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1.
J Biol Phys ; 50(2): 215-228, 2024 Jun.
Article in English | MEDLINE | ID: mdl-38727764

ABSTRACT

The detection of magnetic fields by animals is known as magnetoreception. The ferromagnetic hypothesis explains magnetoreception assuming that magnetic nanoparticles are used as magnetic field transducers. Magnetite nanoparticles in the abdomen of Apis mellifera honeybees have been proposed in the literature as the magnetic field transducer. However, studies with ants and stingless bees have shown that the whole body of the insect contain magnetic material, and that the largest magnetization is in the antennae. The aim of the present study is to investigate the magnetization of all the body parts of honeybees as has been done with ants and stingless bees. To do that, the head without antennae, antennae, thorax, and abdomen obtained from Apis mellifera honeybees were analyzed using magnetometry and Ferromagnetic Resonance (FMR) techniques. The magnetometry and FMR measurements show the presence of magnetic material in all honeybee body parts. Our results present evidence of the presence of biomineralized magnetite nanoparticles in the honeybee abdomen and, for the first time, magnetite in the antennae. FMR measurements permit to identify the magnetite in the abdomen as biomineralized. As behavioral experiments reported in the literature have shown that the abdomen is involved in magnetoreception, new experimental approaches must be done to confirm or discard the involvement of the antennae in magnetoreception.


Subject(s)
Abdomen , Arthropod Antennae , Animals , Bees/physiology , Arthropod Antennae/physiology , Ferrosoferric Oxide/chemistry , Ferrosoferric Oxide/metabolism , Magnetic Fields
2.
J Insect Sci ; 24(3)2024 May 01.
Article in English | MEDLINE | ID: mdl-38809687

ABSTRACT

Huanglongbing (HLB), a devastating citrus disease caused by Candidatus Liberibacter asiaticus, is efficiently vectored by the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae). Tamarixia radiata (Waterston) plays a crucial role as an ectoparasitoid, preying on D. citri nymphs. By collecting and identifying headspace volatiles from fifth instar nymphs of D. citri using a gas chromatograph-mass spectrometer (GC-MS), we obtained a collection of 9 volatile compounds. These compounds were subsequently chosen to investigate the electrophysiological and behavioral responses of female T. radiata. At a concentration of 10 µg/µl, 9 compounds were compared with cis-3-hexen-1-ol (control), resulting in trans-2-nonenal inducing the highest relative electroantennogram (EAG) value, followed by hexanal, heptanal, n-heptadecane, tetradecanal, n-tetradecane, n-pentadecane, 1-tetradecanol, and 1-dodecanol. The top 5 EAG responses of female T. radiata to these compounds were further investigated through EAG dose-response experiments. The results showed positive dose-responses as concentrations increased from 0.01 to 10 µg/µl. In Y-tube olfactometer bioassays, female T. radiata exhibited a preference for specific compounds. They were significantly attracted to tetradecanal at a concentration of 10 µg/µl and trans-2-nonenal at 0.01 µg/µl, while no significant attraction was observed toward hexanal, heptanal, or n-heptadecane. Our report is the first to demonstrate that volatiles produced by D. citri nymphs attract T. radiata, which suggests that this parasitoid may utilize nymph volatiles to locate its host.


Subject(s)
Hemiptera , Nymph , Volatile Organic Compounds , Animals , Nymph/growth & development , Nymph/physiology , Hemiptera/physiology , Female , Wasps/physiology , Electrophysiological Phenomena , Behavior, Animal/drug effects , Arthropod Antennae/physiology , Arthropod Antennae/drug effects
3.
Nat Commun ; 15(1): 2109, 2024 Mar 07.
Article in English | MEDLINE | ID: mdl-38453967

ABSTRACT

Insect antennae facilitate the nuanced detection of vibrations and deflections, and the non-contact perception of magnetic or chemical stimuli, capabilities not found in mammalian skin. Here, we report a neuromorphic antennal sensory system that emulates the structural, functional, and neuronal characteristics of ant antennae. Our system comprises electronic antennae sensor with three-dimensional flexible structures that detects tactile and magnetic stimuli. The integration of artificial synaptic devices adsorbed with solution-processable MoS2 nanoflakes enables synaptic processing of sensory information. By emulating the architecture of receptor-neuron pathway, our system realizes hardware-level, spatiotemporal perception of tactile contact, surface pattern, and magnetic field (detection limits: 1.3 mN, 50 µm, 9.4 mT). Vibrotactile-perception tasks involving profile and texture classifications were accomplished with high accuracy (> 90%), surpassing human performance in "blind" tactile explorations. Magneto-perception tasks including magnetic navigation and touchless interaction were successfully completed. Our work represents a milestone for neuromorphic sensory systems and biomimetic perceptual intelligence.


Subject(s)
Skin , Touch , Animals , Arthropod Antennae/physiology , Mammals , Neurons , Sense Organs , Touch/physiology
4.
Curr Biol ; 34(8): 1772-1779.e4, 2024 04 22.
Article in English | MEDLINE | ID: mdl-38479387

ABSTRACT

The honeybee waggle dance has been widely studied as a communication system, yet we know little about how nestmates assimilate the information needed to navigate toward the signaled resource. They are required to detect the dancer's orientation relative to gravity and duration of the waggle phase and translate this into a flight vector with a direction relative to the sun1 and distance from the hive.2,3 Moreover, they appear capable of doing so from varied, dynamically changing positions around the dancer. Using high-speed, high-resolution video, we have uncovered a previously unremarked correlation between antennal position and the relative body axes of dancer and follower bees. Combined with new information about antennal inputs4,5 and spatial encoding in the insect central complex,6,7 we show how a neural circuit first proposed to underlie path integration could be adapted to decoding the dance and acquiring the signaled information as a flight vector that can be followed to the resource. This provides the first plausible account of how the bee brain could support the interpretation of its dance language.


Subject(s)
Animal Communication , Arthropod Antennae , Animals , Bees/physiology , Arthropod Antennae/physiology , Flight, Animal/physiology
5.
Pest Manag Sci ; 80(7): 3603-3611, 2024 Jul.
Article in English | MEDLINE | ID: mdl-38458148

ABSTRACT

BACKGROUND: The Asian tiger mosquito, Aedes albopictus, is a competent vector for the spread of several viral arboviruses including dengue, chikungunya, and Zika. Several vital mosquito behaviors linked to survival and reproduction are primarily dependent on a sophisticated olfactory system for semiochemical perception. However, a limited number of studies has hampered our understanding of the relationship between the A. albopictus acute olfactory system and the complex chemical world. RESULTS: Here, we performed a qRT-PCR assay on antennae from A. albopictus of differing sex, age and physiological states, and found that AalbOr10 was enriched in blood-fed female mosquitoes. We then undertook single sensillum recording to de-orphan AalbOr10 using a panel of physiologically and behaviorally relevant odorants in a Drosophila 'empty neuron' system. The results indicated that AalbOr10 was activated by seven aromatic compounds, all of which hampered egg-laying in blood-fed mosquitoes. Furthermore, using a post-RNA interference oviposition assay, we found that reducing the transcript level of AalbOr10 affected repellent activity mediated by 2-ethylphenol at low concentrations (10-4 vol/vol). Computational modeling and molecular docking studies suggested that hydrogen bonds to Y68 and Y150 mediated the interaction of 2-ethylphenol with AalbOr10. CONCLUSION: We reveal a potential link between aromatics-induced oviposition repellency behaviors and a specific odorant receptor in A. albopictus. Our findings provide a foundation for identifying active semiochemicals for the monitoring or controlling of mosquito populations. © 2024 Society of Chemical Industry.


Subject(s)
Aedes , Insect Repellents , Oviposition , Receptors, Odorant , Animals , Aedes/drug effects , Aedes/genetics , Aedes/physiology , Receptors, Odorant/genetics , Receptors, Odorant/metabolism , Oviposition/drug effects , Female , Insect Repellents/pharmacology , Male , Insect Proteins/metabolism , Insect Proteins/genetics , Molecular Docking Simulation , Arthropod Antennae/drug effects , Arthropod Antennae/physiology
6.
J Econ Entomol ; 117(3): 793-799, 2024 Jun 10.
Article in English | MEDLINE | ID: mdl-38517276

ABSTRACT

Sex pheromone analogs have high structural similarity to sex pheromone components. They also play a role in studying many agricultural pests. In our study, (Z, Z, Z)-3,6,9-nonadecadiene (Z3Z6Z9-19:Hy) was successfully synthesized, which is an analogue to 1 of 2 sex pheromone components of Ectropis grisescens Warren (Z, Z, Z)-3,6,9-octadecatriene (Z3Z6Z9-18:Hy), and it showed potential inhibition in experiments. In the electroantennogram test, Z3Z6Z9-19:Hy showed a dose-dependent response, and only measured half the response of Z3Z9-6,7-epo-18:Hy. However, the compound significantly reduced positive response of E. grisescens males by up to 70% in the Y-tube olfactometer. Furthermore, in the wind tunnel, it significantly inhibited all types of behavioral responses. The percentage of moths contacting the pheromone odor source was reduced even at the lowest dose tested. In silico study afterward, molecular docking results showed affinity between Z3Z6Z9-19:Hy and sensory neuron membrane protein 1. Our study revealed the potential of Z3Z6Z9-19:Hy as a sex pheromone inhibitor, which would provide new tools for monitoring and mating disruption of E. grisescens.


Subject(s)
Arthropod Antennae , Moths , Sex Attractants , Animals , Sex Attractants/pharmacology , Moths/drug effects , Moths/physiology , Male , Arthropod Antennae/physiology , Arthropod Antennae/drug effects , Female , Alkadienes , Molecular Docking Simulation , Computer Simulation
7.
Arthropod Struct Dev ; 79: 101345, 2024 Mar.
Article in English | MEDLINE | ID: mdl-38493543

ABSTRACT

Aquatic insects represent a great portion of Arthropod diversity and the major fauna in inland waters. The sensory biology and neuroanatomy of these insects are, however, poorly investigated. This research aims to describe the antennal sensilla of nymphs of the stonefly Dinocras cephalotes using scanning electron microscopy and comparing them with the adult sensilla. Besides, central antennal pathways in nymphs and adults are investigated by neuron mass-tracing with tetramethylrhodamine, and their brain structures are visualized with an anti-synapsin antibody. No dramatic changes occur in the antennal sensilla during nymphal development, while antennal sensilla profoundly change from nymphs to adults when switching from an aquatic to an aerial lifestyle. However, similar brain structures are used in nymphs and adults to process diverging sensory information, perceived through different sensilla in water and air. These data provide valuable insights into the evolution of aquatic heterometabolous insects, maintaining a functional sensory system throughout development, including a distinct adaptation of the peripheral olfactory systems during the transition from detection of water-soluble chemicals to volatile compounds in the air. From a conservation biology perspective, the present data contribute to a better knowledge of the biology of stoneflies, which are very important bioindicators in rivers.


Subject(s)
Insecta , Sensilla , Animals , Sensilla/physiology , Microscopy, Electron, Scanning , Neoptera , Nymph/anatomy & histology , Water , Brain , Arthropod Antennae/physiology
8.
J Neurosci Methods ; 390: 109842, 2023 04 15.
Article in English | MEDLINE | ID: mdl-36965763

ABSTRACT

BACKGROUND: Electroantennography (EAG) is a basic neuroscientific tool that is widely used to measure olfactory responses in insects. It is particularly adapted to probing the olfactory systems of non-model insect species in chemical ecology and evolutionary biology. As currently practiced, EAG measures have varying degrees of correlation with olfactory responses, especially for insects whose olfactory sensory neurons (OSNs) are arranged in zones on the antennae. This limitation was shown to be partly due to the fact that only a single antennal position was recorded. NEW METHODS: We describe a setup using triple electroantennography (EAG3), whereby three antennal positions are recorded simultaneously. The spatial arrangement of the electrodes ensures the mechanical stability of the assembly. The EAG3 detector was coupled to a gas chromatograph (GC-EAD3), customized using a Dean's switch to improve the EAG signals by chopper modulation. EAG3 signals were analysed through a current point model to estimate olfactory responses across the antenna. RESULTS: Recordings were performed on Tephritidae and Drosophila species, which have antennae of different shapes and sizes. We confirmed that the spatio-temporal pattern of antennal activation was stimulus dependent and allowed us to quantify the antennal olfactory response. COMPARISONS WITH EXISTING METHOD: Compared to typical single-probe EAG, we show that EAG3 improves response quantification and increases the range of compounds for which a sensory response is detected. CONCLUSIONS: Our EAG3 setup is an original low-cost and easy-to-use method. It offers a useful bridge between comprehensive neurophysiological investigations and the broader themes explored in chemical ecology.


Subject(s)
Olfactory Receptor Neurons , Animals , Smell/physiology , Arthropod Antennae/physiology , Insecta/physiology , Drosophila
9.
Curr Biol ; 33(4): 780-789.e4, 2023 02 27.
Article in English | MEDLINE | ID: mdl-36731464

ABSTRACT

Insects use their antennae to smell odors,1,2 detect auditory cues,3,4 and sense mechanosensory stimuli such as wind5 and objects,6,7,8 frequently by combining sensory processing with active movements. Genetic access to antennal motor systems would therefore provide a powerful tool for dissecting the circuit mechanisms underlying active sensing, but little is known about how the most genetically tractable insect, Drosophila melanogaster, moves its antennae. Here, we use deep learning to measure how tethered Drosophila move their antennae in the presence of sensory stimuli and identify genetic reagents for controlling antennal movement. We find that flies perform both slow adaptive movements and fast flicking movements in response to wind-induced deflections, but not the attractive odor apple cider vinegar. Next, we describe four muscles in the first antennal segment that control antennal movements and identify genetic driver lines that provide access to two groups of antennal motor neurons and an antennal muscle. Through optogenetic inactivation, we provide evidence that antennal motor neurons contribute to active movements with different time courses. Finally, we show that activation of antennal motor neurons and muscles can adjust the gain and acuity of wind direction encoding by antennal displacement. Together, our experiments provide insight into the neural control of antennal movement and suggest that active antennal positioning in Drosophila may tune the precision of wind encoding.


Subject(s)
Drosophila melanogaster , Drosophila , Animals , Drosophila melanogaster/genetics , Wind , Arthropod Antennae/physiology , Sensation
10.
Article in English | MEDLINE | ID: mdl-35986777

ABSTRACT

Overall body proportions and relative limb length are highly characteristic for most insect taxa. In case of the legs, limb length has mostly been discussed with regard to parameters of locomotor performance and, in particular cases, as an adaptation to environmental factors or to the mating system. Here, we compare three species of stick and leaf insects (Phasmatodea) that differ strongly in the length ratio between antennae and walking legs, with the antennae of Medauroidea extradentata being much shorter than its legs, nearly equal length of antennae and legs in Carausius morosus, and considerably longer antennae than front legs in Aretaon asperrimus. We show that that relative limb length is directly related to the near-range exploration effort, with complementary function of the antennae and front legs irrespective of their length ratio. Assuming that these inter-species differences hold for both sexes and all developmental stages, we further explore how relative limb length differs between sexes and how it changes throughout postembryonic development. We show that the pattern of limb-to-body proportions is species-characteristic despite sexual dimorphism, and find that the change in sexual dimorphism is strongest during the last two moults. Finally, we show that antennal growth rate is consistently higher than that of front legs, but differs categorically between the species investigated. Whereas antennal growth rate is constant in Carausius, the antennae grow exponentially in Medauroidea and with a sudden boost during the last moult in Aretaon.


Subject(s)
Arthropod Antennae , Extremities , Neoptera , Spatial Behavior , Neoptera/anatomy & histology , Neoptera/physiology , Animals , Arthropod Antennae/anatomy & histology , Arthropod Antennae/physiology , Extremities/anatomy & histology , Extremities/physiology , Movement , Sex Characteristics , Male , Female
11.
Nature ; 611(7937): 754-761, 2022 11.
Article in English | MEDLINE | ID: mdl-36352224

ABSTRACT

Odour plumes in the wild are spatially complex and rapidly fluctuating structures carried by turbulent airflows1-4. To successfully navigate plumes in search of food and mates, insects must extract and integrate multiple features of the odour signal, including odour identity5, intensity6 and timing6-12. Effective navigation requires balancing these multiple streams of olfactory information and integrating them with other sensory inputs, including mechanosensory and visual cues9,12,13. Studies dating back a century have indicated that, of these many sensory inputs, the wind provides the main directional cue in turbulent plumes, leading to the longstanding model of insect odour navigation as odour-elicited upwind motion6,8-12,14,15. Here we show that Drosophila melanogaster shape their navigational decisions using an additional directional cue-the direction of motion of odours-which they detect using temporal correlations in the odour signal between their two antennae. Using a high-resolution virtual-reality paradigm to deliver spatiotemporally complex fictive odours to freely walking flies, we demonstrate that such odour-direction sensing involves algorithms analogous to those in visual-direction sensing16. Combining simulations, theory and experiments, we show that odour motion contains valuable directional information that is absent from the airflow alone, and that both Drosophila and virtual agents are aided by that information in navigating naturalistic plumes. The generality of our findings suggests that odour-direction sensing may exist throughout the animal kingdom and could improve olfactory robot navigation in uncertain environments.


Subject(s)
Drosophila melanogaster , Motion Perception , Odorants , Olfactory Perception , Spatial Navigation , Wind , Animals , Drosophila melanogaster/anatomy & histology , Drosophila melanogaster/physiology , Odorants/analysis , Spatial Navigation/physiology , Motion Perception/physiology , Time Factors , Olfactory Perception/physiology , Arthropod Antennae/physiology , Cues , Walking/physiology
12.
Acta Biomater ; 147: 102-119, 2022 07 15.
Article in English | MEDLINE | ID: mdl-35649508

ABSTRACT

Insect antennae are hollow, blood-filled fibers with complex shape. Muscles in the two basal segments control antennal movement, but the rest (flagellum) is muscle-free. The insect can controllably flex, twist, and maneuver its antennae laterally. To explain this behavior, we performed a comparative study of structural and tensile properties of the antennae of Periplaneta americana (American cockroach), Manduca sexta (Carolina hawkmoth), and Vanessa cardui (painted lady butterfly). These antennae demonstrate a range of distinguishable tensile properties, responding either as brittle or strain-adaptive fibers that stiffen when stretched. Scanning electron microscopy and high-speed imaging of antennal breakup during stretching revealed complex coupling of blood pressure and cuticle deformation in antennae. A generalized Lamé theory of solid mechanics was developed to include the force-driven deformation of blood-filled antennal tubes. We validated the theory against experiments with artificial antennae with no adjustable parameters. Blood pressure increased when the insect inflated its antennae or decreased below ambient pressure when an external tensile load was applied to the antenna. The pressure-cuticle coupling can be controlled through changes of the blood volume in the antennal lumen. In insects that do not fill the antennal lumen with blood, this blood pressure control is lacking, and the antennae react only by muscular activation. We suggest that the principles we have discovered for insect antennae apply to other appendages that share a leg-derived ancestry. Our work offers promising new applications for multifunctional fiber-based microfluidics that could transport fluids and be manipulated by the same fluid on demand. STATEMENT OF SIGNIFICANCE: Insect antennae are blood-filled, segmented fibers with muscles in the two basal segments. The long terminal segment is muscle-free but can be flexed. To explain this behavior, we examined structure-function relationships of antennae of cockroaches, hawkmoths, and butterflies. Hawkmoth antennae behaved as brittle fibers, but butterfly and cockroach antennae showed strain-adaptive behavior like fibers that stiffen when stretched. Videomicroscopy of antennal breakup during stretching revealed complex coupling of blood pressure and cuticle deformation. Our solid mechanics model explains this behavior. Because antennae are leg-derived appendages, we suggest that the principles we found apply to other appendages of leg-derived ancestry. Our work offers new applications for multifunctional fiber-based microfluidics that could transport fluids and be manipulated by the fluid on demand.


Subject(s)
Butterflies , Periplaneta , Animals , Arthropod Antennae/physiology , Blood Pressure , Humans , Insecta , Movement , Periplaneta/physiology
13.
J Exp Biol ; 225(4)2022 02 15.
Article in English | MEDLINE | ID: mdl-35072207

ABSTRACT

Animals perceive their surroundings using various modalities of sensory inputs to guide their locomotion. Nocturnal insects such as crickets use mechanosensory inputs mediated by their antennae to orient in darkness. Spatial information is acquired via voluntary antennal contacts with surrounding objects, but it remains unclear whether the insects modulate behaviors mediated by other sensory organs based on that information. Crickets exhibit escape behavior in response to a short air puff, which is detected by the abdominal mechanosensory organs called cerci and is perceived as a 'predator approach' signal. We placed objects of different shapes at different locations with which the cricket actively made contact using its antennae. We then examined the effects on wind-elicited escape behavior. The crickets changed their movement trajectory in response to nearby objects such as walls so that they could avoid collision with these obstacles even during the cercal-mediated behavior. For instance, when a wall was placed in front of the crickets so that it was detected by one antenna, the escape trajectory in response to a stimulus from behind was significantly biased toward the side opposite the wall. Even when the antenna on the free side without the wall was ablated, this collision avoidance was also observed, suggesting that the mechanosensory inputs from one antennae detecting an object edge would be sufficient to perceive the location of obstacle in front. This study demonstrated that crickets were able to use the spatial information acquired with their antennal system to modify their behavior mediated by other sensory organs.


Subject(s)
Gryllidae , Animals , Arthropod Antennae/physiology , Gryllidae/physiology , Locomotion , Perception , Wind
14.
PLoS Comput Biol ; 17(12): e1009583, 2021 12.
Article in English | MEDLINE | ID: mdl-34898600

ABSTRACT

When flies explore their environment, they encounter odors in complex, highly intermittent plumes. To navigate a plume and, for example, find food, they must solve several challenges, including reliably identifying mixtures of odorants and their intensities, and discriminating odorant mixtures emanating from a single source from odorants emitted from separate sources and just mixing in the air. Lateral inhibition in the antennal lobe is commonly understood to help solving these challenges. With a computational model of the Drosophila olfactory system, we analyze the utility of an alternative mechanism for solving them: Non-synaptic ("ephaptic") interactions (NSIs) between olfactory receptor neurons that are stereotypically co-housed in the same sensilla. We find that NSIs improve mixture ratio detection and plume structure sensing and do so more efficiently than the traditionally considered mechanism of lateral inhibition in the antennal lobe. The best performance is achieved when both mechanisms work in synergy. However, we also found that NSIs decrease the dynamic range of co-housed ORNs, especially when they have similar sensitivity to an odorant. These results shed light, from a functional perspective, on the role of NSIs, which are normally avoided between neurons, for instance by myelination.


Subject(s)
Odorants , Olfactory Receptor Neurons/physiology , Smell/physiology , Animals , Arthropod Antennae/physiology , Biophysics , Computational Biology , Drosophila/physiology , Female , Male , Models, Biological , Models, Theoretical , Myelin Sheath/metabolism , Recognition, Psychology , Sense Organs/physiology
15.
Cell Rep ; 37(13): 110165, 2021 12 28.
Article in English | MEDLINE | ID: mdl-34965425

ABSTRACT

Ongoing neural activity has been observed across several brain regions and is thought to reflect the internal state of the brain. Yet, it is important to understand how ongoing neural activity interacts with sensory experience and shapes sensory representations. Here, we show that the projection neurons of the fruit fly antennal lobe exhibit spatiotemporally organized ongoing activity. After repeated exposure to odors, we observe a gradual and cumulative decrease in the amplitude and number of calcium events occurring in the absence of odor stimulation, as well as a reorganization of correlations between olfactory glomeruli. Accompanying these plastic changes, we find that repeated odor experience decreases trial-to-trial variability and enhances the specificity of odor representations. Our results reveal an odor-experience-dependent modulation of ongoing and sensory-evoked activity at peripheral levels of the fruit fly olfactory system.


Subject(s)
Arthropod Antennae/physiology , Drosophila melanogaster/physiology , Interneurons/physiology , Neuronal Plasticity , Odorants/analysis , Olfactory Bulb/physiology , Smell , Animals , Arthropod Antennae/drug effects , Calcium/metabolism , Drosophila melanogaster/drug effects , Female , Interneurons/drug effects , Olfactory Bulb/drug effects , Olfactory Pathways
16.
Elife ; 102021 11 25.
Article in English | MEDLINE | ID: mdl-34822323

ABSTRACT

Most animals survive and thrive due to navigational behavior to reach their destinations. In order to navigate, it is important for animals to integrate information obtained from multisensory inputs and use that information to modulate their behavior. In this study, by using a virtual reality (VR) system for an insect, we investigated how the adult silkmoth integrates visual and wind direction information during female search behavior (olfactory behavior). According to the behavioral experiments using a VR system, the silkmoth had the highest navigational success rate when odor, vision, and wind information were correctly provided. However, the success rate of the search was reduced if the wind direction information provided was different from the direction actually detected. This indicates that it is important to acquire not only odor information but also wind direction information correctly. When the wind is received from the same direction as the odor, the silkmoth takes positive behavior; if the odor is detected but the wind direction is not in the same direction as the odor, the silkmoth behaves more carefully. This corresponds to a modulation of behavior according to the degree of complexity (turbulence) of the environment. We mathematically modeled the modulation of behavior using multisensory information and evaluated it using simulations. The mathematical model not only succeeded in reproducing the actual silkmoth search behavior but also improved the search success relative to the conventional odor-source search algorithm.


Subject(s)
Bombyx/physiology , Olfactory Perception , Orientation , Spatial Navigation , Virtual Reality , Animals , Arthropod Antennae/physiology , Male , Odorants , Pheromones , Visual Perception , Wind
17.
Sci Rep ; 11(1): 20883, 2021 10 22.
Article in English | MEDLINE | ID: mdl-34686710

ABSTRACT

Olfaction is a crucial sensory modality underlying foraging, social and mating behaviors in many insects. Since the olfactory system is at the interface between the animal and its environment, it receives strong evolutionary pressures that promote neuronal adaptations and phenotypic variations across species. Hornets are large eusocial predatory wasps with a highly developed olfactory system, critical for foraging and intra-specific communication. In their natural range, hornet species display contrasting ecologies and olfactory-based behaviors, which might match to adaptive shifts in their olfactory system. The first olfactory processing center of the insect brain, the antennal lobe, is made of morphological and functional units called glomeruli. Using fluorescent staining, confocal microscopy and 3D reconstructions, we compared antennal lobe structure, glomerular numbers and volumes in four hornet species (Vespa crabro, Vespa velutina, Vespa mandarinia and Vespa orientalis) with marked differences in nesting site preferences and predatory behaviors. Despite a conserved organization of their antennal lobe compartments, glomeruli numbers varied strongly between species, including in a subsystem thought to process intraspecific cuticular signals. Moreover, specific adaptations involving enlarged glomeruli appeared in two species, V. crabro and V. mandarinia, but not in the others. We discuss the possible function of these adaptations based on species-specific behavioral differences.


Subject(s)
Arthropod Antennae/physiology , Bees/physiology , Wasps/physiology , Animals , Brain/physiology , Olfactory Receptor Neurons/physiology , Species Specificity
18.
Sci Rep ; 11(1): 16702, 2021 08 17.
Article in English | MEDLINE | ID: mdl-34404861

ABSTRACT

Members of numerous animal species show consistent inter-individual differences in behaviours, but the forces generating animal "personality" or individuality remain unclear. We show that experiences gathered solely from social conflict can establish consistent differences in the decision of male crickets to approach or avoid a stimulus directed at one antenna. Adults isolated for 48 h from a colony already exhibit behavioural differences. Prior to staging a single dyadic contest, prospective winners approached the stimulus whereas prospective losers turned away, as they did also after fighting. In contrast, adults raised as nymphs with adult males present but isolated from them as last instar nymphs, all showed avoidance. Furthermore, adults raised without prior adult contact, showed no preferred directional response. However, following a single fight, winners from both these groups showed approach and losers avoidance, but this difference lasted only one day. In contrast, after 6 successive wins or defeats, the different directional responses of multiple winners and losers remained consistent for at least 6 days. Correlation analysis revealed examples of consistent inter-individual differences in the direction and magnitude of turning responses, which also correlated with individual aggressiveness and motility. Together our data reveal that social subjugation, or lack thereof, during post-embryonic and early adult development forges individuality and supports the notion of a proactive-reactive syndrome in crickets.


Subject(s)
Gryllidae , Aggression , Animals , Arthropod Antennae/physiology , Behavior, Animal , Gryllidae/physiology , Male , Social Behavior
19.
Molecules ; 26(15)2021 Jul 21.
Article in English | MEDLINE | ID: mdl-34361547

ABSTRACT

Essential oils of aromatic plants represent an alternative to classical pest control with synthetic chemicals. They are especially promising for the alternative control of stored product pest insects. Here, we tested behavioral and electrophysiological responses of the stored product pest Tribolium confusum, to the essential oil of a Brazilian indigenous plant, Varronia globosa, collected in the Caatinga ecosystem. We analyzed the essential oil by GC-MS, tested the effects of the entire oil and its major components on the behavior of individual beetles in a four-way olfactometer, and investigated responses to these stimuli in electroantennogram recordings (EAG). We could identify 25 constituents in the essential oil of V. globosa, with anethole, caryophyllene and spathulenole as main components. The oil and its main component anethole had repellent effects already at low doses, whereas caryophyllene had only a repellent effect at a high dose. In addition, the essential oil abolished the attractive effect of the T. confusum aggregation pheromone. EAG recordings revealed dose-dependent responses to the individual components and increasing responses to the blend and even more to the entire oil. Our study reveals the potential of anethole and the essential oil of V. globosa in the management of stored product pests.


Subject(s)
Arthropod Antennae/physiology , Behavior, Animal/drug effects , Insect Repellents , Magnoliopsida/chemistry , Oils, Volatile , Tribolium/physiology , Animals , Insect Repellents/chemistry , Insect Repellents/pharmacology , Oils, Volatile/chemistry , Oils, Volatile/pharmacology
20.
J Neurophysiol ; 126(2): 398-412, 2021 08 01.
Article in English | MEDLINE | ID: mdl-34161139

ABSTRACT

In insects the tactile sense is important for near-range orientation and is involved in various behaviors. Nocturnal insects, such as the stick insect Carausius morosus, continuously explore their surroundings by actively moving their antennae when walking. Upon antennal contact with objects, stick insects show a targeted front-leg movement. As this reaction occurs within 40 ms, descending transfer of information from the brain to the thorax needs to be fast. So far, a number of descending interneurons have been described that may be involved in this reach-to-grasp behavior. One of these is the contralateral ON-type velocity-sensitive neuron (cONv). cONv was found to encode antennal joint-angle velocity during passive movement. Here, we characterize the transient response properties of cONv, including its dependence on joint angle range and direction. As antennal hair field afferent terminals were shown to arborize close to cONv dendrites, we test whether antennal hair fields contribute to the joint-angle velocity encoding of cONv. To do so, we conducted bilateral extracellular recordings of both cONv interneurons per animal before and after hair field ablations. Our results show that cONv responses are highly transient, with velocity-dependent differences in delay and response magnitude. As yet, the steady state activity level was maintained until the stop of antennal movement, irrespective of movement velocity. Hair field ablation caused a moderate but significant reduction of movement-induced cONv firing rate by up to 40%. We conclude that antennal proprioceptive hair fields contribute to the velocity-tuning of cONv, though further antennal mechanoreceptors must be involved, too.NEW & NOTEWORTHY Active tactile exploration and tactually induced behaviors are important for many animals. They require descending information transfer about tactile sensor movement to thoracic networks. Here, we investigate response properties and afferent input to the identified descending interneuron cONv in stick insects. cONv may be involved in tactually induced reach-to-grasp movements. We show that cONv response delay, transient and steady state are velocity-dependent and that antennal proprioceptive hair fields contribute to the velocity encoding of cONv.


Subject(s)
Arthropod Antennae/physiology , Interneurons/physiology , Sensory Receptor Cells/physiology , Animals , Arthropod Antennae/cytology , Arthropod Antennae/innervation , Ganglia, Invertebrate/cytology , Ganglia, Invertebrate/physiology , Insecta , Movement , Touch , Touch Perception
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