Semiochemicals and Insect Behavior

A special issue of Insects (ISSN 2075-4450).

Deadline for manuscript submissions: closed (31 October 2019) | Viewed by 115106

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Guest Editor
Laboratory of Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, University of Liege (ULiege), Passage des Déportés, 2-5030 Gembloux, Belgium
Interests: insect chemical ecology; plant–insect interactions; biological control; pheromones; invasive species
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Special Issue Information

Dear colleagues,

Thank to their complex olfactory system, insects are able to perceive a large panel of semiochemicals, including pheromones (for intraspecific communication) and allelochemicals (for interspecific communication). Semiochemicals can be volatile or non-volatile molecules, released above or below ground, limited to the insect cuticule or dispersed several kilometers away from their source. In numerous insect species, olfaction plays a crucial role in many behavioral contexts, such as locating host plant, sexual partners, oviposition sites, overwintering sites and prey or host. Semiochemicals allow insects to discriminate between virus-infected and non-infected plants, to perceive the presence of natural enemies or to identify the mating status of a potential partner. The study of the origin, function, and significance of all these semiochemicals falls within the scope of the multidisciplinary discipline named chemical ecology, which brings together the expertise of chemists, ecologists, behavioral biologists, neurobiologists and molecular biologists. This discipline is receiving increasing attention, particularly with regard to the multiple applications of semiochemicals, for example in biological control.

This Special Issue is addressed to all scientists performing research in the field of chemical ecology, including the identification and synthesis of the substances that carry information, the elucidation of receptor and transduction systems, and the behavioral and ecological consequences of these chemical signals. We invite the submission of high quality original research papers and also encourage the submission of mini-reviews covering any aspect of semiochemical-mediated insect behavior.

Prof. Dr. François Verheggen
Guest Editor

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Keywords

  • collection and identification of semiochemicals
  • insect pheromones
  • host plant location
  • courtship and mating behavior
  • aggregation behavior
  • social communication
  • plant volatile organic compounds
  • hydrocarbons

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Published Papers (23 papers)

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18 pages, 2850 KiB  
Article
Low Host Specialization in the Cuckoo Wasp, Parnopes grandior, Weakens Chemical Mimicry but Does Not Lead to Local Adaption
by Carlo Polidori, Yolanda Ballesteros, Mareike Wurdack, Josep Daniel Asís, José Tormos, Laura Baños-Picón and Thomas Schmitt
Insects 2020, 11(2), 136; https://doi.org/10.3390/insects11020136 - 20 Feb 2020
Cited by 5 | Viewed by 3661
Abstract
Insect brood parasites have evolved a variety of strategies to avoid being detected by their hosts. Few previous studies on cuckoo wasps (Hymenoptera: Chrysididae), which are natural enemies of solitary wasps and bees, have shown that chemical mimicry, i.e., the biosynthesis of cuticular [...] Read more.
Insect brood parasites have evolved a variety of strategies to avoid being detected by their hosts. Few previous studies on cuckoo wasps (Hymenoptera: Chrysididae), which are natural enemies of solitary wasps and bees, have shown that chemical mimicry, i.e., the biosynthesis of cuticular hydrocarbons (CHC) that match the host profile, evolved in several species. However, mimicry was not detected in all investigated host-parasite pairs. The effect of host range as a second factor that may play a role in evolution of mimicry has been neglected, since all previous studies were carried out on host specialists and at nesting sites where only one host species occurred. Here we studied the cuckoo wasp Parnopes grandior, which attacks many digger wasp species of the genus Bembix (Hymenoptera: Crabronidae). Given its weak host specialization, P. grandior may either locally adapt by increasing mimicry precision to only one of the sympatric hosts or it may evolve chemical insignificance by reducing the CHC profile complexity and/or CHCs amounts. At a study site harbouring three host species, we found evidence for a weak but appreciable chemical deception strategy in P. grandior. Indeed, the CHC profile of P. grandior was more similar to all sympatric Bembix species than to a non-host wasp species belonging to the same tribe as Bembix. Furthermore, P. grandior CHC profile was equally distant to all the hosts’ CHC profiles, thus not pointing towards local adaptation of the CHC profile to one of the hosts’ profile. We conducted behavioural assays suggesting that such weak mimicry is sufficient to reduce host aggression, even in absence of an insignificance strategy, which was not detected. Hence, we finally concluded that host range may indeed play a role in shaping the level of chemical mimicry in cuckoo wasps. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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12 pages, 1081 KiB  
Article
Evaluation of d-Limonene and β-Ocimene as Attractants of Aphytis melinus (Hymenoptera: Aphelinidae), a Parasitoid of Aonidiella aurantii (Hemiptera: Diaspididae) on Citrus spp.
by Khalid Mohammed, Manjree Agarwal, Beibei Li, James Newman, Tao Liu and Yonglin Ren
Insects 2020, 11(1), 44; https://doi.org/10.3390/insects11010044 - 8 Jan 2020
Cited by 24 | Viewed by 4332
Abstract
The volatile organic compounds (VOCs) released from herbivore-infested plants can be used as chemical signals by parasitoids during host location. In this research, we investigated the VOC chemical signals for the parasitoid Aphytis melinus to discriminate between Aonidiella aurantii (California red scale)-infested fruit [...] Read more.
The volatile organic compounds (VOCs) released from herbivore-infested plants can be used as chemical signals by parasitoids during host location. In this research, we investigated the VOC chemical signals for the parasitoid Aphytis melinus to discriminate between Aonidiella aurantii (California red scale)-infested fruit and non-infested fruit on three different citrus species. First, we identified the chemical stimuli emanating from non-infested and A. aurantii-infested citrus fruits via solid phase microextraction (SPME) and gas chromatography-mass spectrometry (GC-MS) analyses and identified 34 volatile organic compounds (VOCs). The GC-MS analysis showed qualitative and quantitative differences between VOCs emitted from non-infested and infested citrus fruit. Two VOCs, d-limonene and β-ocimene, were significantly increased in all infested fruit, regardless of the fruit species. The response of the female adult A. melinus to olfactory cues associated with A. aurantii infested fruit was evaluated using a Y-tube olfactometer. In two-choice behavioural assays, A. melinus females preferred infested citrus cues over non-infested fruit. Females showed positive chemotaxis toward these VOCs in all tested combinations involving two dosages of synthetic compounds, d-limonene and β-ocimene, except for d-limonene at a dosage of 10 μL/mL. The application of these VOCs may help to enhance the effectiveness of bio-control programs and parasitoid mass-rearing techniques. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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13 pages, 1891 KiB  
Article
Oviposition-Induced Volatiles Affect Electrophysiological and Behavioral Responses of Egg Parasitoids
by Panagiotis G Milonas, Eirini Anastasaki and Georgios Partsinevelos
Insects 2019, 10(12), 437; https://doi.org/10.3390/insects10120437 - 5 Dec 2019
Cited by 23 | Viewed by 3487
Abstract
In response to an attack by herbivores, plants emit a variety of compounds that may act as semiochemicals. Oviposition-induced volatiles (OIPVs) have been shown to mediate interactions between plants and natural enemies. Here, we investigated the role of OIPVs by Tuta absoluta towards [...] Read more.
In response to an attack by herbivores, plants emit a variety of compounds that may act as semiochemicals. Oviposition-induced volatiles (OIPVs) have been shown to mediate interactions between plants and natural enemies. Here, we investigated the role of OIPVs by Tuta absoluta towards two egg parasitoids, Trichogramma cordubense and T. achaeae. We collected headspace volatiles from tomato plants at 24, 48, and 72 h after oviposition by T. absoluta females and tested the antennographic response of Trichogramma parasitoids to them by means of gas chromatography- electro-antennographical detection (GC-EAD). The response of the parasitoids was also tested in behavioral experiments using a Y-tube olfactometer. Oviposition by T. absoluta females induced qualitative and quantitative changes in the volatiles emitted by tomato plants. Antennae of Trichogramma parasitoids responded to several of the induced volatiles in GC-EAD. T. cordubense females were attracted to tomato plants with T. absoluta eggs 24 h after oviposition. The elucidation of the behavior of egg parasitoids towards OIPVs enhances the development of sustainable management strategies either by selecting species that exploit OIPVs or by manipulating their foraging behavior by utilizing specific OIPVs that are used by parasitoids as a host location. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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16 pages, 3031 KiB  
Article
Trapping Brown Marmorated Stink Bugs: “The Nazgȗl” Lure and Kill Nets
by David Maxwell Suckling, Valerio Mazzoni, Gerardo Roselli, Mary Claire Levy, Claudio Ioriatti, Lloyd Damien Stringer, Valeria Zeni, Marco Deromedi and Gianfranco Anfora
Insects 2019, 10(12), 433; https://doi.org/10.3390/insects10120433 - 30 Nov 2019
Cited by 6 | Viewed by 6134
Abstract
Improvements to current brown marmorated stink bug (BMSB), Halyomorpha halys, surveillance and killing systems are needed to improve detection sensitivity and to reduce pesticide use. Detection of BMSB in New Zealand with traps is reliant on sticky panels with aggregation pheromone, which [...] Read more.
Improvements to current brown marmorated stink bug (BMSB), Halyomorpha halys, surveillance and killing systems are needed to improve detection sensitivity and to reduce pesticide use. Detection of BMSB in New Zealand with traps is reliant on sticky panels with aggregation pheromone, which are low cost but inefficient compared with beating foliage. Trapping for BMSB adults and nymphs was conducted daily with lethal traps consisting of an aggregation pheromone-baited-coat hanger covered with dark-colored long-lasting insecticide-treated mesh, we termed “The Nazgȗl”, based on its sinister appearance. A deep tray lined with white plastic was attached centrally at the base for collecting the dead BMSB. The lethal traps killed and caught up to 3.5-fold more nymphs and adult BMSB than identically-baited sticky panels in the 3 weeks of deployment, and provided a snapshot of phenology by instar. We expect that lure-and-kill stations could contribute to the suppression of a delimited population and could be included as part of a semiochemical-based eradication program. Attracting and killing females and nymphs, thus removing future offspring, could contribute to population suppression during an eradication. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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15 pages, 1189 KiB  
Article
Effects of Variety and Grape Berry Condition of Vitis vinifera on Preference Behavior and Performance of Drosophila suzukii
by Lisa Weißinger, Niklas Samuel, Michael Breuer and Caroline Müller
Insects 2019, 10(12), 432; https://doi.org/10.3390/insects10120432 - 30 Nov 2019
Cited by 9 | Viewed by 3278
Abstract
Drosophila suzukii is an invasive fruit pest and represents a potential economic threat to viticulture. After first observations of D. suzukii in Europe in 2008, research mainly focused on the evaluation of the host range and infestation risk for fruit and berry crops. [...] Read more.
Drosophila suzukii is an invasive fruit pest and represents a potential economic threat to viticulture. After first observations of D. suzukii in Europe in 2008, research mainly focused on the evaluation of the host range and infestation risk for fruit and berry crops. However, the risk assessment of D. suzukii in viticulture has only recently started. Understanding the factors influencing preferences of D. suzukii for host species and varieties as well as offspring performance is essential to improve management strategies. We investigated the field infestation of different grape varieties across Baden-Wuerttemberg, southwestern Germany, between 2015 and 2018. Moreover, we performed dual-choice assays in the laboratory to investigate whether adults show preferences for certain varieties and whether offspring performance differs between varieties. Furthermore, we studied the impact of grape damage on choice behavior. Field monitoring revealed that D. suzukii show preferences for red varieties, whereas almost no oviposition occurred in white varieties. The results of dual-choice assays confirmed that D. suzukii preference and performance are influenced by grape variety and that flies preferred damaged over intact “Pinot Noir”, “Pinot Blanc”, and “Müller-Thurgau” berries. Overall, these findings may have important implications for winegrowers regarding cultivated varieties, grape health, and insecticide reduction. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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15 pages, 2166 KiB  
Article
Methyl Salicylate Increases Attraction and Function of Beneficial Arthropods in Cranberries
by Jordano Salamanca, Brígida Souza, Vera Kyryczenko-Roth and Cesar Rodriguez-Saona
Insects 2019, 10(12), 423; https://doi.org/10.3390/insects10120423 - 25 Nov 2019
Cited by 28 | Viewed by 3859
Abstract
Methyl salicylate (MeSA) is an herbivore-induced plant volatile (HIPV) known to attract the natural enemies of herbivores in agro-ecosystems; however, whether this attraction leads to an increase in natural enemy functioning, i.e., predation, remains largely unknown. Here, we monitored for 2 years (2011–2012) [...] Read more.
Methyl salicylate (MeSA) is an herbivore-induced plant volatile (HIPV) known to attract the natural enemies of herbivores in agro-ecosystems; however, whether this attraction leads to an increase in natural enemy functioning, i.e., predation, remains largely unknown. Here, we monitored for 2 years (2011–2012) the response of herbivores and natural enemies to MeSA lures (PredaLure) by using sticky and pitfall traps in cranberry bogs. In addition, European corn borer, Ostrinia nubilalis, egg masses were used to determine whether natural enemy attraction to MeSA leads to higher predation. In both years, MeSA increased adult hoverfly captures on sticky traps and augmented predation of O. nubilalis eggs. However, MeSA also attracted more phytophagous thrips and, in 2012, more plant bugs (Miridae) to sticky traps. Furthermore, we used surveillance cameras to record the identity of natural enemies attracted to MeSA and measure their predation rate. Video recordings showed that MeSA lures increase visitation by adult lady beetles, adult hoverflies, and predatory mites to sentinel eggs, and predation of these eggs doubled compared to no-lure controls. Our data indicate that MeSA lures increase predator attraction, resulting in increased predation; thus, we provide evidence that attraction to HIPVs can increase natural enemy functioning in an agro-ecosystem. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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17 pages, 1977 KiB  
Article
Queen Recognition Signals in Two Primitively Eusocial Halictid Bees: Evolutionary Conservation and Caste-Specific Perception
by Iris Steitz, Katharina Brandt, Felix Biefel, Ädem Minat and Manfred Ayasse
Insects 2019, 10(12), 416; https://doi.org/10.3390/insects10120416 - 21 Nov 2019
Cited by 11 | Viewed by 3008
Abstract
Queen signals are known to regulate reproductive harmony within eusocial colonies by influencing worker behavior and ovarian physiology. However, decades of research have resulted in the identification of just a few queen signals, and studies of their mode of action are rare. Our [...] Read more.
Queen signals are known to regulate reproductive harmony within eusocial colonies by influencing worker behavior and ovarian physiology. However, decades of research have resulted in the identification of just a few queen signals, and studies of their mode of action are rare. Our aim was to identify queen recognition signals in the halictid bee Lasioglossum pauxillum and to analyze caste differences in the olfactory perception of queen signals in L. pauxillum and the closely related species L. malachurum. We performed chemical analyses and bioassays to test for caste differences in chemical profiles and worker behavior influenced by queen-specific compounds in L. pauxillum. Our results indicated that caste differences in the chemical profiles were mainly attributable to higher amounts of macrocyclic lactones in queens. Bioassays demonstrated a higher frequency of subordinate behavior in workers elicited by queen-specific amounts of macrocyclic lactones. Thus, macrocyclic lactones function as queen recognition signals in L. pauxillum, as in L. malachurum. Using electrophysiological analyses, we have demonstrated that queens of both tested species lack antennal reactions to certain macrocyclic lactones. Therefore, we assume that this is a mechanism to prevent reproductive self-inhibition in queens. Our results should stimulate debate on the conservation and mode of action of queen signals. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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21 pages, 4663 KiB  
Article
Characterization of the Expression and Functions of Two Odorant-Binding Proteins of Sitophilus zeamais Motschulsky (Coleoptera: Curculionoidea)
by Ying Zhang, Chen Shen, Daosong Xia, Jian Wang and Qingfeng Tang
Insects 2019, 10(11), 409; https://doi.org/10.3390/insects10110409 - 15 Nov 2019
Cited by 12 | Viewed by 3389
Abstract
Odorant-binding proteins (OBPs) are important in insect chemical communication. The objective of this research was to identify the functions of two OBPs in Sitophilus zeamais. qRT-PCR and western blot (WB) were performed to investigate the expression profiles at the transcript and protein [...] Read more.
Odorant-binding proteins (OBPs) are important in insect chemical communication. The objective of this research was to identify the functions of two OBPs in Sitophilus zeamais. qRT-PCR and western blot (WB) were performed to investigate the expression profiles at the transcript and protein levels, respectively. Fluorescence competitive binding assays were used to measure the ability of the OBPs to bind to host volatiles, and a Y-tube olfactometer was used to verify the results (attraction/no response) via behavioral experiments. The RNAi was used to verify the function by knocking down the ability of proteins to bind odorants. qRT-PCR showed the highest expression SzeaOBP1 and SzeaOBP28 at the low-instar larva (LL) and eclosion adult (EA) stages, respectively. WB showed that both SzeaOBP1 and SzeaOBP28 were highly expressed in the EA stage. Fluorescence competitive binding assays indicated that SzeaOBP1 exhibited extremely high binding affinity with cetanol. SzeaOBP28 exhibited a pronounced binding affinity for 4-hydroxy-3-methoxybenzaldehyde. The behavioral experiment showed that the adult S. zeamais responded strongly to 4-hydroxy-3-methoxybenzaldehyde and valeraldehyde from Sorghum bicolor. The RNAi knockdown individuals displayed behavioral differences between normal insects and dsRNA (SzeaOBP1)-treated insects. We infer that they both have functions in perception and recognition of host volatiles, whereas SzeaOBP28 may also have other functions. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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15 pages, 2449 KiB  
Article
Electrophysiological Responses of Eighteen Species of Insects to Fire Ant Alarm Pheromone
by Yuzhe Du, Michael J. Grodowitz and Jian Chen
Insects 2019, 10(11), 403; https://doi.org/10.3390/insects10110403 - 14 Nov 2019
Cited by 16 | Viewed by 5685
Abstract
Olfaction plays a dominant role in insect communication. Alarm pheromones, which alert other insects of the same species of impending danger, are a major class of releaser pheromones. The major components of alarm pheromones in red imported fire ants, honeybees and aphids have [...] Read more.
Olfaction plays a dominant role in insect communication. Alarm pheromones, which alert other insects of the same species of impending danger, are a major class of releaser pheromones. The major components of alarm pheromones in red imported fire ants, honeybees and aphids have been identified as 2-ethyl-3,6-dimethylpyrazine (2E-3,6-DP), isopentyl acetate (IPA), and E-β-farnesene (EβF), respectively. In this study, electroantennography (EAG) responses to EDP (a mixture of 2-ethyl-3,6-dimethylpyrazine and 2-ethyl-3,5-dimethylpyrazine), IPA and EβF were investigated in a wide range of insect species. Beside imported fire ants, the EDP (2-ethyl-3,6(5)-dimethylpyrazine) elicited significant EAG response from all other tested insects, including six ant species and one hybrid ant, honeybee, bagrada bug, lady beetle, housefly, small hive beetle, yellow fever mosquito, termite, bedbug, water hyacinth weevil, southern green stink bug and two aphid species. In contrast, IPA elicited significant EAG response only in the honeybee, red imported fire ant, an Aphaenogaster ant, and the water hyacinth weevil. The EβF only elicited EAG responses in two aphids, small hive beetle and housefly. The results clearly indicate that EDP can be detected by widespread insect species that did not coevolve with S. invicta and further suggested alkylpyrazine may activate multiple generally tuned olfactory receptors (ORs) across a wide number of insect species. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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13 pages, 51548 KiB  
Article
Recent Advances in Management by Pheromones of Thaumetopoea Moths in Urban Parks and Woodland Recreational Areas
by Pasquale Trematerra and Marco Colacci
Insects 2019, 10(11), 395; https://doi.org/10.3390/insects10110395 - 8 Nov 2019
Cited by 8 | Viewed by 4096
Abstract
Caterpillars of the pine processionary moths, Thaumetopoea complex, cause serious defoliation to Cedrus, Pinus, and Pseudotsuga trees. Thaumetopoea caterpillars also have fine hairs on their abdominal tergites that contain a protein that can severely irritate and cause dermatitis in humans and domestic [...] Read more.
Caterpillars of the pine processionary moths, Thaumetopoea complex, cause serious defoliation to Cedrus, Pinus, and Pseudotsuga trees. Thaumetopoea caterpillars also have fine hairs on their abdominal tergites that contain a protein that can severely irritate and cause dermatitis in humans and domestic animals. The control of the T. pityocampa pine processionary moth has become necessary in many European countries because of the sanitary risks that are related to larval urtication and the defoliation threat to pine forests and plantations. New research activities have been aimed at the development of eco-friendly, innovative technologies for Integrated Pest Management (IPM) of these moths, particularly in urban parks and woodland recreational areas. This paper describes the recent advances in the use of pheromones in monitoring, mass trapping, and mating disruption related to management of processionary moths T. hellenica and T. pityocampa. According to the results, the use of pheromones may provide a practical alternative to insecticide sprays, as they can be safe and simple as compared to other control methods. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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11 pages, 2199 KiB  
Article
Ants Sense, and Follow, Trail Pheromones of Ant Community Members
by Jaime M. Chalissery, Asim Renyard, Regine Gries, Danielle Hoefele, Santosh Kumar Alamsetti and Gerhard Gries
Insects 2019, 10(11), 383; https://doi.org/10.3390/insects10110383 - 1 Nov 2019
Cited by 10 | Viewed by 6694
Abstract
Ants deposit trail pheromones that guide nestmates to food sources. We tested the hypotheses that ant community members (Western carpenter ants, Camponotus modoc; black garden ants, Lasius niger; European fire ants, Myrmica rubra) (1) sense, and follow, each other’s trail [...] Read more.
Ants deposit trail pheromones that guide nestmates to food sources. We tested the hypotheses that ant community members (Western carpenter ants, Camponotus modoc; black garden ants, Lasius niger; European fire ants, Myrmica rubra) (1) sense, and follow, each other’s trail pheromones, and (2) fail to recognize trail pheromones of allopatric ants (pavement ants, Tetramorium caespitum; desert harvester ants, Novomessor albisetosus; Argentine ants, Linepithema humilis). In gas chromatographic-electroantennographic detection analyses of a six-species synthetic trail pheromone blend (6-TPB), La. niger, Ca. modoc, and M. rubra sensed the trail pheromones of all community members and unexpectedly that of T. caespitum. Except for La. niger, all species did not recognize the trail pheromones of N. albisetosus and Li. humilis. In bioassays, La. niger workers followed the 6-TPB trail for longer distances than their own trail pheromone, indicating an additive effect of con- and hetero-specific pheromones on trail-following. Moreover, Ca. modoc workers followed the 6-TPB and their own trail pheromones for similar distances, indicating no adverse effects of heterospecific pheromones on trail-following. Our data show that ant community members eavesdrop on each other’s trail pheromones, and that multiple pheromones can be combined in a lure that guides multiple species of pest ants to lethal food baits. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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15 pages, 7103 KiB  
Article
A Subset of Odorant Receptors from the Desert Locust Schistocerca gregaria Is Co-Expressed with the Sensory Neuron Membrane Protein 1
by Pablo Pregitzer, Xingcong Jiang, René-Sebastian Lemke, Jürgen Krieger, Jörg Fleischer and Heinz Breer
Insects 2019, 10(10), 350; https://doi.org/10.3390/insects10100350 - 17 Oct 2019
Cited by 8 | Viewed by 3454
Abstract
In the desert locust Schistocerca gregaria (S. gregaria), pheromones are considered to be crucial for governing important behaviors and processes, including phase transition, reproduction, aggregation and swarm formation. The receptors mediating pheromone detection in olfactory sensory neurons (OSNs) on the antenna [...] Read more.
In the desert locust Schistocerca gregaria (S. gregaria), pheromones are considered to be crucial for governing important behaviors and processes, including phase transition, reproduction, aggregation and swarm formation. The receptors mediating pheromone detection in olfactory sensory neurons (OSNs) on the antenna of S. gregaria are unknown. Since pheromone receptors in other insects belong to the odorant receptor (OR) family and are typically co-expressed with the “sensory neuron membrane protein 1” (SNMP1), in our search for putative pheromone receptors of S. gregaria, we have screened the OR repertoire for receptor types that are expressed in SNMP1-positive OSNs. Based on phylogenetic analyses, we categorized the 119 ORs of S. gregaria into three groups (I–III) and analyzed a substantial number of ORs for co-expression with SNMP1 by two-color fluorescence in situ hybridization. We have identified 33 ORs that were co-expressed with SNMP1. In fact, the majority of ORs from group I and II were found to be expressed in SNMP1-positive OSNs, but only very few receptors from group III, which comprises approximately 60% of all ORs from S. gregaria, were co-expressed with SNMP1. These findings indicate that numerous ORs from group I and II could be important for pheromone communication. Collectively, we have identified a broad range of candidate pheromone receptors in S. gregaria that are not randomly distributed throughout the OR family but rather segregate into phylogenetically distinct receptor clades. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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14 pages, 2111 KiB  
Article
Sub-Lethal Doses of Clothianidin Inhibit the Conditioning and Biosensory Abilities of the Western Honeybee Apis mellifera
by Merle T. Bartling, Andreas Vilcinskas and Kwang-Zin Lee
Insects 2019, 10(10), 340; https://doi.org/10.3390/insects10100340 - 11 Oct 2019
Cited by 13 | Viewed by 3774
Abstract
Insects play an important role in the stability of ecosystems by fulfilling key functions such as pollination and nutrient cycling, as well as acting as prey for amphibians, reptiles, birds and mammals. The global decline of insects is therefore a cause for concern, [...] Read more.
Insects play an important role in the stability of ecosystems by fulfilling key functions such as pollination and nutrient cycling, as well as acting as prey for amphibians, reptiles, birds and mammals. The global decline of insects is therefore a cause for concern, and the role of chemical pesticides must be examined carefully. The lethal effects of insecticides are well understood, but sub-lethal concentrations have not been studied in sufficient detail. We therefore used the western honeybee Apis mellifera as a model to test the effect of the neonicotinoid insecticide clothianidin on the movement, biosensory abilities and odor-dependent conditioning of insects, titrating from lethal to sub-lethal doses. Bees treated with sub-lethal doses showed no significant movement impairment compared to untreated control bees, but their ability to react to an aversive stimulus was inhibited. These results show that clothianidin is not only highly toxic to honeybees, but can, at lower doses, also disrupt the biosensory capabilities of survivors, probably reducing fitness at the individual level. In our study, sub-lethal doses of clothianidin altered the biosensory abilities of the honeybee; possible consequences at the colony level are discussed. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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10 pages, 679 KiB  
Article
EAG Responses of Adult Lobesia botrana Males and Females Collected from Vitis vinifera and Daphne gnidium to Larval Host-Plant Volatiles and Sex Pheromone
by Alicia Pérez-Aparicio, Luis M. Torres-Vila and César Gemeno
Insects 2019, 10(9), 281; https://doi.org/10.3390/insects10090281 - 2 Sep 2019
Cited by 7 | Viewed by 3264
Abstract
We analysed electroantennogram (EAG) responses of male and female adults of the European grapevine moth Lobesia botrana (Denis et Schiffermüller) (Lepidoptera: Tortricidae) collected as larvae from grapevine (Vitis vinifera L.) and flax-leaved daphne (Daphne gnidium L.). The host-plant odorants tested were [...] Read more.
We analysed electroantennogram (EAG) responses of male and female adults of the European grapevine moth Lobesia botrana (Denis et Schiffermüller) (Lepidoptera: Tortricidae) collected as larvae from grapevine (Vitis vinifera L.) and flax-leaved daphne (Daphne gnidium L.). The host-plant odorants tested were either V. vinifera-specific [1-octen-3-ol, (E)-β-farnesene, (E)-4,8-dimethyl-1,3,7-nonatriene], D. gnidium-specific (2-ethyl-hexan-1-ol, benzothiazole, linalool-oxide, ethyl benzanoate), or were shared by both host-plants (linalool, methyl salicylate). Sex pheromone compounds were also tested. The male response to the major pheromone component (E7,Z9-12:Ac) was higher than to any other stimuli, whereas the response to the minor pheromone components (E7,Z9-12:OH and Z9-12:Ac) was not different from the response to the plant odorants. The female response to pheromone was lower or not different from that to plant odorants. Methyl salicylate elicited a higher response in females and (E)-β-farnesene elicited a higher response than several other plant odorants in both sexes. Non-significant interactions between host-plant odorant and sex indicated an absence of sex specialization for host-plant volatile detection. The lack of a significant interaction between plant volatiles and larval host-plants suggested that there was no specialization for plant-volatile detection between V. vinifera and D. gnidium individuals. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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9 pages, 1308 KiB  
Article
Cuticular Hydrocarbon Recognition in the Mating Behavior of Two Pissodes Species
by Ruixu Chen, Tian Xu, Dejun Hao and Stephen A. Teale
Insects 2019, 10(7), 217; https://doi.org/10.3390/insects10070217 - 23 Jul 2019
Cited by 7 | Viewed by 3861
Abstract
Two sibling weevil species, Pissodes strobi Peck and P. nemorensis Germar (Coleoptera: Curculionidae), can form reduced-fitness hybrids in the laboratory, but neither their premating isolation mechanisms nor mating behaviors are well-understood. Cuticular hydrocarbons (CHCs) have been reported as crucial chemical cues in mating [...] Read more.
Two sibling weevil species, Pissodes strobi Peck and P. nemorensis Germar (Coleoptera: Curculionidae), can form reduced-fitness hybrids in the laboratory, but neither their premating isolation mechanisms nor mating behaviors are well-understood. Cuticular hydrocarbons (CHCs) have been reported as crucial chemical cues in mating recognition in many insects, including weevils, and, thus, may also mediate the mating behavior of P. strobi and P. nemorensis. We conducted a series of behavioral observations, bioassays, and chemical analyses to investigate the role of CHCs in their mating behavior. Copulation behavior of both species followed similar steps: approaching, mounting, tapping, aedeagus extrusion, and copulation. In P. strobi, hexane extraction significantly reduced the number of successful male copulations compared with freeze-killed females. Conversely, significantly fewer P. nemorensis males copulated with dead females compared with live females. No significant differences were detected among hexane-extracted, freeze-killed or recoated female carcasses to P. nemorensis. These findings suggested that female cuticular extracts contain important cues in mate recognition in P. strobi but not in P. nemorensis. We identified 21 CHCs from both species with variation in abundances between sexes and seasons. Discriminant analysis revealed incomplete overlap of CHC compositions in females of the two species in summer, when hybridization potentially occurs. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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16 pages, 11850 KiB  
Article
Parthenogenetic Females of the Stick Insect Clitarchus hookeri Maintain Sexual Traits
by Mari Nakano, Mary Morgan-Richards, A. Jonathan R. Godfrey and Andrea Clavijo McCormick
Insects 2019, 10(7), 202; https://doi.org/10.3390/insects10070202 - 10 Jul 2019
Cited by 9 | Viewed by 7208
Abstract
The New Zealand stick insect Clitarchus hookeri has both sexual and parthenogenetic (all-female) populations. Sexual populations exhibit a scramble competition mating system with distinctive sex roles, where females are signalers and males are searchers, which may lead to differences in the chemical and [...] Read more.
The New Zealand stick insect Clitarchus hookeri has both sexual and parthenogenetic (all-female) populations. Sexual populations exhibit a scramble competition mating system with distinctive sex roles, where females are signalers and males are searchers, which may lead to differences in the chemical and morphological traits between sexes. Evidence from a range of insect species has shown a decay of sexual traits is common in parthenogenetic lineages, especially those traits related to mate attraction and location, presumably due to their high cost. However, in some cases, sexual traits remain functional, either due to the recent evolution of the parthenogenetic lineage, low cost of maintenance, or because there might be an advantage in maintaining them. We measured morphological and chemical traits of C. hookeri to identify differences between males and females and between females from sexual and parthenogenetic populations. We also tested the ability of males to discriminate between sexual and parthenogenetic females in a laboratory bioassay. Our results show that male C. hookeri has morphological traits that facilitate mobility (smaller body with disproportionately longer legs) and mate detection (disproportionately longer antennae), and adult females release significantly higher amounts of volatile organic compounds than males when this species is sexually active, in accordance with their distinctive sex roles. Although some differences were detected between sexual and parthenogenetic females, the latter appear to maintain copulatory behaviors and chemical signaling. Males were unable to distinguish between sexual and parthenogenetic females, suggesting that there has been little decay in the sexual traits in the parthenogenetic lineage of C. hookeri. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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11 pages, 1208 KiB  
Article
Effects of Host Plants Reared under Elevated CO2 Concentrations on the Foraging Behavior of Different Stages of Corn Leaf Aphids Rhopalosiphum maidis
by Yu Chen, Clément Martin, Junior Corneille Fingu Mabola, François Verheggen, Zhenying Wang, KangLai He and Frederic Francis
Insects 2019, 10(6), 182; https://doi.org/10.3390/insects10060182 - 23 Jun 2019
Cited by 12 | Viewed by 3908
Abstract
Climate change is a major environmental concern and is directly related to the increasing concentrations of greenhouse gases. The increase in concentrations of atmospheric carbon dioxide (CO2), not only affects plant growth and development, but also affects the emission of plant [...] Read more.
Climate change is a major environmental concern and is directly related to the increasing concentrations of greenhouse gases. The increase in concentrations of atmospheric carbon dioxide (CO2), not only affects plant growth and development, but also affects the emission of plant organic volatile compounds (VOCs). Changes in the plant odor profile may affect the plant-insect interactions, especially the behavior of herbivorous insects. In this study, we compared the foraging behavior of corn leaf aphid (Rhopalosiphum maidis) on barley (Hordeum vulgare L.) seedlings grown under contrasted CO2 concentrations. During the dual choice bioassays, the winged and wingless aphids were more attracted by the VOCs of barley seedlings cultivated under ambient CO2 concentrations (aCO2; 450 ppm) than barley seedlings cultivated under elevated CO2 concentrations (eCO2; 800 ppm), nymphs were not attracted by the VOCs of eCO2 barley seedlings. Then, volatile compositions from 14-d-old aCO2 and eCO2 barley seedlings were investigated by GC-MS. While 16 VOCs were identified from aCO2 barley seedlings, only 9 VOCs were found from eCO2 barley seedlings. At last, we discussed the potential role of these chemicals observed during choice bioassays. Our findings lay foundation for functional response of corn leaf aphid under climate change through host plant modifications. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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10 pages, 728 KiB  
Article
Chemical Compounds from Female and Male Rectal Pheromone Glands of the Guava Fruit Fly, Bactrocera correcta
by Xiuge Zhang, Chengmei Wei, Jin Miao, Xiaojiao Zhang, Bo Wei, Wenxia Dong and Chun Xiao
Insects 2019, 10(3), 78; https://doi.org/10.3390/insects10030078 - 18 Mar 2019
Cited by 14 | Viewed by 4291
Abstract
The guava fruit fly, Bactrocera correcta, is one of the major pests affecting mango (Mangifera indica) and guava (Psidium guajava) production in China. The compound β-caryophyllene was identified from the rectal gland extracts of wild B. correcta males [...] Read more.
The guava fruit fly, Bactrocera correcta, is one of the major pests affecting mango (Mangifera indica) and guava (Psidium guajava) production in China. The compound β-caryophyllene was identified from the rectal gland extracts of wild B. correcta males and was demonstrated to be a more specific and potent male lure than methyl eugenol (ME) for B. correcta. In order to find potential additional pheromone attractants for the monitoring and mass-trapping of this fruit fly, a series of chemical and behavioral assays were conducted in this study. Ten compounds were identified from the rectal glands of virgin B. correcta females. These compounds consisted of five major compounds (i.e., ethyl dodecanoate, ethyl tetradecanoate, ethyl (E)-9-hexadecenoate, ethyl hexadecanoate, and ethyl (Z)-9-octadecenoate) in high quantities, and other compounds (i.e., octanal, N-(3-methylbutyl) acetamide, (Z)-9-tricosene, ethyl octadecanoate, and ethyl eicosanoate) in trace amounts, while virtually no compounds were found in male rectal glands. The bioassays indicate that female rectal gland extracts are attractive to virgin females and males. Furthermore, a cyclical production of the five major compounds was found, recurring at roughly 10-d intervals with peaks in 10–13-, 25-, and 35-d-old females. Collectively, these results will contribute to the understanding of pheromone communication in B. correcta and may provide important information for improving existing monitoring and control methods for this pest. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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Review

Jump to: Research, Other

30 pages, 4933 KiB  
Review
Bacterial Semiochemicals and Transkingdom Interactions with Insects and Plants
by Matteo Calcagnile, Salvatore Maurizio Tredici, Adelfia Talà and Pietro Alifano
Insects 2019, 10(12), 441; https://doi.org/10.3390/insects10120441 - 8 Dec 2019
Cited by 24 | Viewed by 10871
Abstract
A peculiar feature of all living beings is their capability to communicate. With the discovery of the quorum sensing phenomenon in bioluminescent bacteria in the late 1960s, it became clear that intraspecies and interspecies communications and social behaviors also occur in simple microorganisms [...] Read more.
A peculiar feature of all living beings is their capability to communicate. With the discovery of the quorum sensing phenomenon in bioluminescent bacteria in the late 1960s, it became clear that intraspecies and interspecies communications and social behaviors also occur in simple microorganisms such as bacteria. However, at that time, it was difficult to imagine how such small organisms—invisible to the naked eye—could influence the behavior and wellbeing of the larger, more complex and visible organisms they colonize. Now that we know this information, the challenge is to identify the myriad of bacterial chemical signals and communication networks that regulate the life of what can be defined, in a whole, as a meta-organism. In this review, we described the transkingdom crosstalk between bacteria, insects, and plants from an ecological perspective, providing some paradigmatic examples. Second, we reviewed what is known about the genetic and biochemical bases of the bacterial chemical communication with other organisms and how explore the semiochemical potential of a bacterium can be explored. Finally, we illustrated how bacterial semiochemicals managing the transkingdom communication may be exploited from a biotechnological point of view. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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16 pages, 265 KiB  
Review
A Review of Interactions between Insect Biological Control Agents and Semiochemicals
by Anamika Sharma, Ramandeep Kaur Sandhi and Gadi V. P. Reddy
Insects 2019, 10(12), 439; https://doi.org/10.3390/insects10120439 - 5 Dec 2019
Cited by 47 | Viewed by 8730
Abstract
Biological control agents and semiochemicals have become essential parts of the integrated pest management of insect pests over recent years, as the incorporation of semiochemicals with natural enemies and entomopathogenic microbials has gained significance. The potential of insect pheromones to attract natural enemies [...] Read more.
Biological control agents and semiochemicals have become essential parts of the integrated pest management of insect pests over recent years, as the incorporation of semiochemicals with natural enemies and entomopathogenic microbials has gained significance. The potential of insect pheromones to attract natural enemies has mainly been established under laboratory conditions, while semiochemicals from plants have been used to attract and retain natural enemies in field conditions using strategies such as trap crops and the push–pull mechanism. The best-known semiochemicals are those used for parasitoids–insect pest–plant host systems. Semiochemicals can also aid in the successful dispersal of entomopathogenic microbials. The use of semiochemicals to disseminate microbial pathogens is still at the initial stage, especially for bacterial and viral entomopathogens. Future studies should focus on the integration of semiochemicals into management strategies for insects, for which several semiochemical compounds have already been studied. More effective formulations of microbial agents, such as granular formulations of entomopathogenic fungi (EPFs), along with bio-degradable trap materials, could improve this strategy. Furthermore, more studies to evaluate species-specific tactics may be needed, especially where more than one key pest is present. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
21 pages, 2518 KiB  
Review
Semiochemical and Communication Ecology of the Emerald Ash Borer, Agrilus planipennis (Coleoptera: Buprestidae)
by Peter Silk, Peter Mayo, Krista Ryall and Lucas Roscoe
Insects 2019, 10(10), 323; https://doi.org/10.3390/insects10100323 - 27 Sep 2019
Cited by 16 | Viewed by 4096
Abstract
Knowledge of buprestid chemical ecology is sparse but the appearance of the invasive pest Agrilus planipennis Fairmaire in North America has provided the impetus to study in detail the semiochemistry and ecology of this important buprestid. The macrocyclic lactone (3Z)-12-dodecenolide [(3Z)-lactone] is identified [...] Read more.
Knowledge of buprestid chemical ecology is sparse but the appearance of the invasive pest Agrilus planipennis Fairmaire in North America has provided the impetus to study in detail the semiochemistry and ecology of this important buprestid. The macrocyclic lactone (3Z)-12-dodecenolide [(3Z)-lactone] is identified as a key antennally-active compound that is produced by females and attracts males. Though a weak trap attractant alone, when combined with the host kairomone (3Z)-hexenol and the important visual cue of a green canopy trap, significant increases in male trap capture occur, thus defining (3Z)-lactone as both a sex pheromone of A. planipennis as well as the first and only known buprestid pheromone. The non-natural stereoisomer (3E)-12-dodecenolide and the saturated analog, 12-dodecanolide also exhibit mimetic activities towards male A. planipennis, suggesting a notable plasticity in this pheromonal structural motif. Efficient synthetic routes to these compounds have been developed. A series of fluoro-12-dodecanolides has also been synthesized containing CF2 groups as a strategy to bias the conformational space accessed by these macrolides and to assess if the analogs may act as mimetics for 12-dodecanolide pheromones associated in A. planipennis. These compounds also afford a unique opportunity to study the binding affinities of lactone surrogates with A. planipennis chemosensory proteins and olfactory receptors. Some progress has also been made in identifying the genes involved in the reception, processing and degradation of volatiles in this invasive insect. It is now evident that the behavior and ecology of A. planipennis involves a complex pattern of sensory modalities, including visual, tactile, olfactory and potentially acoustic components. Earlier reviews focused on studies of attractive host volatiles in development of a trapping system for early detection and visual and contact phenomena in A. planipennis mate finding. This review will update the semiochemistry and chemical ecology of A. planipennis and discuss studies on chemistry and behavior that have identified female-produced pheromone components and host kairomones. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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35 pages, 974 KiB  
Review
Tools in the Investigation of Volatile Semiochemicals on Insects: From Sampling to Statistical Analysis
by Ricardo Barbosa-Cornelio, Fernando Cantor, Ericsson Coy-Barrera and Daniel Rodríguez
Insects 2019, 10(8), 241; https://doi.org/10.3390/insects10080241 - 6 Aug 2019
Cited by 24 | Viewed by 9331
Abstract
The recognition of volatile organic compounds (VOCs) involved in insect interactions with plants or other organisms is essential for constructing a holistic comprehension of their role in ecology, from which the implementation of new strategies for pest and disease vector control as well [...] Read more.
The recognition of volatile organic compounds (VOCs) involved in insect interactions with plants or other organisms is essential for constructing a holistic comprehension of their role in ecology, from which the implementation of new strategies for pest and disease vector control as well as the systematic exploitation of pollinators and natural enemies can be developed. In the present paper, some of the general methods employed in this field are examined, focusing on their available technologies. An important part of the investigations conducted in this context begin with VOC collection directly from host organisms, using classical extraction methods, by the employment of adsorption materials used in solid-phase micro extraction (SPME) and direct-contact sorptive extraction (DCSE) and, subsequently, analysis through instrumental analysis techniques such as gas chromatography (GC), nuclear magnetic resonance (NMR) and mass spectrometry (MS), which provide crucial information for determining the chemical identity of volatile metabolites. Behavioral experiments, electroantennography (EAG), and biosensors are then carried out to define the semiochemicals with the best potential for performing relevant functions in ecological relationships. Chemical synthesis of biologically-active VOCs is alternatively performed to scale up the amount to be used in different purposes such as laboratory or field evaluations. Finally, the application of statistical analysis provides tools for drawing conclusions about the type of correlations existing between the diverse experimental variables and data matrices, thus generating models that simplify the interpretation of the biological roles of VOCs. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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Jump to: Research, Review

6 pages, 763 KiB  
Brief Report
Comparison of the Sex Pheromone Composition of Harmonia axyridis Originating from Native and Invaded Areas
by Pauline Legrand, Maryse Vanderplanck and Francois J. Verheggen
Insects 2019, 10(10), 326; https://doi.org/10.3390/insects10100326 - 30 Sep 2019
Cited by 5 | Viewed by 2770
Abstract
The multicolored Asian lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), originates from South-East Asia and is now considered as an invasive species at a worldwide scale, with populations encountered in North and South America, Africa, and Europe. Several previous studies suggested that invasive populations [...] Read more.
The multicolored Asian lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), originates from South-East Asia and is now considered as an invasive species at a worldwide scale, with populations encountered in North and South America, Africa, and Europe. Several previous studies suggested that invasive populations display different behavioral and physiological traits, leading to a better fitness than native individuals. H. axyridis sex pheromone was identified recently, but only from individuals established in Europe. In this study, we compare the composition of the female sex pheromone of H. axyridis from two populations: (i) an invasive population in North America, and (ii) a native population in South-East China. We found the females originating from both populations to release in similar proportions the same five pheromonal compounds, namely β-caryophyllene, β-elemene, methyl-eugenol, α-humulene, and α-bulnesene. However, females from the North American strain release all five compounds in larger amount than the Chinese ones. Whether invasive individuals were selected during the process of invasion through their capacity to better call and find sexual partners remains to be confirmed. Full article
(This article belongs to the Special Issue Semiochemicals and Insect Behavior)
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