements accordingly. In the arthropod brain, the central complex (CC) receives highly preprocessed sensory information and sends outputs to premotor regions, suggesting that it may play a role in the central control of oriented locomotion. We performed tetrode recordings within the CC in cockroaches walking on an air-suspended ball to examine the role of the CC in turning behaviors. When a rod was placed near the cockroach's head, the cockroach touched the rod repeatedly with one or both antennae before locomotion was initiated. Some CC units responded to self-generated antennal contact with the object, but at lower levels compared with externally imposed antennal stimulation. The neural activity of other CC units responded to locomotion. We found that some CC units showed discrete firing fields corresponding to specific locomotion states. We also found that changes in firing rate of some CC units preceded changes in turning speed in one direction but not the other. Furthermore, such biased units were located in the side of the brain ipsilateral to the direction of the turning speed they could predict. Moreover, electrical stimulation of the CC elicited or modified locomotion, and the direction of some evoked locomotion could be predicted by the response property of locomotion-predictive units near the stimulation site. Therefore, our results suggest that, at the population level, asymmetrical activity in the CC precedes and influences turning behavior.

Active tactile sampling by an insect in a step-climbing paradigm.

Many insects actively explore their near-range environment with their antennae. Stick insects (Carausius morosus) rhythmically move their antennae during walking and respond to antennal touch by repetitive tactile sampling of the object. Despite its relevance for spatial orientation, neither the spatial sampling patterns nor the kinematics of antennation behavior in insects are understood. Here we investigate unrestrained bilateral sampling movements during climbing of steps. The main objectives are: (1) How does the antennal contact pattern relate to particular object features? (2) How are the antennal joints coordinated during bilateral tactile sampling? We conducted motion capture experiments on freely climbing insects, using steps of different height. Tactile sampling was analyzed at the level of antennal joint angles. Moreover, we analyzed contact patterns on the surfaces of both the obstacle and the antenna itself. Before the first contact, both antennae move in a broad, mostly elliptical exploratory pattern. After touching the obstacle, the pattern switches to a narrower and faster movement, caused by higher cycle frequencies and lower cycle amplitudes in all joints. Contact events were divided into wall- and edge-contacts. Wall contacts occurred mostly with the distal third of the flagellum, which is flexible, whereas edge contacts often occurred proximally, where the flagellum is stiff. The movement of both antennae was found to be coordinated, exhibiting bilateral coupling of functionally analogous joints [e.g., left head-scape (HS) joint with right scape-pedicel (SP) joint] throughout tactile sampling. In comparison, bilateral coupling between homologous joints (e.g., both HS joints) was significantly weaker. Moreover, inter-joint coupling was significantly weaker during the contact episode than before. In summary, stick insects show contact-induced changes in frequency, amplitude and inter-joint coordination during tactile sampling of climbed obstacles.

Exploring the coding space of tactile localization in the antennal system of the stick insect

Exploring the coding space of tactile localization in the antennal system of the stick insect

Active tactile exploration for adaptive locomotion in the stick insect

Insects carry a pair of actively movable feelers that supply the animal with a range of multimodal information. The antennae of the stick insect Carausius morosus are straight and of nearly the same length as the legs, making them ideal probes for near-range exploration. Indeed, stick insects, like many other insects, use antennal contact information for the adaptive control of locomotion, for example, in climbing. Moreover, the active exploratory movement pattern of the antennae is context-dependent. The first objective of the present study is to reveal the significance of antennal contact information for the efficient initiation of climbing. This is done by means of kinematic analysis of freely walking animals as they undergo a tactually elicited transition from walking to climbing. The main findings are that fast, tactually elicited re-targeting movements may occur during an ongoing swing movement, and that the height of the last antennal contact prior to leg contact largely predicts the height of the first leg contact. The second objective is to understand the context-dependent adaptation of the antennal movement pattern in response to tactile contact. We show that the cycle frequency of both antennal joints increases after obstacle contact. Furthermore, inter-joint coupling switches distinctly upon tactile contact, revealing a simple mechanism for context-dependent adaptation.

Recruitment in starved nests: the role of direct and indirect interactions between scouts and nestmates in the ant Lasius niger

In social insects, the foraging activity usually increases with the length of food deprivation. In Lasius niger, a mass-recruiting ant species, the foraging adjustment to the level of food deprivation is regulated by the scout that fed at the food source and by the response of the nestmates to signals performed by the scout inside the nest. In this study, we look at the role of these direct interactions (antennations or trophallaxes) and indirect interactions (pheromonal emission) and how they are influenced by the level of food deprivation. At the beginning of recruitment, the relative number of nestmates leaving the nest to forage increases with the level of deprivation. The nestmates’ propensity to exit the nest is not influenced by a previous trophallactic and/or antennal contact with a scout. Our results strongly suggest that the exit of nestmates is triggered by a chemical signal emitted by a scout. Deprivation lowers the response threshold of nestmates to this chemical signal resulting in a more important exit from the nest. Surprisingly, 27% of starved nestmates that receive food from the scout relay the information by depositing a chemical signal before having discovered and drunk the food source. Both phenomena boost the recruitment process. Though successful foragers returning to the nest have a significant role in the recruitment to the food source, we observed that the response of the nestmates inside the nest also greatly influence regulation of the foraging activity.

Contact Sex Pheromones Identified for Two Species of Longhorned Beetles (Coleoptera: Cerambycidae)Tetropium fuscumandT. cinnamopterumin the Subfamily Spondylidinae

Male Tetropium fuscum (F.) and T. cinnamopterum Kirby mated with live and dead (freeze-killed) conspecific females upon antennal contact, but did not respond to dead females after cuticular waxes were removed by hexane rinsing. Significantly fewer males of each species attempted to copulate with live or dead heterospecific females than with conspecifics, indicating that mate recognition was mediated by species-specific contact sex pheromones in the female's cuticular hydrocarbons. GC/MS analysis of T. fuscum elytra identified n-alkanes and mono-methyl branched alkanes of which 11-methylheptacosane and 3- and 5-methyltricosanes were dominant in females. Full male responses, including copulatory behavior, were restored with application of enantiomerically pure synthetic (S)-11-methyl-heptacosane at 40 μg/female (one female equivalent) but not with racemic or (R)-11-methyl-heptacosane. The cuticular hydrocarbons on T. cinnamopterum elytra included 11-methyl-heptacosane as well as n-alkanes, methyl-branched alkanes, mono-alkenes, and (Z, Z)-6, 9-alkadienes. (Z)-9-pentacosene, (Z)-9-heptacosene, and 11-methyl-heptacosane were female dominant, but only (Z)-9-pentacosene elicited precopulatory behaviors in conspecific males at levels similar to those behaviors elicited by unrinsed females, but elicited copulation in fewer than half of males. At female equivalent dosages (10 μg), neither (Z)-9-heptacosene nor (S)-11-methyl- heptacosane elicited responses in males that were significantly different from those responses to a rinsed female but when applied together, the proportion of males responding was significantly increased. 11-methyl-heptacosene is thus a contact pheromone component common to both species, which may explain the heterospecific mating attempts by some males.

Neuronal organization of a fast‐mediating cephalothoracic pathway for antennal‐tactile information in the cricket (Gryllus bimaculatus DeGeer)

Crickets use their long antennae as tactile sensors. Confronted with obstacles, conspecifics, or predators, antennal contacts trigger short-latency motor responses. To reveal the neuronal pathway underlying these antennal-guided locomotory reactions we identified descending interneurons that rapidly transmit antennal-tactile information from the head to the thorax in the cricket Gryllus bimaculatus. Antennae were stimulated with forces approximating those of naturally occurring antennal contacts. Responding interneurons were individually identified by intracellular axon recordings in the pro-mesothoracic connective and subsequent tracer injection. Simultaneous with the intracellular recordings, the overall spike response in the neck connectives was recorded extracellularly to reveal the precise response-timing of each individual neuron within the collective multiunit response. Here we describe four descending brain neurons and two with the soma in the subesophageal ganglion. All antennal-touch elicited action potentials apparent in the neck connective recordings within 10 ms after antennal-contact are generated by these six interneurons. Their dendrites ramify in primary antennal-mechanosensory neuropils of the head ganglia. Each of them consistently generated action potentials in response to antennal touching and three of them responded also to different visual stimulation (light-off, movement). Their descending axons conduct action potentials with 3-5 m/s to the thoracic ganglia where they send off side branches in dorsal neuropils. Their physiological and anatomical properties qualify them as descending giant fibers in the cricket and suggest an involvement in evoking fast locomotory reactions. They form a fast-mediating cephalo-thoracic pathway for antennal-tactile information, whereas all other antennal-tactile interneurons had response latencies exceeding 40 ms.

The effect of individual variation on the structure and function of interaction networks in harvester ants.

Social insects exhibit coordinated behaviour without central control. Local interactions among individuals determine their behaviour and regulate the activity of the colony. Harvester ants are recruited for outside work, using networks of brief antennal contacts, in the nest chamber closest to the nest exit: the entrance chamber. Here, we combine empirical observations, image analysis and computer simulations to investigate the structure and function of the interaction network in the entrance chamber. Ant interactions were distributed heterogeneously in the chamber, with an interaction hot-spot at the entrance leading further into the nest. The distribution of the total interactions per ant followed a right-skewed distribution, indicating the presence of highly connected individuals. Numbers of ant encounters observed positively correlated with the duration of observation. Individuals varied in interaction frequency, even after accounting for the duration of observation. An ant's interaction frequency was explained by its path shape and location within the entrance chamber. Computer simulations demonstrate that variation among individuals in connectivity accelerates information flow to an extent equivalent to an increase in the total number of interactions. Individual variation in connectivity, arising from variation among ants in location and spatial behaviour, creates interaction centres, which may expedite information flow.

Mate Recognition and Sex Differences in Cuticular Hydrocarbons of the Diurnal Firefly Ellychnia corrusca (Coleoptera: Lampyridae)

Abstract There are several genera of diurnally active fireflies (Coleoptera: Lampyridae), and these adults generally do not produce bioluminescent signals. We investigated whether contact sex pheromones play a role in mate recognition in the diurnal firefly Ellychnia corrusca (L.). In laboratory behavioral assays, after antennal contact >70% of males attempted copulation with freeze-killed females, whereas no copulation attempts occurred when freeze-killed females had been washed with hexane. This shows that E. corrusca mate recognition relies on contact chemoreception and suggests that male mating responses are mediated by contact sex pheromones on the female cuticle. Using direct contact solid phase microextraction (SPME) and solvent extraction, we sampled cuticular hydrocarbons (CHCs) from both sexes of E. corrusca adults. Gas chromatography-mass spectrometry showed that SPME was more effective than solvent extraction in detecting CHCs (a two-fold increase in the number of compounds detected). Although E. corrusca males and females showed similar CHCs profiles, we documented several quantitative and qualitative differences between the sexes that may play a role in mate recognition. This report provides the first behavioral evidence for the existence of contact sex pheromones in any diurnal firefly.

Mating behaviour and evidence for sex‐specific pheromones in Hedypathes betulinus (Coleoptera: Cerambycidae: Lamiinae)

AbstractThe mating behaviour and evidence for sex‐specific pheromones of the main pest of green mate, Ilex paraguariensis, of the southern region of Brazil, Hedypathes betulinus (Klug, 1825) (Coleoptera: Cerambycidae: Lamiinae), were studied in the laboratory. The mating sequence of H. betulinus includes: female approaching the male, antennal contact, male mounting the female and start of copulation. This mating sequence provided support for our hypothesis that recognition of males by females may be mediated by a male‐produced pheromone and males recognize females by contact pheromones. The behavioural responses in an olfactometer of male and female H. betulinus to volatiles released by male and female conspecifics confirmed the presence of a male‐produced sex pheromone. This finding suggests that visual cues are not primary in eliciting a sexual response from females. Three male‐specific compounds were detected in the chromatographic analysis, providing chemical support to the behavioural data. Males did not respond to dead‐washed females but 70% of males attempted to mate with dead‐washed extract‐treated females, suggesting that extracts contained contact pheromones. Based on these results, a male‐produced sex pheromone and a female‐produced contact pheromone should be essential in the communication system of H. betulinus.

Visual detection of diminutive floral guides in the bumblebee Bombus terrestris and in the honeybee Apis mellifera

Many flowers display colour patterns comprising a large peripheral colour area that serves to attract flower visitors from some distance, and a small central, contrastingly coloured area made up by stamens or floral guides. In this study, we scaled down the size of floral guides to detect the minimal size bumblebees (Bombus terrestris) and honeybees (Apis mellifera) require for guidance. We analyzed the approach and the precise contact of the antennal tips with the floral guide of artificial flowers which precedes landing and inspection. Both bumblebees and honeybees were able to make antennal contact with circular floral guides which were 2 mm in diameter; bumblebees performed better than honeybees and antennated also at floral guides smaller than 2 mm. In discrimination experiments with bumblebees, a minimum floral guide size of 2 mm was required for discrimination between artificial flowers with and without floral guides. With increasing experience bumblebees targeted close to the site of reward instead of making antennal contact with the floral guide, whereas honeybees did not alter their initial behaviour with growing experience. Bumblebees and honeybees spontaneously target diminutive floral guides to achieve physical contact with flowers by means of their antennae which helps them to inspect flowers.

Evidence of Contact Pheromone Use in Mating Behavior of the Raspberry Weevil (Coleoptera: Curculionidae)

Numerous studies of insect species have shown that a subset of female cuticular hydrocarbons is used as short-range or contact pheromones. Here, we studied the possible use of contact pheromones in the mating behavior of the weevil Aegorhinus superciliosus, a native species of Chile. Males mounted females only after antennal contact with the female's cuticle, and only 33% of the males attempted to mate with dead females washed with solvent. When a glass rod (dummy) was coated with female cuticular extracts, males exhibited behaviors similar to those observed with females. A preliminary gas chromatography-mass spectrometry (GC-MS) analysis of cuticular extracts indicated that males and females share a series of aliphatic hydrocarbons but that the relative abundance of some of these compounds differ between the sexes. These results suggest that cuticular lipids mediate mating behavior of the raspberry weevil and provide the first evidence of contact pheromones in curculionids.

Distribution and Fine Structure of Antennal Sensilla in Emerald Ash Borer (Coleoptera: Buprestidae)

Abstract The antennal sensilla of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), were examined using scanning and transmission electron microscopy. Male and female antennae have a scape, pedicel, and nine flagellomeres. Both male and female antennae share five sensillum types: sensilla chaetica (mechanoreceptors), three types of sensilla basiconica (olfactory), and uniporous gustatory/taste sensilla. Apical depressions containing large sensory fields of uniporous sensilla were seen on the eight most distal flagellomeres of both sexes. Counts of sensillum types showed that males possessed significantly more uniporous sensilla than females. We hypothesize that antennal contact is important for mate recognition by male A. planipennis. The distal apices of the eight outer flagellomeres were seen to have “tufts” composed of two types of sensilla basiconica. A third type of sensilla basiconica was observed within the perimeter of the uniporous sensory fields. The structure and putative function of each sensillum type are discussed.

Mutual mate choice: when it pays both sexes to avoid inbreeding.

Theoretical models of sexual selection predict that both males and females of many species should benefit by selecting their mating partners. However, empirical evidence testing and validating this prediction is scarce. In particular, whereas inbreeding avoidance is expected to induce sexual conflicts, in some cases both partners could benefit by acting in concert and exerting mutual mate choice for non-assortative pairings. We tested this prediction with the gregarious cockroach Blattella germanica (L.). We demonstrated that males and females base their mate choice on different criteria and that choice occurs at different steps during the mating sequence. Males assess their relatedness to females through antennal contacts before deciding to court preferentially non-siblings. Conversely, females biased their choice towards the most vigorously courting males that happened to be non-siblings. This study is the first to demonstrate mutual mate choice leading to close inbreeding avoidance. The fact that outbred pairs were more fertile than inbred pairs strongly supports the adaptive value of this mating system, which includes no “best phenotype” as the quality of two mating partners is primarily linked to their relatedness. We discuss the implications of our results in the light of inbreeding conflict models.

Kin recognition via cuticular hydrocarbons shapes cockroach social life

Genetic relatedness plays a key role in the organization and the functioning of societies. A large diversity of species has developed kin recognition abilities, allowing individuals to discriminate conspecifics in relation to relatedness. In social insects, many studies showed that discrimination generally acts at the level of nestmateship and only few studies report kin recognition abilities. Our results highlight the importance of kin recognition in shaping social life in the urban cockroach Blattella germanica (L.) and present a complete description of the recognition system from expression to action components. Cockroaches of all developmental stages (nymphs and adults) discriminate siblings from nonsiblings independently of any prior social experience. Preference is context dependent so that siblings are preferred as social partners, whereas nonsiblings are preferred as mating partners. Discrimination is based on quantitative differences of cuticular hydrocarbons that are perceived through antennal contacts. As individual cuticular profiles remain stable over time, they constitute reliable discrimination cues correlated with relatedness. Our results offer interesting perspectives for the study of kin recognition and for the understanding of evolution toward sociality in insects.