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Anal Bioanal Chem (2013) 405:6389–6403

DOI 10.1007/s00216-013-7113-9

REVIEW

On-site airborne pheromone sensing


Christoph Wehrenfennig & Matthias Schott &
Tina Gasch & Rolf Alexander Düring &
Andreas Vilcinskas & Claus-Dieter Kohl

Received: 17 February 2013 / Revised: 24 May 2013 / Accepted: 3 June 2013 / Published online: 11 July 2013
# Springer-Verlag Berlin Heidelberg 2013

Abstract Pheromones and other semiochemicals play an im- Keywords Infochemical . Semiochemical . Pheromone
portant role in the natural world by influencing the behavior of sensing . Biosensors . Biomimetic chemical sensors
plants, mammals, and insects. In the latter case, species-
dependent pheromone communication has numerous applica- Abbreviations
tions, including the detection, trapping, monitoring and guiding DRIFT diffuse reflectance infrared Fourier transform
of insects, as well as pest management in agriculture. On-site EAG electroantennography
sensors are desirable when volatile organic compounds (VOCs) e-nose electronic nose
are used as semiochemicals. Insects have evolved highly selec- FETs field-effect transistors
tive sensors for such compounds, so biosensors comprising IMS ion mobility spectrometry
complete insects, isolated organs or individual proteins can be NTD needle trap device
highly effective. However, isolated insect organs have a limited OBPs odorant-binding proteins
lifetime as biosensor, so biomimetic approaches are needed for QMBs quartz-crystal microbalances
prolonged monitoring, novel applications, or measurements in SAW surface-acoustic-wave
challenging environments. We discuss the development of on- SOMMSA selective odorant measurement of a multi-
site biosensors and biomimetic approaches for airborne- sensor array
pheromone sensing, together with biomimetic VOC sensor VOCs Volatile organic compounds
systems. Furthermore, the infochemical effect describing the
anthropogenic contamination of the ecosystem through
semiochemicals, will be considered in the context of novel
on-site pheromone sensing-systems. Introduction

Communication and the ability to understand transmitted


information are advantageous for the survival. This was
This paper is dedicated to Professor Franz Dickert on the occasion of his formalized in 1959 by Karlson and Lüscher, who proposed
70th birthday pheromones as active “substances which are secreted to the
C. Wehrenfennig (*) : C.<D. Kohl outside by an individual and received by a second individual
Institute of Applied Physics, JLU Giessen, Heinrich-Buff-Ring 16, of the same species, in which they release a specific reaction”
35392 Giessen, Germany [1]. This definition has been expanded into a more complex
e-mail: christoph.wehrenfennig@ap.physik.uni-giessen.de
biological terminology describing chemical interactions
C. Wehrenfennig : R. A. Düring within and among organisms, embracing a new research area
Institute for Soil Science and Soil Conservation, JLU Giessen, known as chemical ecology [2]. Pheromones can be detected
Heinrich-Buff-Ring 26-32, Giessen, Germany by vertebrates, invertebrates [3], and plants [4] at extremely
M. Schott : T. Gasch : A. Vilcinskas
low concentrations over long distances [5].
Institute for Phytopathology and Applied Zoology, JLU Giessen,
Heinrich-Buff-Ring 26-32, Giessen, Germany
Terminology
A. Vilcinskas
Fraunhofer Institute for Molecular Biology and Applied Ecology
IME, Project Group Bioresources, Winchesterstraße 2, Infochemicals are compounds that carry information [6]. An
35394 Giessen, Germany extended terminology has arisen from different classification
6390 C. Wehrenfennig et al.

systems based on the communication participants and From the chemical perspective, pheromones are usually
cost–benefit analyses [7]. Infochemicals are classed either hydrocarbons with specific combinations of double bonds,
as hormones or semiochemicals (Fig. 1), the former me- chirality, and functional groups containing nitrogen, oxygen,
diating communication within an organism and the latter and sulfur [33]. The molecular weight ranges from 17.03 Da in
between organisms. Further classifications are summarized the case of ammonia, which is used as a pheromone by the
in Table 1. German cockroach (Blattella germanica) [34], to 885.43 Da in
In the case of hormones, the subclassification level reflects the case of triolein (1,2,3-propanetriyl ester-(Z)-9-octadecenoic
the distance over which the signal is carried (producer acid), which is used as a pheromone by the red imported fire
cell/autocrine < local cells/paracrine < distant cells/endocrine). ant (Solenopsis invicta) [35, 36]. Carbon dioxide is classified
In the case of semiochemicals, the subclassification level re- as a cue rather than a semiochemical [6] even through it can be
flects the cost–benefit criterion to the emitter. Further classifi- detected by many organisms [28]. Semiochemicals are not
cation systems also define predator and host allelomones [8] necessarily restricted to particular taxonomic groups although
and primer and releaser semiochemicals [10]. Semiochemicals species may be able to distinguish particular isomers or enan-
can be assigned to multiple classes if they have more than one tiomers [37]. For example, diverse species with distinct evo-
function (e.g., an intraspecific pheromone could also attract a lutionary origins and habitats may use the same sex phero-
predator and therefore function as a kairomone [11]. mone, as seen in the Asian elephant (Elephas maximus) [38]
The second classification system arises from sorting com- and the African elephant (Loxodonta africana) [39], which
munication chemicals by the behavioral responses or commu- share the sex pheromone (Z)-7-dodecen-1-yl acetate with 140
nication functions listed in Table 2 [27, 28]. An allomone species of moth [40]. One of these moth species is the six-
produced by a predator to lure its prey could be classified as spot burnet (Zygaena filipendulae) [41] shown in Fig. 2. This
an attractant, whereas an allomone produced by the prey could convergence does not cause confusion in shared habitats
function as a predator repellent [8]. But even this behavioral because the moth releases only small quantities below the
classification involves multi-faceted assignments because or- detection threshold of the elephant olfaction, with additional
ganisms often produce multifunctional semiochemicals at- compounds to distinguish the pheromone from elephant urine
tributable to parsimony [29]. For example, the sex phero- [40].
mone of the western horse lubber grasshopper (Taeniopoda A combined classification of molecular characteristics
eques) also functions as a predator repellent [30], whereas the and behavioral responses for different orders is complex
alarm pheromone of the black carpenter ant (Camponotus and requires many exceptions [33]. The analysis of the sex
pennsylvanicus) acts as an aggregation pheromone at lower pheromones from 600 lepidopteran species resulted in the
concentrations [31]. assignment of three major types [42]. Type 1 includes pri-
These species-dependent and multi-faceted classifications mary alcohols and their derivatives, type 2 polyunsaturated
can only be addressed comprehensively by using databases in hydrocarbons and their epoxy derivatives with a longer
which infochemicals can be sorted in different ways (e.g., by straight chain, and type 3 includes all other structures.
species, behavioral response, and molecular weight [32]. Every species has evolved unique pheromone characteristics

Fig. 1 Terminology of
infochemicals based on origin
and benefit (adapted from [6]
and [8])
On-site airborne pheromone sensing 6391

Table 1 Classification of infochemicals based on the communication participants and cost–benefit criteria

Infochemical Participants Sublevel Definition Reference

Hormone Within an organism Endocrine signaling Signals target distant cells through the blood or hemolymph [9]
Paracrine signaling Signals target cells in the vicinity of the glandular cell [9]
Autocrine signaling Signals target the cell producing the signal [9]
Pheromone Intraspecific [+. –] pheromone Signal benefits the emitter [7]
[− .+] pheromone Signal benefits the recipient [7]
[+.+] pheromone Signal benefits the emitter and recipient [7]
Signature mixture Intraspecific – Signal identifies individuals or members of a particular social group [3, 6]
Allelomone Interspecific Allomone Signal evokes a reaction favorable to emitter [7, 8]
Kairomone Signal evokes a reaction favorable to the recipient [7, 8]
Synomone Signal evokes a reaction favorable to the emitter and recipient [7, 8]

with small differences, and closely related species tend to chromatograph-mass spectrometer or flame ionization
have more similar sex pheromones blends [43]. detector.
The identification of semiochemicals is challenging be-
cause they are released at low concentrations into a chemi-
cally diverse environment. They often comprise different Technical applications of pheromones
molecules that trigger different behavioral reactions in a
concentration-dependent manner. Therefore, identification Pheromones can be used for many technical applications,
requires bioassays as well as a panel of analytical methods most in the context of pest management (Table 2). Different
[44]. The commonest methods used for the analysis of insect strategies are required according to the species, including
pheromones are electroantennography combined with a gas programs aiming to survey and eradicate invasive species

Table 2 Common technical applications of semiochemicals

Behavioral function Application Species Reference

Attractant Trapping – e.g., to lure insects into stick traps for eradication gypsy moth, (Lymantria dispar [L.]) [12]
Process monitoring – e.g., to identify marker substances Jewel beetle (Merimna atrata) [13]
for processing steps
Pest management – e.g., to pull pest insect to designed field Cotton (Helicoverpa) [14]
in the push-pull strategy
Repellent Pest management – e.g., to push pest insect from protected Cotton bollworm (Helicoverpa zae) [14]
fields in the push-pull strategy
Insect repellent – e.g., to prevent malaria spreading by (Anopheles arabiensis) [15]
protecting urban areas from vectors
Aggregation Detection – e.g., to notice infestation of domestic pests Bed bug (Cimex lectularius) [16]
pheromone
Alarm pheromone Pest management – e.g., to control plant damages Colorado potato beetle (Leptinotarsa [17]
decemlineata)
Brood pheromone Social insect manipulation – e.g., to enhance colony quality Honey bee (Apis mellifera) [18]
and productivity
[19]
Marking pheromone Pest management – e.g., to reduce residence time in trees by Cherry fruit fly (Rhagoletis cerasi) [20]
a pest insect
Sex pheromone Trapping – e.g., to lure insects into stick traps Oriental fruit moth (Grapholita molesta) [21]
Mating disruption – e.g., to prevent males and females finding Grapevine moths (Lobesia botrana) [22]
Breeding – optimize sperm collection for artificial insemination Mongrel dogs [23]
Spacing pheromone Pest management – e.g., to pretend a colonization by pest insects Indian meal moth (Plodia interpunctella) [24]
Trail pheromone Route guidance – e.g., to organize decentralized traffic systems Ants [25]
Pest management – e.g., to disrupt the harvesting of food sources Red imported fire ant (Solenopsis invicta) [26]
6392 C. Wehrenfennig et al.

Fig. 2 The African elephant


(Loxodonta africana) and the
six-spot burnet (Zygaena
filipendulae) that use the same
sex pheromone: (Z)-7-dodecen-
1-yl acetate. Adapted from [40]

[45]. For moths and other agricultural pests, the greatest [25]. Trail and marking pheromones can also be used for pest
damage is caused by the larvae rather than the adults, so management (e.g., the infestation of urban areas with ants,
the best approaches are push-pull strategies [14] or mating termites, and other insects [26]).
disruption [45]. The push-pull strategy involves the intro- Brood pheromones are important for behavior, develop-
duction of plants or dispensers, which release semioche- ment, and the division of labor in social insect colonies [18].
micals that repel pest insects. A refuge with no agricultural Such pheromones can therefore indicate the colony quality
significance is set aside, and semiochemicals that attract the and thus enhance honey production by bees [19].
same insects are used to avoid counterproductive selection All these methods are based on concentration-dependent
pressure. In the case of insects that act as vectors for human behavioral responses following the application of synthetic
pathogens, a push-only strategy is preferred [15]. Mating pheromones, so an accurate and sensitive monitoring system
disruption involves the use of pheromone dispensers that is required.
prevent males and females finding each other. In vineyards As well as these direct applications of pheromones, the
for example, dispensers are equipped with the major compo- identification of semiochemicals provides a collection of
nent of the sex pheromone of the female grapevine moth marker substances for environmental activities. For example
(Lobesia botrana), preventing males from locating females the jewel beetle (Merimna atrata) detects and distinguishes
by the normal zig-zag track method based on pheromone volatiles emitted from wood fires at different temperatures
concentration differences [28]. Spacing pheromones are pro- [47]. These marker substances can be used in industrial
duced by the larvae of Indian meal moth (Plodia inter- wood-drying facilities to control the heating and thus im-
punctella) to regulate colonization densities at their food prove efficiency [13]. Another example is the ability of plant
source [24]. This spacing pheromone is useful because it pro- pathogens to induce allomone production by host plants thus
tects resources from colonization by a pest. If the adult insect attracting the vector insect, as seen in the case of Cacopsylla
causes damage by acute infestation, mass trapping or attract- picta [48]. This allomone could be used to monitor plant
and-kill methods with attractants, aggregation pheromones, or diseases.
sex pheromones [21] can be used to manage smaller pest
populations [12, 22]. To control the damage caused by forag-
ing of insects, the application of host marking pheromones can Environmental toxicology
be used to limit residence times in treated trees (e.g., as shown
for the cherry fruit fly (Rhagoletis cerasi) [20]). Sex phero- The anthropogenic discharge of infochemicals into the envi-
mones also can be used to improve agricultural breeding (e.g., ronment has an impact on the balance of nature. Deliberate
by monitoring the estrous cycle of cows [46] and optimizing pheromone applications with calculated effects plus uncon-
sperm collection for an artificial insemination [23]). trolled anthropogenic infochemicals provide an important
Trail and marking pheromones can be used to streamline new challenge in ecotoxicology. If hormones are released
modern transport systems. For example, ant trail-pheromone into the environment, the consequences are described as
concentration differences can be used to develop algorithms endocrine effects [49, 50]. This is particularly relevant in
that allow the management of decentralized traffic systems terms of the persistence, bioaccumulation behavior, and
On-site airborne pheromone sensing 6393

toxicity of pharmaceutical products released into wastewater the antenna, which is covered with minute sensilla (Fig. 4).
[51]. Techniques have therefore been developed to monitor Antennal morphology is species-dependent but the organi-
and reduce the environmental impact of organic substances zational principles are conserved [58]. Semiochemicals enter
that cause an endocrine effect [52, 53]. If semiochemicals are the sensillum through small pores on the cuticle and are then
released into the environment, the consequences are described transported by odorant-binding proteins (OBPs), which al-
as infochemical effect [54]. The impact of semiochemical low hydrophobic odorants to cross the aqueous barrier of the
pollution is an emerging research area, particularly because sensilla lymph, whereupon they are released near odorant
the impact of airborne and aquatic semiochemicals depends on receptors on the dendrite membrane. This translocation in-
the species, the concentration, and the concurrent presence of volves encapsulation of the odorant, transport to the mem-
other semiochemicals. The probable impact of anthropogenic brane, and delivery by conformational change and ejection
semiochemicals on the environment is summarized in Fig. 3. resulting from interactions with negatively-charged sites on
This anthropogenic influence includes industrial processes, the dendrite membrane [37]. When an odorant binds its re-
urban activities, agricultural production, wastewater from in- ceptor, an ion channel opens and sends an electrical signal to
dustries, hospitals, or settlements and personal activities. In the odorant receptor neuron [59]. After perception, the odorant
wastewater the accumulation of semiochemicals is a great is degraded by a specific enzyme. The remarkable selectivity
problem, while a high risk arises from scents in cosmetics of the olfactory system is achieved by two filters in which the
and detergents for the airborne infochemical effect [54]. The first level of discrimination is determined by the OBPs and the
integrated pest management and insecticides in addition to second by the odorant receptors [37].
industrial process fumes create another group of problematic Remarkably, antennal olfaction in the great diving beetle
influences on semiochemical communication and cause (Dytiscus marginalis) functions efficiently both underwater
infochemical effects. The effects are diverse and hard to verify and in air [60]. In mammals, OBPs are located in the nose
(e.g., reports that certain cosmetics affect the aggressiveness of mucus [61]. Sensors can be built by utilizing the biological
the Japanese giant hornet, Vespa mandarina [55]). Therefore, components of natural olfaction systems or by mimicking
an on-site airborne semiochemical/pheromone sensing system them to develop biomimetic sensors, as discussed in the
is required to provide accurate measurements that can be following sections [62].
correlated with observed changes in behavior [56].

Sensing technology
Olfaction
Following the identification of a semiochemical, the next chal-
The most sensitive and selective detectors of semiochemicals lenge is the sensitive detection to allow concentrations to be
are found in animals that possess highly-adapted olfactory established for downstream applications. Insects in particular
systems characterized by complex interactions between pro- perceive low concentrations of individual pheromones and
teins and ligands. The insect olfactory system is located in signature mixtures, which provide highly-selective information

Fig. 3 The infochemical


effect–anthropogenic
opportunities to influence the
environment with
semiochemicals include
industrial processes (yellow),
urban activities (orange),
agricultural production (green),
wastewater from industries,
hospitals, or settlements (blue),
and personal activities (red)
6394 C. Wehrenfennig et al.

Fig. 4 The olfaction system of insects. (a) The grapevine moth sensillum; (g) perception of volatiles entering the sensillum pore, trans-
(Lobesia botrana); (b)–(e), scanning electron micrographs of antennal port of the odorant, and its binding protein to the recognition site at the
sensilla at different magnifications; (f) diagram of an individual odorant receptor, and subsequent degradation [57]

allowing them to carry out appropriate tasks. It is therefore Preparation steps


useful to investigate the mechanisms used by insects to sense
semiochemicals that are already applied in agriculture and Biological and particularly chemical sensors are less sensi-
industry. tive than natural sensors and also less selective, which means
On-site airborne pheromone sensing 6395

they are confused by substance mixtures. Therefore, samples likelihood of interference but still neuronal pattern recognition
for analysis need to be prepared by removing the interfering [79]. For example, an insect head can be connected to a robot
chemicals and enriching for the target semiochemicals. system with a programmed insect behavior, yielding a hybrid
Separation can be achieved by chromatography, or inter- robot system that can locate the source of a pheromone [5].
fering molecules can be removed by filtering, as long as the Behavioral changes or adaptations can be avoided com-
filter does not deplete the target semiochemicals [63]. pletely by recording the signals directly from isolated olfacto-
A preconcentration of airborne semiochemicals can be ry organs, an approach known as electroantennography
achieved using fluid systems or cryogenic systems, although (EAG). Here, the signal produced by the antennal neurons is
transport and on-site handling can be cumbersome [64, 65]. measured using two electrodes, which are connected to the dip
Solid sorbents must be optimized for different semiochemicals and the end of the antenna. This can also be achieved using
[66]. Therefore, thermal desorption is the most flexible tech- whole insects but this risks interference (e.g., from muscle
nique compared with light or solvent desorption for on-site impulses) whereas dissected antennae avoid such interference
sensing. Polymer-covered collectors, such as solid-phase but are limited by their reduced lifespan [80]. More specific
micro-extraction fibers, can also be used, but quantification signals can be collected by recording from a single sensillum
in the airborne environment depends on calibration using [81]. Portable EAG systems are adaptable and can be used for
internal standards or the addition of external standards to a on-site measurements, but they are often too bulky, fragile,
certain volume [67]. The direct quantification of air samples and unstable to provide reliable quantitative data [82]. The
requires a controlled air volume to be processed by complete choice of method for the identification of volatiles can also
absorption of all volatiles. This can be achieved using a needle affect the results of on-site recordings [83]. These drawbacks
trap device (NTD), which consists of a 23-gauge needle filled combined with the short lifetime of isolated antennae reduce
with different absorber materials and fulfills all the quantifi- the utility of EAG biosensors in the field [84]. The latest
cation requirements for air sampling [68]. The NTD is ideal biosensor systems based on insect antennae have been
for single enrichment during research and development, but is reviewed recently [57].
not yet functional enough for industrial analysis or on-site Other biosensors have been described that feature single
monitoring [69]. To combine preconcentration and separation, cells [85] or proteins [86]. These devices attempt to combine
the stepwise thermal desorption of the NTD in an injector or OBPs [87] or odorant receptors [88] with different types of
heater provides increased selectivity [70]. transducers, but they cannot match the complexity of natural
olfaction systems because the odorant degrading enzymes
Biosensors are missing, meaning that the same odorant molecule can be
detected multiple times. The biological components also dry
A biosensor contains a biological recognition component out when exposed to air, reducing their lifetime.
[71]. This ranges from the use of complete organisms such Drying can be delayed by refreshing the sensing cells at
as dogs [72] or bees [73] to the use of isolated organs, single certain intervals [89], and this approach has been used suc-
cells or enzymes. cessfully to detect acetone in the ppmv-range [90]. Acetone
Detection dogs are effective sensors but suffer fatigue after in low concentrations and in combination with carbon diox-
40 minutes and become less effective if the refreshing in- ide is an attractant for Anopheles gambiae, the mosquitoes
tervals are too short [74]. Dogs also require prolonged and that spread malaria [91].
expensive training [75]. Insects need no training when the Another drawback of biosensors based on single
target substances are pheromones [−,+] or [+,+] pheromones, cells/proteins is the loss of selectivity because of the missing
allemones, or synomones, but the signal can be difficult to nervous system. Therefore, a separation or elimination step
detect when using complete insects because this requires a is required to suppress interfering odorants.
quantifiable behavioral response. The semiochemicals may
evoke a physical reaction such as the proboscis extension Biomimetic sensors
reflex [76], or movement [77]. If there is no natural behavioral
response towards a particular substance, insects may be con- The traditional nonbiological approach for pheromone sens-
ditioned to respond by initially combining the target volatile ing consists of gas chromatography (or liquid chromatogra-
with a reward that does evoke a response [73]. A handheld phy for dissolved semiochemicals) coupled to a high resolu-
system for on-site measurements with trained insects (e.g., tion detector (e.g., electron capture (ECD), flame ionization
bees) is already available [78]. One drawback of whole- (FID), photoionization (PID), or mass spectrometry (MS)
organism biosensors is the poor quantification possibility [92]. These approaches require large apparatuses that tend
caused by behavioral changes and calibration challenges. not to be suitable for on-site applications or monitoring, so
This can be addressed by removing the physical-responding different sensor strategies are needed to detect semio-
organs and detecting their neuronal signals, where there is less chemicals. Chemical sensors measure the interaction of
6396 C. Wehrenfennig et al.

molecules with their environment. These sensors use trans- ranges and allows high-speed data acquisition. The use of air
ducers or physical sensors to monitor properties such as as carrier gas achieves low detection limits in controlled
molecular weight or mobility. Chemical and physical on- environments for more than 200 different analytes [99] that
site sensors for semiochemicals are less sensitive and less are partly known for their semiochemical activity. Samples
specific than biosensors, but they are more stable and reli- can be introduced by methods such as vaporization, vapor
able. The drawbacks of low sensitivity and selectivity are through a membrane, electrospray, wire desorption, laser
therefore addressed using preconcentration and volatile- desorption, and gas chromatography [100].
separation. Sensor arrays with data evaluation are used to The combination of IMS with a sampling system and a
mimic the biological selectivity of different receptors [93]. multi-capillary column (Fig. 5) allows the measurement of
The data can be evaluated by principal component analysis skin volatiles at low ppbv concentrations [101]. This showed
or linear discriminant analysis and must be extended for that benzaldehyde functions as a minor component of the
ambitious tasks. For successful mimicry, it is desirable to aggregation pheromone of the bed bug (Cimex lectularius)
use adaptive sensor systems that can respond to environmental and can be considered an attractant, providing a new appli-
changes during analysis. These systems include sensors with cation of IMS for the management of this domestic pest [16].
different transducer types, separation, and preconcentration In breath gas analysis, IMS coupled to a multi-capillary
units [94]. These biomimetic approaches for on-site measure- column allowed the detection of volatiles that act as spot
ments are often described as electronic nose (e-nose) systems. biomarkers of diseases. Combined with pattern recognition
E-nose systems are cost-effective, low-power handheld sys- without the need for chemical analysis of the underlying
tems suitable for measurements in different environments compounds, IMS can be used to diagnose lung cancer
utilizing an array of sensors to give a fingerprint response to [102]. The combination of a multi-capillary column, IMS
a given odor and data evaluation to identify and discriminate and pattern recognition is also useful for harvest protection
odors [95]. Therefore e-nose systems offer a high potential for (e.g., the minor pheromone components (vanillin and ethyl
on-site pheromone sensing. acrylate) of the corn bug (Eurygaster integriceps) [103], a
Since pheromone terminology originates from a biologi- cereal pest, which has been detected by IMS [104].
cal rather than a physical or chemical context [8], the prop-
erties described by chemical and physical sensors are diffi- Gravimetric sensors
cult to translate into the biological properties of pheromones.
Some physical and chemical sensing methods are discussed The deposition of volatiles onto the surface of surface-
in more detail below in the context of the on-site detection of acoustic-wave (SAW) sensors or quartz-crystal microbal-
pheromones. ances (QMBs) causes a resonance frequency shift and there-
fore allows the sensitive detection of specific chemicals. The
SAW device uses interdigital electrodes to produce a surface
On-site detection of pheromones wave, which travels along the surface of the sensor, whereas
bulk shear-waves are often used in QMBs to measure the
Ion mobility spectrometer amount of adsorbed gas [95].
The selectivity of such devices depends on the deposition
The different physical drift characteristics of molecules with of the target semiochemical, so a separation is needed for on-
diverse ion-mass, polarity, size, and shape properties through site pheromone detection. For applications in known envi-
a buffer gas in an electric field [96] provide the fundamental ronments, compact systems are available for the on-site
principle for ion mobility spectrometry (IMS). The technique quantification of calibrated volatiles combined with a pattern
was introduced as “plasma chromatography” for separation recognition system [105]. An alternative approach by
in a hybrid system with MS detectors. Unlike typical MS, the Dickert et al. involves molecular imprinting with target vol-
IMS can work at atmospheric pressure and can therefore be atiles to prepare the surface, thus increasing the specificity of
combined with a Faraday plate detector in a compact the surface without the need for a separation step [106]. The
handheld device. In order to reduce apparatus size even polymer chains are generated around the nonreacting tem-
further, the MS can be omitted [97]. The loss of qualita- plate molecules or the volatile is covered with antibodies
tive information as a consequence thereof can be mini- [107]. After polymerization the template is removed and the
mized by varying the field intensity using asymmetric resulting cavities can reversibly bind the target volatiles with
waveforms [98] for the analysis of illicit drugs, explo- high selectivity. This allows the selective detection of vola-
sives, chemical warfare degradation products, biomolecules, tiles with the same molecular weight, such as o-xylene and p-
and combinatorial chemistry samples. xylene. Both are present in the headspace of leaves and half-
IMS is ideal for on-site sensing if the target chemicals are ripe olives where they attract the olive fruit fly (Bactrocera
known because it has detection limits in the ppbv to pptv oleae) [108], and their ratio indicates the degree of ripeness.
On-site airborne pheromone sensing 6397

Fig. 5 Set-up of GC-IMS. The stainless steel pan used for skin VOC sampling was rinsed with nitrogen flow (3 mL/min) and its outlet was directly
connected to the sample loop integrated in the GC-IMS device. Adapted from [101]

Ammonia, which is a component of the aggregation phero- related elements (grain–grain or electrode–grain) caused by
mone of the German cockroach (Blattella germanica) [34], the capacitive behavior of the surface depletion regions [110].
can be detected using imprinted QCBs. Arrays of imprinted The sensing layer consists of a polymer or metal oxide on
sensor surfaces have been prepared and used successfully for top of an electrode structure. Two electrodes are sufficient but
on-site pheromone sensing in complex environments [109]. for time-dependent effects, impedance measurements with
more than two electrodes deliver non-equilibrium polarization
Conductive sensors effects [111]. The semiochemicals are reduced or oxidized on
the metal oxide surface and thereby cause a change in surface
Measuring the conductivity of a sensitive layer is a common charge depending on the reaction properties of the sensing
technique used with gas sensors, especially for the detection of material towards the different volatiles [112]. The application
low-mass volatiles and gases. Different techniques [110] to of different metal oxides, different sensing layers or metal
measure changes in the sensitive layer and identify prepara- doping in the sensor preparation set provides selectivity to-
tion influences are shown in Fig. 6. The diffuse reflectance wards known compounds. Furthermore, the reaction proper-
infrared Fourier transform (DRIFT) spectroscopy measures ties are influenced by the temperature of the sensing layer and
the diffuse reflectance of the sensing layer surface and pro- therefore gas sensors with controlled heating systems are more
vides additional information about surface reactions at differ- selective. Higher temperatures allow the sensors to recover
ent moistures. Hall measurements are important to define the more rapidly whereas lower temperatures show higher sensi-
influence of free charge carrier concentrations variations and tivity towards particular pheromones (e.g., E7,Z9-dodecadien-
the charge mobility contribution in the layer [110]. 1-yl acetate, the main component of the grapevine moth sex
Measurements with short, direct current impulses provide pheromone [113]). A temperature cycle combines these ad-
information about transport and drift processes [111]. The vantages [114, 115] but prevents the use of preconcentration
changes of the electron affinity are accessible through mea- or chromatography steps because the semiochemicals have to
surements of work function changes by the Kelvin probe. The cover the sensing layer with a constant concentration for the
catalytic conversion measurement offer more information whole temperature cycle.
about the catalytic influence of noble metal as additive in the Figure 7 shows the combination of preconcentration with a
layer or at the electrodes. The impedance measurement using NTD, a gas chromatograph and a sensor array with four metal
an alternating current is very useful in identifying contact- oxide sensors (Sn1–Sn3 = tin oxide, W1 = tungsten oxide) in a
6398 C. Wehrenfennig et al.

Fig. 6 Overview of available investigation techniques for gas sensors with sensitive layers, including DRIFT spectroscopy, hall measurement,
catalytic conversion measurement, impedance measurement and work function, and DC measurement. Adapted from [110]

selective odorant measurement of a multi-sensor array temperature cycles to the data recording and processing
(SOMMSA) device compared with the sensitivity of a dissect- [119]. Among these toxic volatiles, formaldehyde is known
ed insect antenna and MS [70]. The insect antenna is more for its semiochemical activity as attractant for certain arthro-
sensitive but suffers from aging (although this can be corrected pods [120]. Even highly-sensitive sensors need an extensive
by calibration impulses that are applied at the beginning and data analysis to detect the target pheromone against the back-
end of the measurement). The sensor signals are collected in a ground of host volatiles [121]. Therefore, a sensor array is
constant temperature mode that provides rapid and separable usually necessary for on-site pheromone sensing systems
reactions for the pheromone and other components (e.g., the based on metal oxide gas sensors.
decomposition product and butylhydroxytoluene, an anti- Another application of the sensing material is the use of
oxidizing additive in the pheromone dispenser). By applying field-effect transistors (FETs) as a gate regulator, allowing
the SOMMSA approach, the individual signals of the four the detection of complex organic molecules [122]. The FET
sensors allow biomimetic pattern recognition. also functions as a transducer system and can be combined
Changing the structure of the sensing layer by increasing with biological components to produce a BioFET [123]. The
the surface using a smaller grain size [116] enhances the application of insect antenna in a BioFET system [124] has
sensitivity but reduces the applicable sensor-temperature limit been tested for the management of potato pests [17].
due to grain growth at higher temperatures [117]. This draw- Electrochemical sensors can also be used to detect volatiles
back can be managed with ordered mesoporous materials based on the current produced by a reaction at the surface of the
produced by casting methods, which achieve higher tempera- working electrode within the electrolyte. To improve selectiv-
ture stability and smaller grain sizes [118]. These micro- ity, the system can incorporate multiple working electrodes
structured sensors allow the prolonged and inexpensive mon- made from different metals operating at different potentials
itoring of indoor air quality and toxic volatiles. Greater selec- [125]. The membrane covering the electrolyte can also
tivity can be achieved by adding virtual sensors based on increase the selectivity. Controllable ion-selective electrodes
On-site airborne pheromone sensing 6399

sensing in challenging environments, electrode stability and


the leaching of membrane components into the sample are
critical factors [128]. In electric noses, the electrochemical
reaction functions as a transducer or basic sensor. With this
combination of chemical and biological components, such
devices are classified as biosensors [129].

Optical sensors

Optical sensors measure interactions between semiochemicals


and light between an emitter and receiver. The principal systems
can be extended by optical elements such as fibers [130], or can
be combined with a sensing layer (Fig. 6) so that the optical
components only act as transducers [110]. Such techniques can
be coupled with new materials such as carbon nanotubes that
allow the rapid and energy-efficient detection of volatiles [131].
Some optical sensors include compact Fourier transform
infrared spectrometers for the gas phase, allowing the charac-
terization of semiochemicals with double-bond configurations
[132]. The location of double bonds, the cis-trans configura-
tion and the existence of diastereoisomerism play an important
role in the activity of pheromones [133]. For example, analy-
sis of the cuticle by near-infrared spectroscopy makes it pos-
sible to discriminate between the closely related species
Drosophila subobscura and D. obscura because they produce
distinct pheromones and signature mixtures [134].

Fig. 7 NTD-GC-MS-EAD-SOMMSA measurement of a 50-mL en- Limitations and challenges


richment from the headspace of a mixture of water and the main
pheromone component of Lobesia botrana. (a) EAD trace and moni-
toring pulses, (b) MS total ion current, (c) metal oxide gas sensor Each of the above-mentioned techniques has its advantages
conductivities (Sn1–Sn3 = tin oxide - SnO2, W1 = tungsten oxide - and disadvantages for the sensing of different pheromones as
WO3), and (d) an enlargement of the timespan of the pheromone summarized in Table 3.
response normalized to the conductance level at 1000 s [70] Limiting factors include the size and cost of the sensing
apparatus, which often determine its portability. Most sensi-
[126] and molecular imprinting [127] can also be combined tive analytical techniques require vacuum, carrier gas, or
with these other improvements. For on-site pheromone heating, which reduces their suitability for on-site pheromone

Table 3 Comparison of sensor systems for pheromone sensing

Sensor Advantages Disadvantages Subgenus / species Semiochemical Detection Reference


system limit

Ion Mobility High sensitivity Limited compound Bed bug (Cimex lectularius) Benzaldehyde 200 pptv [16, 101]
Spectrometer detection , high-cost
sensor
Gravimetric Aquatic applicable Unspecific condensation Olive fruit fly (Bactrocera oleae) o-xylene and 200 ppmv [106, 108]
Sensors (reducible by imprinting p-xylene
with specific bond sites)
Conductive Low-cost sensor, Low selectivity (increasable Grapevine moths E7,Z9-dodecadien- 19 ppmv [22, 70]
sensors fast measurement by temperature-cycles) (Lobesia botrana) 1-yl acetate
Optical sensors Fast measurement Larger system Vinegar flies (Drosophila Mixtures of - [132, 134]
subobscura and D. obscura) hydrocarbons
Olive Bark Beetle Ethylene 280 pptv [135, 136]
(Phloeotribus scarabaeoides)
6400 C. Wehrenfennig et al.

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