Odor tracking flight of male Manduca sexta moths along plumes of different cross-sectional area

Males of the hawkmoth, Manduca sexta, track wind-borne plumes of female sex pheromone by flying upwind, while continuously turning from side-to-side and changing altitude. Their characteristic “zigzagging” trajectory has long been thought to result from the interaction of two mechanisms, an odor-modulated orientation to wind and a built-in central nervous system turning program. An interesting and as of yet unanswered question about this tracking behavior is how the cross-section of an odor plume or its clean-air “edges” affects moths’ odor tracking behavior. This study attempts to address this question by video recording and analyzing the behavior of freely flying M. sexta males tracking plumes from pheromone sources of different lengths and orientations with equal odor concentration per unit area. Our results showed that moths generated significantly wider tracks in wide plumes from the longest horizontally-oriented sources as compared to narrower point-source plumes, but had relatively unaltered tracks when orienting to plumes from the same length sources oriented vertically. This suggests that in addition to wind and the presence of pheromones, the area of the plume’s cross section or its edges may also play an important role in the plume tracking mechanisms of M. sexta.     

Mechanisms of animal navigation in odor plumes

Chemical signals mediate many of life's processes. For organisms that use these signals to orient and navigate in their environment, where and when these cues are encountered is crucial in determining behavioral responses. In air and water, fluid mechanics impinge directly upon the distribution of odorous molecules in time and space. Animals frequently employ behavioral mechanisms that allow them to take advantage of both chemical and fluid dynamic information in order to move toward the source. In turbulent plumes, where odor is patchily distributed, animals are exposed to a highly intermittent signal. The most detailed studies that have attempted to measure fluid dynamic conditions, odor plume structure, and resultant orientation behavior have involved moths, crabs, and lobsters. The behavioral mechanisms employed by these organisms are different but generally integrate some form of chemically modulated orientation (chemotaxis) with a visual or mechanical assessment of flow conditions in order to steer up-current or upwind (rheo- or anemo-taxis, respectively). Across-stream turns are another conspicuous feature of odor-modulated tracks of a variety of organisms in different fluid conditions. In some cases, turning is initiated by detection of the lateral edges of a well-defined plume (crabs), whereas in other animals turning appears to be steered according to an internally generated program modulated by odor contacts (moth counterturning). Other organisms such as birds and fish may use similar mechanisms, but the experimental data for these organisms is not yet as convincing. The behavioral strategies employed by a variety of animals result in orientation responses that are appropriate for the dispersed, intermittent plumes dictated by the fluid-mechanical conditions in the environments that these different macroscopic organisms inhabit.     

Using lobster noses to inspire robot sensor design

Robots are needed to locate the sources of toxic chemical plumes. Lobsters, which track odor plumes for many ecologically crucial activities, can provide inspiration for robot designers. Before accurate search strategies for robots can be developed, how odor molecules are captured by the lobster's chemosensors must be understood. A recent study by Koehl et al. shows how lobster olfactory antennules alter the patterns of concentration in turbulent odor plumes during odor sampling.     

Effects of odor flux and pulse rate on chemosensory tracking in turbulent odor plumes by the blue crab, Callinectes sapidus

The ability of animals to track through chemical plumes is often related to properties of evanescent odor bursts and to small-scale mixing process that determine burst properties. However, odor plumes contain variation over a range of scales, and little is known about how variation in the properties of the odor signal on the scale of one to several seconds affects foraging performance. We examined how flux and pulse rate interact to modulate the search behavior of blue crabs, Callinectes sapidus, locating odor sources in controlled flume flows. Experimental treatments consisted of continuous plumes and plumes with discrete odor pulses at intervals of 2.5 s and 4 s at two fluxes. Crabs experienced diminished search success and reduced search efficiency as flux decreased and the inter-pulse interval lengthened. There often were significant interactions between flux and pulse length, and neither property completely determined search behavior. Thus, over the time span of several seconds, the blue crab chemosensory system is not a simple flux detector. The sensitivity of blue crabs to inter-pulse intervals in the range of several seconds indicates that larger-scale mixing processes, which create odor variation on comparable scales, may exert a significant impact on foraging success in nature.     

Using Insect Electroantennogram Sensors on Autonomous Robots for Olfactory Searches

Robots designed to track chemical leaks in hazardous industrial facilities¹ or explosive traces in landmine fields² face the same problem as insects foraging for food or searching for mates³: the olfactory search is constrained by the physics of turbulent transport⁴. The concentration landscape of wind borne odors is discontinuous and consists of sporadically located patches. A pre-requisite to olfactory search is that intermittent odor patches are detected. Because of its high speed and sensitivity^5-6, the olfactory organ of insects provides a unique opportunity for detection. Insect antennae have been used in the past to detect not only sex pheromones⁷ but also chemicals that are relevant to humans, e.g., volatile compounds emanating from cancer cells⁸ or toxic and illicit substances^9-11. We describe here a protocol for using insect antennae on autonomous robots and present a proof of concept for tracking odor plumes to their source. The global response of olfactory neurons is recorded in situ in the form of electroantennograms (EAGs). Our experimental design, based on a whole insect preparation, allows stable recordings within a working day. In comparison, EAGs on excised antennae have a lifetime of 2 hr. A custom hardware/software interface was developed between the EAG electrodes and a robot. The measurement system resolves individual odor patches up to 10 Hz, which exceeds the time scale of artificial chemical sensors¹². The efficiency of EAG sensors for olfactory searches is further demonstrated in driving the robot toward a source of pheromone. By using identical olfactory stimuli and sensors as in real animals, our robotic platform provides a direct means for testing biological hypotheses about olfactory coding and search strategies¹³. It may also prove beneficial for detecting other odorants of interests by combining EAGs from different insect species in a bioelectronic nose configuration¹⁴ or using nanostructured gas sensors that mimic insect antennae¹⁵.     

Behavioral strategies underlying pheromone-modulated flight in moths: lessons from simulation studies

Several mechanisms have been proposed to underlie the characteristic `zigzag' tracks produced by moths flying up an odor plume. To test which, if any, of these are capable of reproducing the animals' behavior, we constructed behavioral-level simulations. The simulations are as tightly constrained as possible by the known biology, and incorporate realistic physical effects such as air turbulence, and delays due to sensory transduction and axonal condition, to mimic the dynamics of sensory information encountered by real moths. Formulated as schemas, the models all share a common set of sensory and motor systems, but differ in the interposed control systems. We analyzed the behavior of the models with the same methods we use for real moths. Even the simplest of the models was capable of successful orientation some of the time, and of producing flight tracks similar to those of moths. Individuals which succeeded in tracking the odor plume produced average behavior not significantly different from that of real moths. As a population, however, none of the models was as successful as the moths. The best of the models had a success rate in tracking the plume of about 30%, compared to the average of 70% seen in the insects. Accepted: 25 March 1998     

Design and elevation of sex-attractant traps for pea moth, Cydia nigricana (Steph.) and the effect of plume shape on catches

• 1 Catches of male pea moths in six designs of trap, each containing (E,E)-8,10-dodecadienyl acetate as an attractant, were compared; triangular-shaped traps caught most moths.
• 2 The vertical distribution of moths within a pea crop and the size of catches at different levels varied in different wind speeds. Three-quarter crop height is probably the optimum height for monitoring.
• 3 Five trap designs (including the triangular type) captured only 20–30% of individuals landing on them; water traps were slightly more efficient.
• 4 There was an eight-fold range in the number of moths caught depending on the sticky material used. ‘Bird-Tanglefoot’ was most effective.
• 5 Smoke plumes, emitted from different trap designs in the field to simulate plumes of attractant, were photographed and measured. The effect of trap design on plume shape was confirmed in wind tunnel tests.
• 6 Field tests showed that the more elongated the mean plume emitted from a trap the greater the catch.
• 7 The tracks of individual moths flying to traps are discussed in relation to current views on orientation to odour sources.

     

Impact of (Z)-7-dodecenol and turbulence on pheromone-mediated flight manoeuvres of male Trichoplusia ni

Abstract. Turbulence and chemical noise are two factors which may influence pheromone-mediated flight manoeuvres of a moth in natural habitats. In this study, the effects of turbulence and the behavioural antagonist (Z)-7-dodecenol on flight manoeuvres of male Trichoplusia ni (Hübner) were evaluated in a wind tunnel. Male moths increase airspeed and course angles when turbulence is increased. This leads to significant increases in the length of flight tracks, but significant reductions in the time taken to reach a pheromone source. In less disturbed pheromone plumes, distributions of course angles and track angles of male T.ni show a prominent peak centred about 0° relative to the upwind direction, indicating that moths can temporarily steer directly upwind toward a pheromone source.
When (Z)-7-dodecenol is released 10 cm upwind of a pheromone source to form an overlapping plume downwind, course angles, airspeeds and ground-speeds of male T.ni are reduced significantly compared with those in uncon-taminated pheromone plumes. This results in a longer flight time to reach a pheromone source. The decrease in flight speed would decrease the rate of contact with filaments, and thereby perhaps allow the moth to detect uncon-taminated pheromone filaments independently from filaments containing the behavioural antagonist.     

Cautious cannibals: Behavioral responses of juvenile and adult blue crabs to the odor of injured conspecifics

Blue crabs are cannibalistic, and therefore the scent of injured conspecifics represents both a potential food cue, as well as an indicator of predation risk. We examined the response of blue crabs to conspecific odor alone, as well as in mixtures of attractive cues to determine how animals evaluate and respond to this odor. We explicitly manipulated risk-sensitivity based on either animal size (an indicator of susceptibility to predation) or hunger state (susceptibility to starvation) as ways to evaluate theories of risk-allocation, which suggest that decreases in predation risk, or increases in the risk of starvation, ought to result in diminished responses to sensory cues that signal predator presence or activity. Large and small blue crabs were challenged to locate the source of odor plumes consisting of the scent of injured conspecifics (risk cue), attractive food odors (attractive cue), or their mixture (conflicting cue). Neither large nor small blue crabs tracked aversive cues, but large blue crabs consistently tracked conflicting treatments to their source. Responses to conflicting and aversive treatments also involved diminished movement and reduced tracking speed relative to behaviors displayed in attractive plumes. Thus, even cannibalistic crabs seem to respond more prevalently to the apparent predation risk then to food reward, and risk-sensitive behaviors have a likely cost in terms of reduced food intake. Starved animals were more likely than unstarved animals to track conflicting plumes. Both the ontogenic shift and the response of starved animals support the notion that the cost of risk-aversive behaviors results in this strategy being allocated in proportion to the degree of potential risk. Since risk-aversive responses to chemical cues can produce strong effects in communities, the size-dependent nature of these responses in blue crabs may introduce considerable complexity in interactions between blue crabs, their predators, and their prey.     

Cryptically Patterned Moths Perceive Bark Structure When Choosing Body Orientations That Match Wing Color Pattern to the Bark Pattern

Many moths have wing patterns that resemble bark of trees on which they rest. The wing patterns help moths to become camouflaged and to avoid predation because the moths are able to assume specific body orientations that produce a very good match between the pattern on the bark and the pattern on the wings. Furthermore, after landing on a bark moths are able to perceive stimuli that correlate with their crypticity and are able to re-position their bodies to new more cryptic locations and body orientations. However, the proximate mechanisms, i.e. how a moth finds an appropriate resting position and orientation, are poorly studied. Here, we used a geometrid moth Jankowskia fuscaria to examine i) whether a choice of resting orientation by moths depends on the properties of natural background, and ii) what sensory cues moths use. We studied moths’ behavior on natural (a tree log) and artificial backgrounds, each of which was designed to mimic one of the hypothetical cues that moths may perceive on a tree trunk (visual pattern, directional furrow structure, and curvature). We found that moths mainly used structural cues from the background when choosing their resting position and orientation. Our findings highlight the possibility that moths use information from one type of sensory modality (structure of furrows is probably detected through tactile channel) to achieve crypticity in another sensory modality (visual). This study extends our knowledge of how behavior, sensory systems and morphology of animals interact to produce crypsis.     

A Magnetic Tether System to Investigate Visual and Olfactory Mediated Flight Control in Drosophila

It has been clear for many years that insects use visual cues to stabilize their heading in a wind stream. Many animals track odors carried in the wind. As such, visual stabilization of upwind tracking directly aids in odor tracking. But do olfactory signals directly influence visual tracking behavior independently from wind cues? Also, the recent deluge of research on the neurophysiology and neurobehavioral genetics of olfaction in Drosophila has motivated ever more technically sophisticated and quantitative behavioral assays. Here, we modified a magnetic tether system originally devised for vision experiments by equipping the arena with narrow laminar flow odor plumes. A fly is glued to a small steel pin and suspended in a magnetic field that enables it to yaw freely. Small diameter food odor plumes are directed downward over the fly s head, eliciting stable tracking by a hungry fly. Here we focus on the critical mechanics of tethering, aligning the magnets, devising the odor plume, and confirming stable odor tracking.Open in a separate windowClick here to view.^{(57M, flv)}     

Flying Beetles Respond as Moths Predict: Optomotor Anemotaxis to Pheromone Plumes at Different Heights

The current level of understanding of orientation mechanisms used by flying insects responding to pheromone sources, based almost entirely on studies of moths and flies, allows clear predictions to be made of how other, hitherto little-studied insect taxa, such as beetles (Coleoptera), should behave if the same mechanisms are used. Results are presented of the first test of such set of predictions, the effect of flight height on ground speed, on a beetle, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae). The beetle P. truncatus flew upwind toward the source of horizontal pheromone plumes and responded to the movement of visible patterns on the floor of a sustained flight tunnel. Beetles flying at a greater height from the floor were less responsive to moving floor patterns. The flight speeds of P. truncatus increased with flight altitude, as found with moths, suggesting that they use orientation mechanism similar to those of moths.     

Flight behaviour of Cadra cautella males in rapidly pulsed pheromone plumes

Abstract Airborne pheromone plumes in wind comprise filaments of odour interspersed with gaps of clean air. When flying moths intercept a filament, they have a tendency to surge upwind momentarily, and then fly crosswind until another filament is intercepted. Thus, the moment-to-moment contact with pheromone mediates the shape of a flight track along the plume. Within some range of favourable interception rates, flight tracks become straighter and are headed more due upwind. However, as the rate of interception increases, there comes a point at which the moth should not be able to discern discreet filaments but, rather, should perceive a 'fused signal'. At the extreme, homogeneous clouds of pheromone inhibit upwind progress by representative tortricids. In a wind tunnel, Cadra cautella (Walker) (Lepidoptera: Pyralidae) were presented with 10 ms pulses of pheromone at a repetition rate of 5, 10, 17 and 25/s and a continuous, internally turbulent plume. Pulse size and concentrations were verified with a miniature photoionization detector sampling surrogate odour, propylene, at 100 Hz. Male moths maintain upwind progress even at plumes of 25 filaments/s. Furthermore, moths exhibited greater velocities and headings more due upwind at 17 and 25 Hz than at the lower frequencies or with the continuous plume. It is hypothesized that either C. cautella possesses a versatile sensory system that allows the resolution of these rapidly pulsed pheromone plumes, or that this species does not require a 'flickering' signal to fly upwind.     

A single sex pheromone receptor determines chemical response specificity of sexual behavior in the silkmoth Bombyx mori

In insects and other animals, intraspecific communication between individuals of the opposite sex is mediated in part by chemical signals called sex pheromones. In most moth species, male moths rely heavily on species-specific sex pheromones emitted by female moths to identify and orient towards an appropriate mating partner among a large number of sympatric insect species. The silkmoth, Bombyx mori, utilizes the simplest possible pheromone system, in which a single pheromone component, (E, Z)-10,12-hexadecadienol (bombykol), is sufficient to elicit full sexual behavior. We have previously shown that the sex pheromone receptor BmOR1 mediates specific detection of bombykol in the antennae of male silkmoths. However, it is unclear whether the sex pheromone receptor is the minimally sufficient determination factor that triggers initiation of orientation behavior towards a potential mate. Using transgenic silkmoths expressing the sex pheromone receptor PxOR1 of the diamondback moth Plutella xylostella in BmOR1-expressing neurons, we show that the selectivity of the sex pheromone receptor determines the chemical response specificity of sexual behavior in the silkmoth. Bombykol receptor neurons expressing PxOR1 responded to its specific ligand, (Z)-11-hexadecenal (Z11-16:Ald), in a dose-dependent manner. Male moths expressing PxOR1 exhibited typical pheromone orientation behavior and copulation attempts in response to Z11-16:Ald and to females of P. xylostella. Transformation of the bombykol receptor neurons had no effect on their projections in the antennal lobe. These results indicate that activation of bombykol receptor neurons alone is sufficient to trigger full sexual behavior. Thus, a single gene defines behavioral selectivity in sex pheromone communication in the silkmoth. Our findings show that a single molecular determinant can not only function as a modulator of behavior but also as an all-or-nothing initiator of a complex species-specific behavioral sequence.     

Flight of male Cadra cautella along plumes of air and pheromone superimposed on backgrounds of pheromone

Male Cadra cautella were presented with five heterogeneous pheromone clouds (created from source doses of 0, 0.01, 1, 100, and 10 000 ng) with and without superimposed plumes of either clean air or sex pheromone in a wind tunnel. Moths provided with the lowest doses of background clouds without a superimposed plume did not fly upwind. Moths provided with higher doses of background clouds, with or without superimposed air plumes, increased their track, course, and drift angles (i.e., their zigzags headed more towards crosswind) with increased dose, but slowed their velocity. No differences in flight track parameters were observed for moths provided with a superimposed pheromone plume, regardless of the background cloud dose. Moreover, moths were able to locate the source of superimposed air plumes in the highest background dose, and of superimposed pheromone plumes in any background dose. The significance of these results is discussed in the context of mating disruption.     

Crossmodal visual input for odor tracking during fly flight

Flies generate robust and high-performance olfactory and visual behaviors. Adult fruit flies can distinguish small differences in odor concentration across antennae separated by less than 1 mm [1], and a single olfactory sensory neuron is sufficient for near-normal gradient tracking in larvae [2]. During flight a male housefly chasing a female executes a corrective turn within 40 ms after a course deviation by its target [3]. The challenges imposed by flying apparently benefit from the tight integration of unimodal sensory cues. Crossmodal interactions reduce the discrimination threshold for unimodal memory retrieval by enhancing stimulus salience [4], and dynamic crossmodal processing is required for odor search during free flight because animals fail to locate an odor source in the absence of rich visual feedback [5]. The visual requirements for odor localization are unknown. We tethered a hungry fly in a magnetic field, allowing it to yaw freely, presented odor plumes, and examined how visual cues influence odor tracking. We show that flies are unable to use a small-field object or landmark to assist plume tracking, whereas odor activates wide-field optomotor course control to enable accurate orientation toward an attractive food odor.     

Body-size influence on defensive behavior of Amazonlan moths: an ecophysiological approach.

Ectotherm locomotion is restricted by low temperatures, and many species, such as some flying insects, need to achieve thermal thresholds before taking off. Body size influences heat exchange between an animal and the environment. Therefore, larger animals have higher thermal inertia, and necessarily spend more time in pre-flight warming up, a critical period when they remain exposed and more susceptible to predators. Thus, one could expect larger animals, along their evolutionary history, to have developed a more diversified repertoire of defensive behaviors when compared to their smaller counterparts. Moths are an interesting model for testing this hypothesis, as they exhibit considerable variation in body size and many species present pre-flight warming up by muscle shivering, an evidence of thermal restriction on locomotion. I registered the responses of 76 moths immediately after simulating the attack of a predator and then associated behavioral response to body size. I conducted the experiments at 20 and 25 degrees C to check for possible thermal restrictions on behavior, and identified animals to the family level to check for the effects of a common phylogenetic history. When disturbed at 25 degrees C, smaller moths tend to fly, while larger ones tend to run. At 20 degreedC almost all moths ran, including the smaller ones, indicating a possible thermal restriction on flight. Corroborating the proposed hypothesis, a more diversified repertoire of defensive behaviors was registered among larger moths. An alternative interpretation would be that common behaviors among related moths could be explained by common phylogenetic histories. However, two facts support the physiological restriction hypothesis: (1) the analysis within Sphingidae and Geometridae (not closely related families) showed similar results to those of the overall analysis, and (2) a more diverse repertoire of defensive behaviors was associated to the lower, and therefore more restrictive to locomotion, temperature (20 degrees C).     

BEEtag: A Low-Cost,Image-Based Tracking System for the Study of Animal Behavior and Locomotion

A fundamental challenge common to studies of animal movement, behavior, and ecology is the collection of high-quality datasets on spatial positions of animals as they change through space and time. Recent innovations in tracking technology have allowed researchers to collect large and highly accurate datasets on animal spatiotemporal position while vastly decreasing the time and cost of collecting such data. One technique that is of particular relevance to the study of behavioral ecology involves tracking visual tags that can be uniquely identified in separate images or movie frames. These tags can be located within images that are visually complex, making them particularly well suited for longitudinal studies of animal behavior and movement in naturalistic environments. While several software packages have been developed that use computer vision to identify visual tags, these software packages are either (a) not optimized for identification of single tags, which is generally of the most interest for biologists, or (b) suffer from licensing issues, and therefore their use in the study of animal behavior has been limited. Here, we present BEEtag, an open-source, image-based tracking system in Matlab that allows for unique identification of individual animals or anatomical markers. The primary advantages of this system are that it (a) independently identifies animals or marked points in each frame of a video, limiting error propagation, (b) performs well in images with complex backgrounds, and (c) is low-cost. To validate the use of this tracking system in animal behavior, we mark and track individual bumblebees (Bombus impatiens) and recover individual patterns of space use and activity within the nest. Finally, we discuss the advantages and limitations of this software package and its application to the study of animal movement, behavior, and ecology.     

Neural factors and evitability in insect behavior.

Compared with more complex behavior patterns involving goal selection, evasive behavior of prey animals elicited by the presence of a natural predator is usually considered to be relatively inevitable and stereotyped. Noctuid moths, while flying in the field at night, show two types of evasive response pattern when their tympanic organs detect the ultrasonic cries of marauding insectivorous bats. Since sound is the sole communication channel between prey and predator, this situation invites neurophysiological and behavioral analysis. When, in the course of studying this behavior, moths are removed by stages from the natural circumstances of this interaction their evasion responses become much less invariant; that is, more evitable. The possible survival value of some evitability in this behavior under natural circumstances is discussed. The afferent nerve response of the noctuid auditory organ is highly stable; therefore, the source or sources of this evitability must lie down-stream in the moth central nervous system. Acoustic interneuronal systems within the thoracic ganglia and the brain have been examined for lapses in responsiveness and for other indications of transsynaptic instability that might correlate with the demonstrated behavioral evitability.     

2010年牧区2代草地螟成虫迁飞的虫源分析

草地螟(Loxostege sticticalis L.)是危害我国北方农牧区的重要迁飞性害虫,明确其迁飞、扩散规律以及与境外虫源交流情况,对早期预警和有效防治具有重要意义。2010年6月1日至9月17日,利用垂直监测昆虫雷达的观测资料,结合探照灯和地面灯灯诱虫情、迁飞高峰期雌虫卵巢解剖、区域大气环流形势和迁飞轨迹分析,在内蒙古锡林浩特西郊研究了牧区2代草地螟的迁飞过程,结果表明:2010年牧区2代草地螟迁飞高峰期出现在2010年8月8日至8月21日,高峰日为8月11日,高峰日探照灯诱虫量达9167头,卵巢发育级别以1—2级为主,高峰日雷达回波主要集中在300—400 m。轨迹分析显示:迁飞高峰期8月8日、8月10—12日牧区草地螟迁飞虫源主要来自蒙古共和国东南部及中蒙边境地区,由蒙古气旋西南侧的西北气流输送进入我国内蒙古锡林郭勒盟,再随西南气流迁入呼伦贝尔草原。