key message

  • Triatomines are insects of medical importance as they are vectors of the parasite Trypanosoma cruzi, the aetiological agent of Chagas disease.

  • Knowledge on semiochemicals and hormones affecting triatomine behavior is reviewed; these compounds have a key role in sha** the pathogen-vector-host interaction.

  • Triatomine chemical ecology can be exploited for develo** and implementing real-world vector management programs with proven epidemiological impact, reducing the trasmission of Chagas disease. In this framework, novel research approaches in chemoecology and promising control tools are discussed.

Introduction

Triatomines, also known as kissing bugs, are hematophagous insects from the subfamily Reduviidae (Hemiptera: Heteroptera) (Schofield and Galvão 2009; di Giovanni et al. 2021). Around more than 150 species have been described which are currently distributed in five tribes, i.e. Alberproseniini, Bolboderini, Cavernicolini, Rhodniini and Triatomini. The last two are the most diverse and of medical importance (Justi and Galvão 2017; Ceccarelli et al. 2020), and act as vectors of Trypanosoma cruzi, the etiological agent of the Chagas disease. This illness is of major concern as it affects more than 8 million people, mostly in the Americas for which there is not an effective post-infection treatment (Ceccarelli et al. 2020). The triatomine life cycle is composed by pre-nymph, five nymph stages, and imagos (adults). Nymphs generally occupy the same habitat and feed on the same hosts of the adults (Noireau and Dujardin 2010).

Kissing bug natural history and ecology make them prominent vectors of T. cruzi. These insects inhabit a wide variety of environments, i.e. domestic, peridomestic, and wild habitats, in tropical, subtropical, and temperate areas (Ceccarelli et al. 2020). During the day, kissing bugs remain hidden inside shelters (e.g., cracks and crevices), where they find conspecific presence and key conditions of humidity and temperature (Lazzari 2021). These shelters protect them against predators and extreme abiotic conditions. At night, the insects come out in search of blood sources which comprise a variety of vertebrate hosts, including humans (Noireau and Dujardin 2010). Kissing bug olfaction is fundamental for their day-to-day activities (Latorre-Estivalis et al. 2015). The aptitude of organisms to perceive and transmit information through chemicals is a remarkable aspect of animal biology and ecology (Tirindelli et al. 2009). Chemical ecology examines the role of molecules in the interactions between living organisms and their environment, and it also deals with the consequences of those chemicals on the behaviour and evolution of involved organisms.

Conventional chemical ecology is based on extracting secretions from chemical signal senders, separating extracts into fractions following bioassay-guided protocols (using receivers to assist in the identification of active molecules) (Leal et al. 2008), concluding with the elucidation of chemical structures and in some cases with the chemical synthesis (Leal 2017). Techniques as gas chromatography coupled to mass spectrometry (GC–MS), gas chromatography coupled to infrared spectroscopy and electrophysiology studies [electroantennography (EAG) (May-Concha et al. 2018b), gas chromatography-electroantennography (GC-EAD) (Vitta et al. 2009), and single sensillum recording (SSR) (Campetella et al. 2021)] are routinary used for elucidation of insect infochemicals. A crucial part of the development of infochemicals is shedding light on the potential biological function, which is usually investigated through behavioural assays under laboratory and field conditions (Syed 2015).

Basic knowledge on triatomine chemical ecology has been reviewed earlier (Cruz-López et al. 2001). Recently, other contributions on this topic have been published (Latorre-Estivalis 2022; Lorenzo 2022), mostly focused on Rhodnius prolixus Stål physiology (Barrozo et al. 2017). The aim of the present review is to summarize and discuss current information and recent advances about triatomine chemical ecology, and the development of chemoecology-based monitoring and control tools. Although information in this regard is still fragmented, we believe there is room for both a literature analysis and a future research agenda, the latter highlighting the tight connection between basic chemical ecology research and the implementation of effective and sustainable methods for managing kissing bugs in the Integrated Vector Management (IVM) framework.

Infochemicals and triatomine behaviour

Traditionally, infochemicals have been seen as synonymous with semiochemicals. Notwithstanding, we followed the most recent classification proposed to use the term infochemicals for both hormones and semiochemicals because of their unifying function in information transfer (Supplementary Fig. 1) (Wehrenfennig et al. 2013; Müller et al. 2020). Recently, it has become clear that chemical ecology must deal with the influence of hormones and semiochemicals in the causes and consequences of species interactions, distribution, abundance, and diversity, providing mechanisms to understand ecological interactions and allowing novel vector management options. (Raguso et al. 2015).

Infochemicals, which include hormones and semiochemicals (pheromones and allelochemicals), play a key role in intra- and inter-specific interactions mainly during search for shelter and food, mating, and situations of alarm and threat (Cruz-López et al. 2001). These compounds are released by specialized glands that develop at the adult stage only (Guerenstein and Guerin 2004). The most studied glands are the Brindley (BGs) and metasternal glands (MGs) (Crespo and Manrique 2007; Manrique and Lorenzo 2012). However, it is of remarkable importance to investigate other glands (Santiago et al. 2020). Even though some studies have described the gland morphology for some species, the large variability as well as the lack of descriptions for most species do not allow to reach generalizations in this regard (Lopes et al. 2020). Since the first works on chemical ecology of triatomines, importance was attributed to the glandular system of the bugs (see Cruz-López et al. 2001 and references therein). A confusion emerged about the function of the compounds produced by both MGs and BGs. Moreover, as more data were available, it was clear that while MGs emit compounds that mediate sexual behaviour (Lopes et al. 2020), BGs emit compounds that underlie alarm/defence behaviour (Crespo and Manrique 2007). Apparently both glands are involved during sexual and defensive behaviours. However, detailed studies on different species are still needed (Palottini and Manrique 2016). Notice that these glands are also present in other insects, e.g., wheel bugs (Heteroptera: Reduviidae: Harpactorinae: Arilus), which produce isobutyric acid and other short chain carboxylic acids from BGs (Aldrich et al. 2013). The volatile components of MGs of Megacyllene robiniae (Forster) (Coleoptera: Cerambycidae) males and females contain 2-(1,3-hexadien-1-yl)-5-methyltetrahydrofuran and some esters (Mitchell et al. 2017). Intra-and inter-specific recognition is key for gregarious insects, and kissing bugs make use of cuticular hydrocarbons to achieve such function (Juárez and Fernández 2007; Figueiras et al. 2009). In the same fashion, by using olfaction they can distinguish the sites that serve as refuge (Lazzari 2021), hosts, and food sources (Castillo-Neyra et al. 2015).

Pheromones and cuticular compounds

Sex pheromones

Compared to other insect groups, our knowledge of chemical-mediated sexual behaviour in triatomines is still limited. As a general trend, before mating, triatomine females emit a sexual pheromone from the MGs, and males use these cues to locate the females (Manrique and Lorenzo 2012). Even though there has been evidence of sexual pheromones in triatomines, until recently, a compound or a synthetic mixture that works as a pheromone has been uncovered (Bohman et al. 2018). Most studies have focused on determining the compounds coming from the MGs for some species; Triatoma brasiliensis Neiva (Vitta et al. 2009), Triatoma dimidiata Latreille (May-Concha et al. 2013), Triatoma infestans (Klug) (Manrique et al. 2006), R. prolixus (Bohman et al. 2018), and three species of the Triatoma phyllosoma group (May-Concha et al. 2018a). Volatile oxygenated compounds, such as ketones and alcohols, are present (Table 1). Opposite to what occurs with triatomines, MGs in other insects (e.g., long horned beetles, Coleoptera: Cerambycidae) are involved in terpene and terpenoid production and/or storage and are used for defence (Ohmura et al. 2009).

Table 1 Compounds found in the sexual behaviour of triatomines
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Once copulation starts, a volatile-mediated response takes place by which conspecific males aggregate around the mating couple (Fontan et al. 2002b; Rocha Pires et al. 2004; Pontes et al. 2008; May-Concha et al. 2013). Although little is known about the effect of chiral compounds on kissing bug behaviour, the existence of such molecules in MGs should be highlighted (Unelius et al. 2010), as the bioactivity of pheromones depends on their chirality (Fig. 1a) (Mori 2007). For example, T. infestans and T. brasiliensis produce the (4R, 5R) and (4S, 5S) isomers of 2,2,4-triethyl-5-methyl-1,3-dioxolane as the most abundant compounds (Fig. 1b) (Bohman et al. 2011). Moreover, not all compounds, both chiral and achiral, are antennal active. For example, while T. brasiliensis produces 16 compounds in the MGs, only 5 elicit antennal activity (Vitta et al. 2009). A mixture of 10 compounds from R. prolixus MGs were recently proposed as a synthetic pheromone (Bohman et al. 2018) (Fig. 2). Yet results with other species seem to be contradictory or preliminary. For example, an absence of a sexual pheromone was reported for Triatoma mazzotti Usinger, although these studies have not been conclusive and have not determined the glands’ chemical composition (Rojas et al. 1991). In preliminary studies, it has been showed that terpenoids, as the rose oxides, could affect the sexual communication of triatomines (May-Concha et al. 2018a). However, the chirality of compounds was not elucidated, and only two of the four possible compounds were reported (Fig. 3). Pheromone research has limitations, especially in the identification of compounds, due to the amounts produced by insects. However, with the recent creation of libraries of chiral retention indices of compounds would greatly increase the accuracy and speed of chemical identification for these runs (Alavez-Rosas et al. 2022). More studies are needed to perform a correct chiral identification of triatomine semiochemicals. Further experimental research should be also directed to the influence of pheromone chirality on the sexual behaviour of kissing bugs.

Fig. 1
figure 1

Chirality in triatomines semiochemicals. a 4-methyl-1-heptanol, found in metasternal glands of some species, only the (R)-isomer is found and elicit antennal and behavioural responses. b Chiral dioxolanes found in metasternal glands of some triatomine species (Mori 2007; Bohman et al. 2011)

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Fig. 2
figure 2

Compounds from Rhodnius prolixus females, formulated as a synthetic pheromone (Bohman et al. 2018). (1) 2-Butanone, (2) (S)-2-butanol, (3) 2-Methyl-3-buten-2-ol, (4) 3-Methyl-2-butanol, (5) 2-Methyl-1-butanol, (6) 2-Pentanone, (7) 3-Pentanol, (8) (S)-2-pentanol, (9) (E)-2-Methyl-3-penten-2-ol and (10) 4-Methyl-3-penten-2-ol

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Fig. 3
figure 3

Cis- and trans-Rose oxides (isomers of 4-methyl-2-(2-methylprop-1-en-1-yl)tetrahydro-2H-pyran). Compounds found in the metasternal glands of triatomines of the Triatoma phyllosoma group (May-Concha et al. 2018a)

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Alarm pheromones

When disturbed, adult triatomines (both males and females) release an alarm pheromone emitted by the BGs (Palottini et al. 2014). This leads to a locomotion and escape response by conspecifics (Manrique et al. 2006). Elucidation of BGs components has been carried out for some species of the Phyllosoma complex (May-Concha et al. 2018a), T. infestans (Crespo and Manrique 2007; González et al. 2007), three haplogroups of T. dimidiata (May-Concha et al. 2015), and R. prolixus (Rojas et al. 2002). The pheromone includes volatiles whose combination varies intra-specifically and includes carboxylic acids: isobutyric acid, acetic acid, propanoic acid, butanoic acid, pentanoic acid, hexanoic acid, heptanoic acid, octanoic acid, nonanoic acid, and isovaleric acid (González et al. 2007). Esters and alcohols derived from the above-mentioned acids (González et al. 2007; May-Concha et al. 2015), some ketones (3-methyl-2-hexanone, 2-butanone, 3-pentanone), and other ramified pentanones and hexanones have been also detected (González et al. 2007; May-Concha et al. 2015, 2018a) (Fig. 4). The main component of the pheromone is isobutyric acid, which was the first compound identified and catalogued as an alarm pheromone in species such as T. brasiliensis, T. maculata (Ericsson), T. infestans, T. phyllosoma, Triatoma vitticeps (Stål), Triatoma lecticularia (Stål), R. prolixus and Panstrongylus megistus (Burmeister) (Cruz-López et al. 2001). Interestingly, isobutyric acid bears implications on cognitive roles (i.e. acquiring knowledge through experience) (Minoli et al. 2013b) as well as innate responses (Minoli et al. 2018). Other species possess different compounds that are used in the alarm/defence behaviour, such as in the case of Dipetalogaster maxima (Uhler), which produces 3-methyl-2-hexanone via the MGs (Guerenstein and Guerin 2004).

Fig. 4
figure 4

Compounds found in alarm pheromones of triatomines. The most abundant compound is the isobutyric acid (1), and other minor ketones as 3-methylhexan-2-one (2), 2-butanone (3), 3-pentanone (4), other esters, acids and alcohols (González et al. 2007; May-Concha et al. 2015)

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Aggregation pheromones

Aggregation pheromones play a key role during mate choice, group foraging, and collective gathering near the pheromone source, either by attracting them from a distance (attractant activity) or inducing passing conspecifics to remain at the pheromone source (arrestant activity) (Gries et al. 2014; Mitaka et al. 2020). Related to this, triatomine bugs use different physical and chemical cues to orient towards refuges (Galvez-Marroquin et al. 2018; May-Concha et al. 2020). Triatoma species are attracted to and aggregate around conspecific as well as on heterospecific faeces (Cruz-López et al. 1993; Lorenzo-Figueiras and Lazzari 1998; Pires et al. 2002), footprints (Vitta et al. 2002, 2007; May-Concha et al. 2018c), and cuticular lipids (Figueiras et al. 2009; Cocchiararo-Bastias et al. 2011). However, this was not the case for R. prolixus, which deposit faeces inside the refuges thereby releasing a weak aggregation response by conspecifics (Falvo et al. 2016). Also, other Rhodnius species did not respond to these aggregation signals (Mosquera and Lorenzo 2020). Despite important efforts aimed to look for aggregation signals on triatomine bugs (Cruz-López et al. 1993, 2001; Cruz-López and Morgan 1995; Lorenzo-Figueiras and Lazzari 1998), there is no report of an aggregation pheromone.

Compounds responsible for attraction have also been reported, which are used during control programs (Rojas de Arias et al. 2012). Short chain aldehydes (C6–C10) have been found in faeces or volatiles from aggregated insects that work as attractants of triatomines (Cruz-López et al. 2001; Fontan et al. 2002a; Galvez-Marroquin et al. 2018). Alkanes (C18–C25) have also been found in faeces of T. dimidiata and T. infestans (Galvez-Marroquin et al. 2018), while two quinazolines occurred in faeces of T. infestans, to which nymphs were attracted to (Cruz-López and Morgan 1995; Alzogaray et al. 2005). Other faecal compounds (3-methylbutyric acid, hexanoic acid, 2,3-butanediol, acetic acid and acetamide) function to attract T. infestans, P. megistus, and T. brasiliensis (Fig. 5) (Mota et al. 2014). Lipids (hexadecanoic acid, octadecanoic acid, and octacosanoic acid) and fatty alcohols (eicosanol and docosanol) from the cuticle mediate aggregation in T. infestans (Figueiras et al. 2009; Cocchiararo-Bastias et al. 2011). Different classes of polar compounds are deposited in the faeces of triatomines, yet their function is unclear (Antunes et al. 2013), it is possible that these compounds act as arrestants. Other related aspects also remain unexplored, including (a) the possible origin of the pheromone components, (b) the components associated with the arrestant behaviour, and (c) the mixture of compounds that act as an aggregation pheromone.

Fig. 5
figure 5

Compounds found in the faeces of triatomines that were attractive to conspecifics, usually short-chain aldehydes, long-chain carboxylic acids, alcohols and some aromatics. In some species compounds as 2,3-butanediol (1), acetamide (2), acetic acid (3), hexanoic acid (4), and 3-methylbutyric acid (5) could be found. Polar compounds are usually amino acids or derived products, histamine (6), histidine (7) and proline (8) (Antunes et al. 2013)

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Cuticular compounds (CCs), as signature mixtures in triatomines

As in most insects, CCs have the function of protecting against desiccation (Dulbecco et al. 2020), serve as a barrier to prevent the entry of microorganisms, and participate during chemical communication (Juárez and Fernández 2007). Although a defined role for CCs in triatomine chemical communication is not clear, the profile of compounds varies inter-specifically (Juárez and Blomquist 1993). There are some further differences such as ontogenetic (nymphs vs. adults) and adult sex variation in CCs (Juarez et al. 2001). In T. infestans, CCs promote aggregation and locomotion arrest (Figueiras et al. 2009), and propensity to mate by males. The most abundant CCs are hydrocarbons, fatty alcohols, and free and esterified fatty acids, eicosanol and docosanol are responsible of the attraction of males to females (Cocchiararo-Bastias et al. 2011). It is likely that CCs function as cues or signature mixtures in kissing bugs. Interestingly, CCs are also useful for species identification (e.g., a species complex in T. dimidiata) (Calderon-Fernández et al. 2011).

Allelochemicals

Host location

In triatomines,chemical mechanisms during host search had been less studied than other behaviours (Cruz-López et al. 2001). However, in recent years, robust data have been obtained leading the better understanding of chemical aspects of this process (Guerenstein and Lazzari 2009, 2010; Lazzari 2022). Triatomines use volatiles from hosts (Fig. 6) as these induce a strong antennal response (Campetella et al. 2021) and promote locomotion and exit from roosts (Ferreira et al. 2019). Compounds such as ammonia, isobutylamine, isobutyric acid, heptanal, octanal, nonanal, α-pinene, furane, pyridine, terpinen-4-ol, and other aromatic amines evoke electrophysiological responses in nymphs and adults of T. infestans, R. prolixus and D. maxima (Guerenstein and Lazzari 2009). Odours such as CO2 and ammonia (ubiquitous in vertebrates) are attractive to R. prolixus and have a synergistic combination effect (Otálora-Luna et al. 2004). Some compounds that have been found attractive to T. infestans are heptanal, octanal, nonanal and isobutyric acid, isolated from sheep wool, chicken feathers and rabbit hair (Guerenstein and Guerin 2001). Some volatile amines present as vertebrate waste products are attractive to R. prolixus, T. infestans, and Panstrongylus geniculatus Latreille (Otálora-Luna and Guerin 2014). l-lactic acid synergizes the attractive effect of CO2, while the d-isomer has no biological activity, highlighting the importance of chiral compounds in triatomine attraction (Barrozo and Lazzari 2004). Further, host-borne odours attract T. dimidiata and R. prolixus over short and long distances (Milne et al. 2009); the role of chemical signals from the host stimulates and guides kissing bugs to oviposit (Guidobaldi and Guerenstein 2015).

Fig. 6
figure 6

Antennal active volatiles found in different triatomine hosts. Ammonia (1), carbon dioxide (2), 2-methylpropanamine (3), isobutyric acid (4), terpineol (5), furan (6), pyridine (7), pinene (8) and nonanal (9) (Guerenstein and Lazzari 2009)

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Hormones and their role in triatomines

Hormones are important for species interactions. These molecules mediate the production of allelochemicals, and their expression is influenced by many interspecific interactions (Raguso et al. 2015). The most studied hormone in triatomines, and in many insects, is the juvenile hormone (JH), a sesquiterpenoid hormone (Fig. 7) which regulates both insect metamorphosis and reproduction (Riddiford 2020). Among other functions in triatomines, JH manages lipid storage thereby affecting growth and reproduction (Ramos et al. 2021). JH also regulates production of sex pheromones (Kotaki et al. 2009). It has been speculated that hormones promote a signalling system so that triatomines can start copulation yet the exact mechanisms for this are unknown (Kotaki et al. 2009; Ramos et al. 2021). Another hormone that has a critical role in signalling the way in which triatomines adapt to nutritional conditions is the adipokinetic hormone (AKH) (Gäde and Marco 2022). In insects, the AKHs are 8–10 amino acids long (Fig. 8) (Marco et al. 2022). Recently, using bioinformatics on genes of R. prolixus, a novel mature octapeptide AKH was deduced (Marco et al. 2013). This hormone regulates lipid metabolism and carbohydrate mobilization, allowing them to survive during long fasting periods (Leyria et al. 2021). Understanding how AKH works could led to a strategy to mitigate the dispersal flights of triatomines, thus these insects will not be able to reach new areas and colonize them.

Fig. 7
figure 7

Structures of some natural juvenile hormones, JH III is found in triatomines (Riddiford, 2020)

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Fig. 8
figure 8

pGlu-Leu-Thr-Phe-Ser-Thr-Asp-Trp amide, the sequence of a novel mature octapeptide AKH in some species of triatomines (Marco et al. 2013)

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Reverse chemical ecology of triatomines: a leap forward

Coupled techniques (GC–MS, GC-EAD, and GC-SSR) have reduced analysis to even single individuals in many cases, yet these technniques imply killing the animal (Syed 2015). In the last two decades, with the understanding of the molecular basis of insect olfaction (Liu et al. 2021), an emerging approach has been used to the study of bloodsucking insects semiochemicals, the “reverse chemical ecology” (Supplementary Fig. 2) (Leal et al. 2008; Choo et al. 2018). This is a new term for screening of molecules based on the binding ability of odour binding proteins (OBPs) to test compounds, rather than performing series of behavioural bioassays (Rihani et al. 2021). This approach comprises the in silico study of binding potential between a OBP and a molecule (Kamala et al. 2014). Additional to OBPs, the odorant receptors (ORs) are proteins used to the screening process (Franco et al. 2016). OBPs are involved in the transport of molecules through the sensillum lymph to the olfactory receptor neurons (ORNs) where ORs are embedded (Campetella et al. 2021; Liu et al. 2021). ORs form ion channels with the obligatory odorant receptor coreceptor (ORCO) (Faro de Brito et al. 2016), and infochemicals activating OR-ORCO complexes generate electrical signals that are transmitted to the brain and lead to a behavioural response (Latorre-Estivalis et al. 2015, 2017; Franco et al. 2018) (Supplementary Fig. 3). However, evidence of binding to an OBP or activation of an OR is not sufficient to infer behavioural activity, and it must be confirmed by laboratory and field bioassays (Leal et al. 2008; Choo et al. 2018; Mweresa et al. 2020). Reverse chemical ecology has been applied to triatomines seeking infochemicals of possible applications for monitoring or controlling populations, e.g., silencing the host searching behaviour (Franco et al. 2016) and develo** effective repellents. Using a reverse chemical ecology approach, Franco et al. (2018) accidentally found four good repellents for R. prolixus; the initial goal of the authors was to identify odorant receptor sensitive to putative pheromones receptors. Using an exposure device, the time spent by the insect near to the host in the presence or absence of the compounds tested was quantified. This highlights the importance of behavioural assays in reverse chemical ecology studies. In this scenario, reverse chemical ecology provides molecules that repel triatomines, potentially increasing the number of available repellents for these insects (Sainz et al. 2012; Ramírez et al. 2020). However, this approach is scarcely studied in kissing bugs, most of the studies are centred in basic aspects (characterization of OBPs (Oliveira et al. 2018), proteomic analysis of antennas (Oliveira et al. 2017), and antennal gene expression (Latorre-Estivalis et al. 2022)) and more substantial and robust knowledge of triatomine OBPs, ORs and ORCO are needed for future research (Sparks et al. 2015).

Practical applications

Traps baited with compounds identified in triatomine faces (mostly short-chain aldehydes) have been used to capture triatomines with good results (Lazzari and Lorenzo 2009). In this regard, CO2 has been used successfully (Ryelandt et al. 2011). However, CO2-free baits have also been used in traps with good results in the laboratory (Guidobaldi and Guerenstein 2013, 2016). For post-control surveillance of T. sordida and T. infestans, hexanal, octanal and nonanal have been used in South America (Fig. 9) (Rojas de Arias et al. 2012). Somehow related to this, a key problem to control kissing bugs using insecticides is its aggregation behaviour as this impedes penetration to the insect shelters. To overcome this issue, one may combine insecticide application with a substance that causes bugs to leave their shelters. For this, compounds produced by BGs have been used as “dislodging agents” in triatomine control (Fig. 9) (Minoli et al. 2013a). Reverse chemical ecology-based approach has led to the discovery of repellents for R. prolixus (Franco et al. 2018), and it is leading the new era of “rational infochemicals design”.

Fig. 9
figure 9

Semiochemicals applied in triatomine post-control surveillance along South America. Benzaldehyde (1), hexanal (2), octanal (3) and nonanal (4) (Rojas de Arias et al. 2012). 3-Methylbutanol (5), 3-pentanol (6) and isobutyric acid (7) are effective dislodging agents for triatomines (Minoli et al. 2013a)

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Conclusions and research challenges

Having a robust database of chemical compounds that kissing bugs use to communicate could improve our knowledge and practical application in the control and monitoring of these insects (Tobias and Latorre-Estivalis 2021). Insect chemical ecology research has its limitations, especially in the identification of compounds, due to the amounts produced by insects (Yew and Chung 2015). Techniques as Nuclear Magnetic Resonance (NMR) or X-Ray diffraction are limited in pheromone research yet their integration will facilitate the purification and chemical identification of triatomine pheromones and other infochemicals (Nojima et al. 2011). The emergent techniques used in metabolomics could provide new opportunities to study such ecological relevant signalling molecules (Prince and Pohnert 2010). These techniques facilitate the identification of infochemicals and possibly reducing the need of bioassay-guided fractionation (Kuhlisch and Pohnert 2015). Transcriptomics and proteomics could contribute to the identification of molecules involved in vector–host interactions (Santiago et al. 2020). An unexplored part is the possible influence of T. cruzi parasites on the chemical communication of triatomines. In this regard, the possible influence of the parasite on the production and perception of the compounds has been hypothesized (Córdoba-Aguilar 2020). In support of this, a difference has been shown in the patterns of antennal sensilla between infected and uninfected insects (May-Concha et al. 2021), and circadian cycles (Chacón et al. 2022). Also, fifth instar parasitized nymphs were able to better detect a potential host (Botto-Mahan et al. 2006). These differences may be influenced by the parasite where morphological/behavioural changes in the infected bug may facilitate host detection and, thereby, parasite transmission from the vector to the host (Córdoba-Aguilar 2020). Further studies should test whether communication at the chemical level differs between parasitized and non-parasitized triatomines. In the near future, structures of triatomines will be solved, and we will understand the molecular basis of kissing bug olfaction. Such types of research will open up promising perspectives in triatomine regulation based on the manipulation in chemosensory behaviour (Marchant et al. 2021). With this information, we could design infochemicals for controlling populations of these insects, saving human lives by reducing transmission of the parasite (Leal 2014). The next step in studies of triatomine chemical ecology should be focused on the implementation of Integrated Vector Management (IVM) approaches (Lizzi et al. 2014; Chanda et al. 2017). For example, sex pheromones could be used as baits for traps, in an attraction and kill system (Barrera 2022; Lopes et al. 2022). In this regard, aggregation pheromones could be useful to attract nymphs and both imagoes (female and male) (Bell et al. 2018). Alarm pheromone could be evaluated as dislodgement agents (Minoli et al. 2013a). Knowledge about host-borne compounds (both attractants and repellents) could be used in push–pull strategies (Lorenzo et al. 2014; Wooding et al. 2020). Lastly, the reverse chemical ecology could represent the basis of a new management strategy; indeed, following a rational infochemical design it is possible to develop a species- or instar-selective attractant/repellent products (Olsson et al. 2015).

Author contributions

All authors have made substantial contributions to the following: (i) conception of the study or data collection (DAR, RVA, CAF, MMA, AGC, GB, LC, ACA), (ii) drafting the article and/or revising it critically for important intellectual content (DAR, RVA, CAF, MMA, AGC, GB, LC, ACA), (iii&iv) final approval of the submitted version (DAR, GB, LC, ACA).