Airborne Chemical Cues Research Articles

Males respond to substrate-borne, not airborne, female chemical cues in the jumping spider, Habronattus pyrrithrix (Araneae: Salticidae)

Jumping spiders are known for complex courtship displays with both visual and vibratory components, but increasing evidence shows they also use chemoreception in intraspecific communication. We conducted two experiments using Habronattus pyrrithrix (Chamberlin, 1924) to assess male response to substrate-borne or airborne chemical cues produced by virgin females. First, we tested the effect of substrate-borne cues by allowing males to inspect two pieces of filter paper that had either been exposed to a female (thus covered in silk and/or excreta) or not (control). Second, we used a Y-tube olfactometer to test male response to female airborne cues versus a no-odor control in the absence of substrate-borne cues. Males responded to substrate-borne cues (spending more time traversing and palpating female-treated filter paper compared with the control) but did not respond to airborne cues alone. Together, these experiments suggest male H. pyrrithrix may use contact chemical cues from female silk to locate or assess females.

Conspecific odor cues induce different vocal responses in serrate-legged small treefrogs, but only in the absence of acoustic signals

BackgroundSignal detection is crucial to survival and successful reproduction, and animals often modify behavioral decisions based on information they obtained from the social context. Undeniably, the decision-making in male-male competition and female choice of anurans (frogs and toads) depends heavily on acoustic signals. However, increasing empirical evidence suggests that additional or alternative types of cue (e.g., visual, chemical, and vibratory) can be used to detect, discriminate and locate conspecifics in many anuran species. Nevertheless, few studies have investigated whether conspecific odor cues affect male’s calling behavior. In this study, we conducted an experiment to investigate whether and how different chemical cues (male odors, female odors, and stress odors) from conspecifics affect male’s calling strategies in serrate-legged small treefrogs (Kurixalus odontotarsus), and whether the combined chemical and acoustic stimuli have additive effects on calling behavior or not.ResultsWe found that compared with female odors, male K. odontotarsus reduced calling investment in response to male odors or stress odors, in the absence of rival’s advertisement calls. When odor stimuli and advertisement calls were presented simultaneously, however, there were no differences in the vocal response of focal males among odor groups.ConclusionsThese results provide evidence that male treefrogs switch calling investment according to different odor cues from conspecifics, and further demonstrate that calling behavior can be affected by chemical cues in anuran species. Our study highlights the potential role of airborne chemical cues in sex identification and contributes to increase our understanding of anuran communication.

Smelling in the dark: Phylogenomic insights into the chemosensory system of a subterranean beetle.

The chemosensory system has experienced relevant changes in subterranean animals, facilitating the perception of specific chemical signals critical to survival in their particular environment. However, the genomic basis of chemoreception in cave-dwelling fauna has been largely unexplored. We generated de novo transcriptomes for antennae and body samples of the troglobitic beetle Speonomus longicornis (whose characters suggest an extreme adaptation to a deep subterranean environment) in order to investigate the evolutionary origin and diversification of the chemosensory gene repertoire across coleopterans through a phylogenomic approach. Our results suggested a diminished diversity of odourant and gustatory gene repertoires compared to polyphagous beetles that inhabit surface habitats. Moreover, S.longicornis showed a large diversity of odourant-binding proteins, suggesting an important role of these proteins in capturing airborne chemical cues. We identified a gene duplication of the ionotropic coreceptor IR25a, a highly conserved single-copy gene in protostomes involved in thermal and humidity sensing. In addition, no homologous genes to sugar receptors or the ionotropic receptor IR41a were detected. Our findings suggest that the chemosensory gene repertoire of this cave beetle may result from adaptation to the highly specific ecological niche it occupies, and that gene duplication and loss may have played an important role in the evolution of gene families involved in chemoreception. Altogether, our results shed light on the genomic basis of chemoreception in a cave-dwelling invertebrate and pave the road towards understanding the genomic underpinnings of adaptation to the subterranean lifestyle at a deeper level.

Olfaction at depth: Cribriform plate size declines with dive depth and duration in aquatic arctoid carnivorans.

It is widely accepted that obligate aquatic mammals, specifically toothed whales, rely relatively little on olfaction. There is less agreement about the importance of smell among aquatic mammals with residual ties to land, such as pinnipeds and sea otters. Field observations of marine carnivorans stress their keen use of smell while on land or pack ice. Yet, one dimension of olfactory ecology is often overlooked: while underwater, aquatic carnivorans forage “noseblind,” diving with nares closed, removed from airborne chemical cues. For this reason, we predicted marine carnivorans would have reduced olfactory anatomy relative to closely related terrestrial carnivorans. Moreover, because species that dive deeper and longer forage farther removed from surface scent cues, we predicted further reductions in their olfactory anatomy. To test these hypotheses, we looked to the cribriform plate (CP), a perforated bone in the posterior nasal chamber of mammals that serves as the only passageway for olfactory nerves crossing from the periphery to the olfactory bulb and thus covaries in size with relative olfactory innervation. Using CT scans and digital quantification, we compared CP morphology across Arctoidea, a clade at the interface of terrestrial and aquatic ecologies. We found that aquatic carnivoran species from two lineages that independently reinvaded marine environments (Pinnipedia and Mustelidae), have significantly reduced relative CP than terrestrial species. Furthermore, within these aquatic lineages, diving depth and duration were strongly correlated with CP loss, and the most extreme divers, elephant seals, displayed the greatest reductions. These observations suggest that CP reduction in carnivorans is an adaptive response to shifting selection pressures during secondary invasion of marine environments, particularly to foraging at great depths. Because the CP is fairly well preserved in the fossil record, using methods presented here to quantify CP morphology in extinct species could further clarify evolutionary patterns of olfactory loss across aquatic mammal lineages that have independently committed to life in water.

Antennal Lobe Atlas of an Emerging Corn Pest, Athetis dissimilis.

Moths develop sophisticated olfactory systems to sense the airborne chemical cues from the environment. Understanding the structural basis in the neuronal center is a fundamental neuroethological step. Little is known about the emerging crop pest Athetis dissimilis with regard to its morphology or its neuronal organizations. Through antibody staining and digital 3D modeling, we re-constructed the primary olfactory center—the antennal lobe of A. dissimilis. In the antennal lobes 68.8 ± 3.1 male glomeruli and 70.8 ± 1.0 female glomeruli were identified with obvious sexual dimorphism. In particular, male adults of A. dissimilis contain a macroglomerular complex (MGC) that consists of three subunits, while the female lobe has four relatively enlarged glomeruli at the entrance of the antennal nerve. Glomeruli were later clustered with deviation and variance, and referring to reported olfactory related receptor family genes in seven different moth species, we found that glomerular counts of these insects are better related to the sum of odorant receptor and ionotropic receptor numbers, suggesting olfactory receptors and ionotropic receptors may both involved in olfaction of Noctuidae moths.

Balearic lizards use chemical cues from a complex deceptive mimicry to capture attracted pollinators

AbstractDeceptive flowers from several plant species emit odors that mimic oviposition cues and attract female insects seeking for a laying site. Helicodiceros muscivorus is a species that emits an odor mimicking the foul smell of rotting meat and thereby attracts blowflies that usually oviposit on carcasses but are deceived into pollinating the plant. Thus, H. muscivorus is a striking case of pollination by brood‐site deception. The Balearic lizard, Podarcis lilfordi, exhibits remarkable interactions with dead horse arum. Balearic lizards, which sometimes forage on carcasses, are attracted to blooming dead horse arum. We showed experimentally that P. lilfordi can detect chemical cues from carcasses on cotton swabs and exhibits elevated tongue‐flick rates to carcass chemical cues compared to control stimuli. Lizards also detected and located hidden carcasses using only airborne chemical cues. The responses of lizards to chemical cues from the spadix of blooming dead horse arum were qualitatively and quantitatively similar to those to carcass odors. Therefore, the decay‐like odor that attracts blowflies for the plant's benefit also attracts lizards. This attraction may initially have been somewhat favorable for lizards that eat blowflies, but slightly unfavorable for plants because the lizards ate some pollinators. We suggest that lizards attracted by odor may have learned later to use the plant for thermoregulation and then consume its fruits, making the association more positive for lizards and benefitted arum by seed dispersal.

Airborne Chemical Information and Context-Dependent Post-Strike Foraging Behavior in Pacific Rattlesnakes (Crotalus oreganus)

Predators demonstrate context-dependent foraging behaviors to dynamically and successfully track prey and can use multiple cues in this process. In squamate reptiles (snakes and lizards), chemical signals from prey significantly influence predatory behavior, especially substrate and airborne cues. In this study, we examined behavioral variation in rattlesnakes (Crotalus oreganus) during strike-induced chemosensory searching (SICS), a sterotyped complex of behaviors seen in squamates. Rattlesnakes can use both substrate and airborne chemical cues during SICS, but we sought to determine the changes during SICS when either substrate, airborne, or air-deposited chemical cues were the only types available to snakes in a Y-maze. We hypothesize that these cues represent the spectrum of chemical information available in the natural environment. We also modified scoring of choice in the Y-maze by deriving a choice penalty score, a reflection of how extensively the snake explored the unscented arm of the maze. In t...

Possible environmental chemical cues affecting behaviour of the mangrove gastropod Cerithidea decollata

The Indo-West Pacific mangrove gastropod Cerithidea decollata feeds on the ground at low tide and climbs the trees (Avicennia marina) two hours before the arrival of water, settling well above the level that the incoming tide will reach at high tide (from 0 to 80 cm, depending on the tidal phase). In addition, it has been shown that these snails climb twice as high when translocated to lower shore sites (dominated by Rhizophora mucronata), where C. decollata is missing and the high water can reach 1.6 m instead of about 80 cm as within the snail home environment. The study assesses the possible role of chemical cues in the afore-mentioned behaviours. The hypothesis that snails may foresee the periodical tide level variation thanks to airborne chemical cues, possibly released by trees or sediments, has been rejected. On the other hand, airborne chemical cues released by R. mucronata may play a role in inducing snails translocated to low shore sites to climb much higher than control, allowing them to avoid submersion.

Is love in the air or at first sight? Mate finding cues used by sympatric male velvet ants (Hymenoptera: Mutillidae)

AbstractMate finding has been examined in a wide range of hymenopteran families, with the greatest knowledge from social species and parasitoids used in pest management. Velvet ants (Hymenoptera: Mutillidae) provide a unique system to study mate finding because short‐lived flying males must find solitary, wingless females that have spatially and temporally dispersed emergence. Based on limited field observations, it is thought that male velvet ants may use visual, chemical, and vibratory cues for mate finding, though there have been no controlled experiments to test these hypotheses. Using choice experiments, this study aims to determine the role of visual and airborne chemical cues used in female detection by three sympatric species of Dasymutilla males. We find that visual cues are not used for initial female detection and that airborne chemicals are sufficient for female detection. We also discover that males readily approach females of different species, indicating airborne chemicals are not used for species recognition. Despite the lack of discrimination by males, we determined that the sympatric, morphologically similar species show no genetic introgression, and therefore some other isolating mechanism must be at play after males make initial contact with the females.

Controlling airborne cues to study small animal navigation

Small animals such as nematodes and insects analyze airborne chemical cues to infer the direction of favorable and noxious locations. In these animals, the study of navigational behavior evoked by airborne cues has been limited by the difficulty of precisely controlling stimuli. We present a system that can be used to deliver gaseous stimuli in defined spatial and temporal patterns to freely moving small animals. We used this apparatus, in combination with machine-vision algorithms, to assess and quantify navigational decision making of Drosophila melanogaster larvae in response to ethyl acetate (a volatile attractant) and carbon dioxide (a gaseous repellant).

Involvement of Gαolf‐expressing neurons in the vomeronasal system of Bufo japonicus

Most terrestrial vertebrates possess anatomically distinct olfactory organs: the olfactory epithelium (OE) and the vomeronasal organ (VNO). In rodents, olfactory receptors coupled to Gα(olf) are expressed in the OE, whereas vomeronasal receptors type 1 (V1R) and vomeronasal receptors type 2 (V2R), coupled to Gα(i2) and Gα(o) , respectively, are expressed in the VNO. These receptors and G proteins are thought to play important roles in olfactory perception. However, we previously reported that only V2R and Gα(o) expression is detected in the Xenopus laevis VNO. As X. laevis spends its entire life in water, we considered that expression of limited types of chemosensory machinery in the VNO might be due to adaptation of the VNO to aquatic life. Thus, we analyzed the expression of G proteins in the VNO and the accessory olfactory bulb (AOB) of the adult Japanese toad, Bufo japonicus, because this species is well adapted to a terrestrial life. By using immunohistochemical analysis in combination with in situ hybridization and DiI labeling, we found that B. japonicus Gα(olf) and Gα(o) were expressed in the apical and middle-to-basal layer of the vomeronasal neuroepithelium, and that the axons of these Gα(olf) - and Gα(o) -expressing vomeronasal neurons projected to the rostral and caudal accessory olfactory bulb, respectively. These results strongly suggest that both the Gα(olf) - and Gα(o) -mediated signal transduction pathways function in the B. japonicus VNO. The expression of Gα(olf) in the B. japonicus VNO may correlate with the detection of airborne chemical cues and with a terrestrial life.

Perception of airborne odors by loggerhead sea turtles

Sea turtles are known to detect chemical cues, but in contrast to most marine animals, turtles surface to breathe and thus potentially have access to olfactory cues both in air and in water. To determine whether sea turtles can detect airborne chemical cues, captive loggerhead turtles (Caretta caretta) were placed into a circular, water-filled arena in which odorants could be introduced to the air above the water surface. Air that had passed across the surface of a cup containing food elicited increased activity, diving and other behavior normally associated with feeding. By contrast, air that had passed across the surface of an identical cup containing distilled water elicited no response. Increases in activity during food odor trials occurred only after turtles surfaced to breathe and peaked in the first post-breath minute, implying that the chemical cues eliciting the responses were unlikely to have been detected while the turtles were under water. These results provide the first direct evidence that sea turtles can detect airborne odors. Under natural conditions, this sensory ability might function in foraging, navigation or both.

Odor-modulated Navigation in Insects and Artificial Systems

Two pieces of information are absolutely required to locate a source of chemicals from a distance. The first and most obvious is the presence of the chemical cue, and the second is the direction of the flow of air or water carrying the chemicals. Insects orienting to wind while walking in terrestrial environments appear to use the mechanical deflection of their antennae to detect the direction and magnitude of the flow they are moving through (Bell and Kramer, 1979). Thus, in these cases the antennae are providing information on both the presence (and absence) of odor and the direction of the flow. Many flying insects locate resources such as food and mates using windborne odors (Willis and Arbas, 1991; Arbas et al., 1993). Flying insects also use mechanosensory deflection of their antennae, in addition to deflection of mechanosensory hairs on their faces, to detect their speed and direction of movement through the air (Arbas, 1986). This information is then integrated with visually detected flow field feedback showing their movement with respect to the environment (David, 1986) to determine their steering movements (Olberg, 1983). Thus, the visual flow field feedback used to stabilize and control their flight behaviour also provides the information on wind speed and direction necessary to steer and control flight with respect to the wind during odor tracking behaviour (i.e. wind information is the result of the difference between intended and actual course) (David, 1986). One of the most studied flying odor tracking systems is that of male moths tracking female sex attractant pheromone to locate mates (Arbas et al., 1993). Perhaps the most remarkable olfactory task achieved by insects is that of locating distant resources using airborne chemical cues. It is currently thought that two primary mechanisms underlie flying insects’ ability to perform this behavior: (i) an odor-modulated, visually mediated orientation to the wind direction; and (ii) an odoractivated internal program of turns. The blending of these two mechanisms is thought to generate the upwind zigzagging paths that we observe from insects tracking odors in flight (Figure 1B). It is well established that these two mechanisms are both modulated by characteristics of odor plumes, resulting in predictable changes in the structure of the tracking behavior. It is not yet clear whether vision contributes significantly to the odor tracking behavior of walking insects. However, recent experiments revealed that the structure of the walking paths of pheromone tracking cockroaches look remarkably like those observed from flying insects, and thus may be governed by similar mechanisms (Figure 1A). These new results suggest that zigzagging into the wind may possess elements that enable odor trackers to more successfully adapt their behavior and locate important resources using odor information. We are using robots that can move in two and three dimensions to test hypothetical control algorithms based on our results and the results of similar behavioral studies. Our recent experiments with wheeled robots tracking wind-borne plumes of ionized air (Figure 1C) have shown that there are tradeoffs between algorithms that generate rapid tracking but low probabilities of source location, and algorithms that generate very slow tracking but much higher probabilities of source location. While algorithms that alter the robot’s steering and turning behavior according to the local plume concentration generate tracks that are both rapid and highly successful at locating the source. Wheeled robots are a good way to test hypothetical control algorithms underlying the olfactory orientation of walking insects, but not for flying insects. We have recently developed a gantry robot that is capable of tracking windborne plumes in three dimensions (Figure 1D). This robot will eventually have all of the sensors possessed by the pheromone tracking moths and use them to control its motion.

Response of male Centruroides vittatus (Scorpiones: Buthidae) to aerial and substrate-borne chemical signals

Summary Chemical signaling promotes mate location throughout numerous animal taxa. In this study we investigated the possibility that striped scorpions, Centruroides vittatus, use chemical signaling in the form of odor plumes or substrate-borne deposits as communication channels. A Y-shaped arena was constructed to test scorpions’ use of air-borne chemical cues in the detection of potential mates. A second, circular behavioral choice chamber was used to test male scorpions’ responses to female deposits by direct substrate contact. Male scorpions showed no tendency to move toward the female in tests of air-borne chemical transmission but they did demonstrate behavior associated with chemical detection when exposed to substrate-borne feminine deposits. Our experiments do not provide evidence that male C. vittatus use aerial pheromones to locate female scorpions but that they are highly sensitive to direct contact of substrate-borne chemical deposits.

The Role of Olfaction in Host-Seeking of Mosquitoes: A Review

This review concentrates on air-borne chemical cues that blood-seeking mosquitoes use to locate a host. A distinction is made between short- and long-range attraction. Carbon dioxide is involved in both processes. It activates and attracts mosquitoes. The latter function is only observed in combination with an odorous organo-chemical. Other olfactory cues are primarily involved in long-range attraction. Bodily emanations from the host that contain olfactory cues can be divided into three groups: Skin emanations, exhaled air and urine. Each of these is attractive to mosquitoes, but there is little knowledge about the chemical compounds that cause the attraction. Lactic acid in the presence of CO2 is attractive, and lactic acid-sensitive neurosensilla are present on the antennae. Other host-produced chemicals are also attractive, but chemical identification and subsequent confirmation of attractiveness for mosquitoes has not been reported. Host preference in mosquitoes is speciesspecific and varies from highly specific to opportunistic. Attraction is likely to be caused by a mixture of several compounds. Synergism may be an important way of increasing the effect of separate chemical cues.

Stimulus control of predatory attack in the brown tree snake (Boiga irregularis)

AbstractThree experiments studied predation upon neonatal rodents by brown tree snakes (Boiga irregularis). Experiment 1 showed that chemical cues arising from prey were used in foraging tests that could not be completed on the basis of vision alone. Experiment 2 provided only airborne chemical cues, and snakes performed at chance levels in selecting among odoriferous (baited) and non-odoriferous (unbaited) nests. Snakes performed above chance, however, when a chemical trail led to the baited nest (Experiment 3), suggesting that non-volatile chemicals are most important in guiding choice behaviour.