Physical Processes and Real-Time Chemical Measurement of the Insect Olfactory Environment

Odor-mediated insect navigation in airborne chemical plumes is vital to many ecological interactions, including mate finding, flower nectaring, and host locating (where disease transmission or herbivory may begin). After emission, volatile chemicals become rapidly mixed and diluted through physical processes that create a dynamic olfactory environment. This review examines those physical processes and some of the analytical technologies available to characterize those behavior-inducing chemical signals at temporal scales equivalent to the olfactory processing in insects. In particular, we focus on two areas of research that together may further our understanding of olfactory signal dynamics and its processing and perception by insects. First, measurement of physical atmospheric processes in the field can provide insight into the spatiotemporal dynamics of the odor signal available to insects. Field measurements in turn permit aspects of the physical environment to be simulated in the laboratory, thereby allowing careful investigation into the links between odor signal dynamics and insect behavior. Second, emerging analytical technologies with high recording frequencies and field-friendly inlet systems may offer new opportunities to characterize natural odors at spatiotemporal scales relevant to insect perception and behavior. Characterization of the chemical signal environment allows the determination of when and where olfactory-mediated behaviors may control ecological interactions. Finally, we argue that coupling of these two research areas will foster increased understanding of the physicochemical environment and enable researchers to determine how olfactory environments shape insect behaviors and sensory systems.

[1]  R. Wehner,et al.  Pinpointing food sources: olfactory and anemotactic orientation in desert ants, Cataglyphis fortis. , 2000, The Journal of experimental biology.

[2]  Werner Lindinger,et al.  Proton-transfer-reaction mass spectrometry (PTR–MS): on-line monitoring of volatile organic compounds at pptv levels , 1998 .

[3]  K. Hiraoka,et al.  Development of Sniffing Atmospheric Pressure Penning Ionization , 2006 .

[4]  Juan M Sanchez,et al.  Performance characteristics of a new prototype for a portable GC using ambient air as carrier gas for on-site analysis. , 2007, Journal of separation science.

[5]  J. Visser THE DESIGN OF A LOW‐SPEED WIND TUNNEL AS AN INSTRUMENT FOR THE STUDY OF OLFACTORY ORIENTATION IN THE COLORADO BEETLE (LEPTINOTARSA DECEMLINEATA) , 1976 .

[6]  M. Koehl,et al.  The fluid mechanics of arthropod sniffing in turbulent odor plumes. , 2006, Chemical senses.

[7]  T. Baker,et al.  Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[8]  P. Guerenstein,et al.  Olfactory and behavioural responses of the blood-sucking bug Triatoma infestans to odours of vertebrate hosts. , 2001, The Journal of experimental biology.

[9]  G. Bri,et al.  Dispersion of carbon dioxide plumes in African woodland: implications for host-finding by tsetse flies , 2004 .

[10]  K. Mylne,et al.  Concentration fluctuation measurements in a plume dispersing in a stable surface layer , 1992 .

[11]  John Palassis,et al.  Instrument Performance Criteria Portable Photoionization Detector Instruments , 1997 .

[12]  D Schneider,et al.  Insect olfaction: deciphering system for chemical messages. , 1969, Science.

[13]  J. D. de Gouw,et al.  Measurements of volatile organic compounds in the earth's atmosphere using proton-transfer-reaction mass spectrometry. , 2007, Mass spectrometry reviews.

[14]  G. Stange Effects of changes in atmospheric carbon dioxide on the location of hosts by the moth, Cactoblastis cactorum , 1997, Oecologia.

[15]  P. J. Mason,et al.  Concentration fluctuation measurements in a dispersing plume at a range of up to 1000 m , 1991 .

[16]  A fast, multichannel fluorometer for investigating aquatic chemoreception and odor trails , 1988 .

[17]  M J Weissburg,et al.  The fluid dynamical context of chemosensory behavior. , 2000, The Biological bulletin.

[18]  B. Lamb,et al.  Surrogate Pheromone Plumes in Three Forest Trunk Spaces: Composite Statistics and Case Studies , 2004 .

[19]  Comparison between measured tracer fluxes and footprint model predictions over a homogeneous canopy of intermediate roughness , 2003 .

[20]  Eugene Yee,et al.  Statistical characteristics of concentration fluctuations in dispersing plumes in the atmospheric surface layer , 1993 .

[21]  H. Mustaparta Responses of single olfactory cells in the pine weevilHylobius abietis L. (Col.: Curculionidae) , 1975, Journal of comparative physiology.

[22]  R. Zimmermann Laser ionisation mass spectrometry for on-line analysis of complex gas mixtures and combustion effluents , 2005, Analytical and bioanalytical chemistry.

[23]  Jörg-Peter Schnitzler,et al.  Practical approaches to plant volatile analysis. , 2006, The Plant journal : for cell and molecular biology.

[24]  A. Lewis,et al.  Two high-speed, portable GC systems designed for the measurement of non-methane hydrocarbons and PAN: results from the Jungfraujoch High Altitude Observatory. , 2004, Journal of environmental monitoring : JEM.

[25]  N. Dean Pentcheff,et al.  PHYSICAL CONSTRAINTS ON ECOLOGICAL PROCESSES: A FIELD TEST OF ODOR‐MEDIATED FORAGING , 2000 .

[26]  Ring T. Cardé,et al.  Antennal resolution of pulsed pheromone plumes in three moth species. , 2002, Journal of insect physiology.

[27]  N. Dean Pentcheff,et al.  Odor transport in turbulent flows: Constraints on animal navigation , 1999 .

[28]  C. Yeretzian,et al.  Laser mass spectrometry as on-line sensor for industrial process analysis: process control of coffee roasting. , 2004, Analytical chemistry.

[29]  R. Schlögl,et al.  Caterpillar-elicited methanol emission: a new signal in plant-herbivore interactions? , 2006, The Plant journal : for cell and molecular biology.

[30]  K. Kaissling,et al.  Die Riechschwelle des Seidenspinners , 2004, Naturwissenschaften.

[31]  Junwei Zhu,et al.  Odor discrimination using insect electroantennogram responses from an insect antennal array. , 2002, Chemical senses.

[32]  John Murtis,et al.  Odor Plumes and How Insects Use Them , 1992 .

[33]  Thomas W. Kirchstetter,et al.  Emissions From Miombo Woodland and Dambo Grassland Savanna Fires in Southern Africa , 2003 .

[34]  Masoud Agah,et al.  Temperature-programmed GC using silicon microfabricated columns with integrated heaters and temperature sensors. , 2007, Analytical chemistry.

[35]  R. Cardé,et al.  Spatial and temporal structures of pheromone plumes in fields and forests , 2000 .

[36]  F. Bogner Sensory physiological investigation of carbon dioxide receptors in lepidoptera , 1990 .

[37]  A. Guenther,et al.  Eddy covariance measurement of biogenic oxygenated VOC emissions from hay harvesting , 2001 .

[38]  Frank Vogt Trends in Remote Spectroscopic Sensing and Imaging - Experimental Techniques and Chemometric Concepts , 2006 .

[39]  D. Schneider Elektrophysiologische Untersuchungen von Chemo- und Mechanorezeptoren der Antenne des Seidenspinners Bombyx mori L. , 2004, Zeitschrift für vergleichende Physiologie.

[40]  A. Robins,et al.  The effects of source size on concentration fluctuations in plumes , 1982 .

[41]  T. C. Turlings,et al.  Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. , 2006, The Analyst.

[42]  A. Snyder,et al.  Monitoring of Airborne Organic Vapors Using Ion Mobility Spectrometry , 1990 .

[43]  T. Eisner,et al.  Sex attractant of an arctiid moth (Utetheisa ornatrix): A pulsed chemical signal , 1980, Behavioral Ecology and Sociobiology.

[44]  R. Cooks,et al.  Direct analysis of semivolatile organic compounds in air by atmospheric pressure chemical ionization mass spectrometry. , 2001, Analytical chemistry.

[45]  Clifford K. Ho,et al.  Overview of Sensors and Needs for Environmental Monitoring , 2005, Sensors (Basel, Switzerland).

[46]  R. Cody,et al.  Versatile new ion source for the analysis of materials in open air under ambient conditions. , 2005, Analytical chemistry.

[47]  H. E. Hummel,et al.  Techniques in Pheromone Research , 1984, Springer Series in Experimental Entomology.

[48]  R. Stull An Introduction to Boundary Layer Meteorology , 1988 .

[49]  W. Boland,et al.  Ultrafast sampling and analysis of plant volatiles by a hand‐held miniaturised GC with pre‐concentration unit: Kinetic and quantitative aspects of plant volatile production , 2002 .

[50]  N. Bârsan,et al.  Electronic nose: current status and future trends. , 2008, Chemical reviews.

[51]  J. Hildebrand,et al.  Analysis of chemical signals by nervous systems. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Cheryl Ann Zimmer,et al.  Dynamic Scaling in Chemical Ecology , 2008, Journal of Chemical Ecology.

[53]  N D Pentcheff,et al.  Odor Plumes and Animal Navigation in Turbulent Water Flow: A Field Study. , 1995, The Biological bulletin.

[54]  David J. Thomson,et al.  Concentration fluctuation measurements in tracer plumes using high and low frequency response detectors , 1996 .

[55]  P. Moore,et al.  Odor landscapes and animal behavior: tracking odor plumes in different physical worlds , 2004 .

[56]  J. E. Cermak,et al.  Problems of atmospheric shear flows and their laboratory simulation , 1970 .

[57]  Donald R. Webster,et al.  Chemosensory guidance cues in a turbulent chemical odor plume , 2001 .

[58]  Flavio Roces,et al.  Wind-induced ventilation of the giant nests of the leaf-cutting ant Atta vollenweideri , 2001, Naturwissenschaften.

[59]  Andrew M. Taylor,et al.  Direct atmospheric pressure chemical ionisation ion trap mass spectrometry for aroma analysis: Speed, sensitivity and resolution of isobaric compounds , 2005 .

[60]  G. Stange Sensory and Behavioural Responses of Terrestrial Invertebrates to Biogenic Carbon Dioxide Gradients , 1996 .

[61]  Chuji Wang,et al.  Absorption Cross-Sections of the C—H Overtone of Volatile Organic Compounds: 2 Methyl-1,3-Butadiene (Isoprene), 1,3-Butadiene, and 2,3-Dimethyl-1,3-Butadiene , 2007, Applied spectroscopy.

[62]  F. Fehsenfeld,et al.  Use of proton‐transfer‐reaction mass spectrometry to characterize volatile organic compound sources at the La Porte super site during the Texas Air Quality Study 2000 , 2003 .

[63]  Eran Pichersky,et al.  Biology of floral scent , 2006 .

[64]  A. Mbi,et al.  A new acetone detection device using cavity ringdown spectroscopy at 266 nm: evaluation of the instrument performance using acetone sample solutions , 2007 .

[65]  W. Roelofs Electroantennogram Assays: Rapid and Convenient Screening Procedures for Pheromones , 1984 .

[66]  J Atema,et al.  Eddy Chemotaxis and Odor Landscapes: Exploration of Nature With Animal Sensors. , 1996, The Biological bulletin.

[67]  J. Hildebrand,et al.  Sensory processing of ambient CO2 information in the brain of the moth Manduca sexta , 2004, Journal of Comparative Physiology A.

[68]  A. S. French,et al.  A new method for wide frequency range dynamic olfactory stimulation and characterization. , 2007, Chemical senses.

[69]  J. Hildebrand,et al.  Effect of elevated atmospheric CO2 on oviposition behavior in Manduca sexta moths , 2005 .

[70]  J. Murlis Odor Plumes and the Signal They Provide , 1997 .

[71]  Ring T. Cardé,et al.  Strategies for recontacting a lost pheromone plume: casting and upwind flight in the male gypsy moth , 1994 .

[72]  R. Cardé,et al.  Fine-scale structure of pheromone plumes modulates upwind orientation of flying moths , 1994, Nature.

[73]  F. Harren,et al.  Selective trace gas detection of complex molecules with a continuous wave optical parametric oscillator using a planar jet expansion , 2007 .

[74]  Huanwen Chen,et al.  Rapid in vivo fingerprinting of nonvolatile compounds in breath by extractive electrospray ionization quadrupole time-of-flight mass spectrometry. , 2007, Angewandte Chemie.

[75]  J. Atema,et al.  Spatial Information in the Three-Dimensional Fine Structure of an Aquatic Odor Plume. , 1991, The Biological bulletin.

[76]  E. Zellers,et al.  Multi-adsorbent preconcentration/focusing module for portable-GC/microsensor-array analysis of complex vapor mixtures. , 2002, The Analyst.

[77]  R. Zimmer,et al.  Chemical signaling processes in the marine environment. , 2000, The Biological bulletin.

[78]  Helko Borsdorf,et al.  Ion Mobility Spectrometry: Principles and Applications , 2006 .

[79]  R. Sacks,et al.  Silicon microfabricated column with microfabricated differential mobility spectrometer for GC analysis of volatile organic compounds. , 2005, Analytical chemistry.

[80]  O. Haefliger,et al.  Direct mass spectrometric analysis of flavors and fragrances in real applications using DART. , 2007, Rapid communications in mass spectrometry : RCM.

[81]  D. Tholl 1 Detection and Identification of Floral Scent Compounds , 2006 .

[82]  R. Cardé,et al.  Insect Pheromone Research: New Directions , 1997 .

[83]  J. Elkinton,et al.  Evaluation of time-average dispersion models for estimating pheromone concentration in a deciduous forest , 1984, Journal of Chemical Ecology.

[84]  J. Murlis,et al.  Effects of pheromone plume structure and visual stimuli on the pheromone-modulated upwind flight of male gypsy moths (Lymantria dispar) in a Forest (Lepidoptera: Lymantriidae) , 1994, Journal of Insect Behavior.

[85]  A. Hansel,et al.  On-line monitoring of volatile organic compounds at pptv levels by means of proton-transfer-reaction mass spectrometry (PTR-MS) medical applications, food control and environmental research , 1998 .

[86]  J. Hildebrand,et al.  Temporal tuning of odor responses in pheromone‐responsive projection neurons in the brain of the sphinx moth Manduca sexta , 1999, The Journal of comparative neurology.

[87]  P. Crutzen,et al.  Comprehensive laboratory measurements of biomass‐burning emissions: 2. First intercomparison of open‐path FTIR, PTR‐MS, and GC‐MS/FID/ECD , 2004 .

[88]  John Murlis,et al.  Measurement of Odor-Plume Structure in a Wind Tunnel Using a Photoionization Detector and a Tracer Gas , 2002 .

[89]  D. Baldocchi Turbulent transfer in a deciduous forest. , 1989, Tree physiology.

[90]  A. Borg-Karlson,et al.  (–)-Germacrene D receptor neurones in three species of heliothine moths: structure-activity relationships , 2003, Journal of Comparative Physiology A.

[91]  J. C. Kaimal,et al.  Atmospheric boundary layer flows , 1994 .

[92]  John G Hildebrand,et al.  Roles and effects of environmental carbon dioxide in insect life. , 2008, Annual review of entomology.

[93]  A. S. French,et al.  Dynamic properties of antennal responses to pheromone in two moth species. , 2005, Journal of neurophysiology.

[94]  Thomas L Daniel,et al.  Flower tracking in hawkmoths: behavior and energetics , 2007, Journal of Experimental Biology.

[95]  R. Cooks,et al.  Ambient Mass Spectrometry , 2006, Science.

[96]  Marc J. Weissburg,et al.  Life and Death in Moving Fluids: Hydrodynamic Effects on Chemosensory‐Mediated Predation , 1993 .

[97]  N. Mole,et al.  Concentration fluctuation data from dispersion experiments carried out in stable and unstable conditions , 1994 .

[98]  J. Peñuelas,et al.  Dynamics of the enhanced emissions of monoterpenes and methyl salicylate, and decreased uptake of formaldehyde, by Quercus ilex leaves after application of jasmonic acid. , 2006, The New phytologist.

[99]  W. Roelofs,et al.  Sustained-flight tunnel for measuring insect responses to wind-borne sex pheromones , 1978, Journal of Chemical Ecology.

[100]  Cori Bargmann Comparative chemosensation from receptors to ecology , 2006, Nature.

[101]  F. Roces,et al.  Carbon dioxide concentrations and nest ventilation in nests of the leaf-cutting ant Atta vollenweideri , 2000, Insectes Sociaux.

[102]  R. Desjardins,et al.  Advances in Bioclimatology , 1992 .

[103]  L A Todd Mapping the air in real-time to visualize the flow of gases and vapors: occupational and environmental applications. , 2000, Applied occupational and environmental hygiene.

[104]  J. Murlis,et al.  Fine‐scale structure of odour plumes in relation to insect orientation to distant pheromone and other attractant sources , 1981 .

[105]  T. Baker,et al.  Effects of varying sex pheromone component ratios on the zigzagging flight movements of the oriental fruit moth,Grapholita molesta , 1988, Journal of Insect Behavior.

[106]  M. Kleiman,et al.  Characterization of concentration fluctuations of a surface plume in a neutral boundary layer , 1988 .

[107]  P. Zimmerman,et al.  Isoprene measurement by ozone-induced chemiluminescence , 1990 .

[108]  P. Marriott,et al.  Analytical Limbo: How low can you go? , 2006 .

[109]  T. Baker,et al.  Latencies of behavioral response to interception of filaments of sex pheromone and clean air influence flight track shape in Heliothis virescens (F.) males , 1996, Journal of Comparative Physiology A.

[110]  R. Cardé,et al.  Navigational Strategies Used by Insects to Find Distant, Wind-Borne Sources of Odor , 2008, Journal of Chemical Ecology.

[111]  E. Matisová,et al.  Fast gas chromatography and its use in trace analysis. , 2003, Journal of chromatography. A.

[112]  H. Schlichting Boundary Layer Theory , 1955 .