Insects’ perception and behavioral responses to plant semiochemicals

Plant hormones

Plant hormones are crucial in controlling various developmental processes and stress response pathways, enabling plants to adapt to a variety of environmental challenges, from living organisms to physical conditions (Bari & Jones, 2009; Hu et al., 2024). Plant hormones, such as jasmonic acid and salicylic acid, play crucial roles in regulating plant responses to insect herbivory. These hormones can induce the production of defense compounds and signaling molecules in response to herbivore attacks. Plant hormone signaling pathways are intricately connected and influenced by a complex network of defense and developmental processes. Understanding how plants integrate multiple hormonal signals in response to various environmental and developmental cues is a significant challenge. It is crucial to recognize that the nature and response of plant interactions with stressors vary depending on the specific plant-pathogen system, timing, hormone concentration, and tissue location (Bari & Jones, 2009). Future research on plant hormones and insect-plant interactions should focus on deciphering hormone roles in defense responses, elucidating molecular mechanisms, engineering defense responses, developing diagnostic tools, and investigating tritrophic interactions. This will advance our understanding of plant-insect interactions and inform the development of novel pest management strategies.

Allelochemicals

These are chemicals produced by plants that influence the growth, survival, or behavior of other organisms, often acting as defense mechanisms against herbivores, pathogens, or competing plants. There are also herbivore-induced plant volatiles which are released by plants in response to phytophagous damage, serving as a warning signal to nearby plants and attracting natural enemies of the phytophagous insects for biological control. These includes terpenes, green leaf volatiles, benzyl acetones and others. There are various types of plant allelochemicals, each with different effects on target organisms. These are basically categorized into (i) kairomones: that benefits the receiver but not the emitter whereas (ii) allomones: benefit emitter/producer only and (iii) synomones: that support both the producer and the beneficiary (Kost, 2008; Mweresa et al., 2020). For example, flowers produce floral scents that attract pollinators, such as bees and butterflies, benefiting both the plant (through pollination) and the pollinator (through nectar as a food source). Pest-infested plants may produce volatiles to attract natural enemies of the same pest in what is termed “a cry for help” (Dicke et al., 2009; Hung et al., 2015). The study on allelochemicals has revealed complex interactions between plants and insects. Despite progress in understanding allelochemicals and its role in insect-plant interactions, several areas remain underexplored. These include mechanisms of perception, chemical synthesis and degradation, long-term effects, multiple stressors, co-evolution, cross-species interactions, microbial mediation, behavioral adaptations, and economic and social implications.

Phytochemicals

Phytochemicals are a class of constitutive metabolites, which play a crucial role in the survival and proper functioning of plants. These bioactive compounds are produced by plants to overcome environmental stress and regulate essential physiological processes, including growth and reproduction (Molyneux et al., 2007). They are found in various plant tissues, including stems, leaves, roots, seeds, fruits, and flowers, with many being concentrated in the outer layers of plant tissues (King & Young, 1999; Rabizadeh et al., 2022). Phytochemicals can be categorized into primary and secondary metabolites based on their function in plant metabolism. Primary metabolites are essential for plant life and include carbohydrates, amino acids, proteins, lipids, purines, and pyrimidines of nucleic acids. They are the fundamental building blocks of plant growth and development, and play a pivotal role in plant defense against insect herbivores. During an insect attack, primary metabolites such as carbohydrates and amino acids are mobilized and redirected within the plant to provide substrates for local defense responses. The import of systemic resources from other parts of the plant can also occur, enabling the production of defense-related compounds. These compounds, including cinnamic acid and phenolic glycosides, contribute to the plant’s defense against insect herbivores (Zhou et al., 2015).

Secondary metabolites are produced through metabolic pathways derived from primary metabolic pathways, and they function as defense compounds, providing protection against herbivores and pathogens. Additionally, these secondary metabolites act as signal compounds, attracting pollinators and seed dispersers to facilitate the plant’s reproductive processes (Hussein & El-Anssary, 2019; Divekar et al., 2022; Wink, 2003). Secondary metabolites are classified into three main groups based on their biosynthetic pathway: nitrogen-containing compounds (e.g., alkaloids, glucosinolates, and cyanogenic glycosides), phenolic compounds (e.g., phenylpropanoids and flavonoids), and terpenes (Jamwal, Bhattacharya & Puri, 2018; Jan et al., 2021). Alkaloids are a class of nitrogen-containing compounds that are produced in response to environmental stimuli and exhibit remarkable biological activities and structural diversity (Ng, Or & Ip, 2015; Takooree et al., 2019). Alkaloids play a crucial role in plant defense, serving as a natural deterrent against herbivorous insects and pathogens. These compounds possess toxic properties that render them unpalatable or even deadly to these organisms, thereby impeding their ability to feed on or infect the plant. Additionally, alkaloids can repel pests such as aphids, whiteflies, and other insects that feed on plant tissues, providing an additional layer of protection against damage and disease.

Glucosinolates, a class of compounds mainly found in the Brassicaceae family, play a crucial role in insect-plant interaction. These compounds are synthesized in plant cells and stored in various plant tissues. They can serve as attractants for beneficial insects such as bees and butterflies (Giamoustaris & Mithen, 1996). Notably, over 25 insect species from the Coleoptera, Lepidoptera, and Diptera orders have been found to be attracted to and utilize glucosinolates as a primary resource (Hopkins, Van Dam & Van Loon, 2009). Furthermore, researchers have discovered that glucosinolates have a profound impact on a broad range of generalist herbivores, deterring them from feeding on the plant and providing a natural defense against herbivory (Hopkins, Van Dam & Van Loon, 2009; Kos et al., 2012). Cyanogenic glycosides are amino acid-derived plant compounds that exhibit widespread distribution across over 100 families of flowering plants (Francisco & Pinotti, 2000; Rabizadeh et al., 2022). In particular, cyanogenic glycosides serve as a deterrent to herbivores by releasing HCN, which is toxic to these insects and thereby helps protect the plant from damage caused by herbivory (Nyirenda, 2020). This defense mechanism is crucial for the survival of plants, allowing them to adapt to their environment and compete with other organisms for resources.

Phenolic compounds are a crucial component of plant defense responses, playing a vital role in the production of phytoalexins, which are toxic compounds that help plants resist pathogens and insects. These compounds serve as antimicrobial and antioxidant agents, enabling plants to evade pathogenic infections and protect major tissues from damage. The biosynthesis of phenolic compounds occurs through various pathways, including the shikimate, pentose phosphate, and phenylpropanoid pathways (Lin et al., 2016; Pratyusha, 2022). The phenolic compound family encompasses a range of substances, including flavonoids, phytoalexins, curcumin, resveratrol, epigallocatechin-3-gallate, and others (Kennedy & Wightman, 2011).

Terpenoids are the most abundant group of plant secondary metabolites produced in flowers, vegetative tissues, and roots (Dudareva, Pichersky & Gershenzon, 2004). Terpenoids play a crucial role in plant-insect interactions, serving as chemical mediators that facilitate communication between plants and insects. These compounds can serve as defense mechanisms against herbivorous insects, acting as repellents to deter them from feeding on the plant or attracting predators that feed on the herbivores. Additionally, terpenoids can be induced to be emitted as volatile organic compounds in response to insect attack, attracting predators or parasitoids that feed on the herbivores and providing indirect defense against the herbivores. Furthermore, terpenoids can act as attractants for beneficial insects, such as pollinators and predators, which can help plants defend against herbivores. Moreover, they can facilitate communication between plants and insects, allowing plants to send signals to insects about the presence of herbivores or other threats (Boncan et al., 2020; Sharma, Anand & Kapoor, 2017). Although significant advancements have been made in elucidating the complex interactions between phytochemicals and insects, several aspects of this relationship remain underserved by existing research. Specifically, the impact of phytochemicals on insect microbiome, social behavior, developmental biology, migratory patterns, population dynamics, human-insect interactions, plant-soil interactions, and climate-induced changes has yet to be comprehensively explored.

Root exudates

Plant roots secrete a complex mixture of molecules known as root exudates, which are composed of thousands of different substances, including organic acids, amino acids, fatty acids, sugars, mucilage, phenolics, proteins, and more (Bais et al., 2006; Dennis, Miller & Hirsch, 2010; Steeghs et al., 2004). Several signaling chemicals have been identified, including ethylene, strigolactones (SLs), jasmonic acid (JA), (-)-loliolide, and allantoin (Wang et al., 2021). These root-secreted signaling chemicals play a crucial role in insect-plant interactions and defense against insect herbivores. Ethylene is a classical phytohormone that responds to plant neighbors, herbivores, pathogens, or other attackers (Baldwin et al., 2006; Farmer, 2001), while JA is a common signaling chemical that elicits the production of defensive metabolites in plants against feeding herbivores or plant competitors (Kong et al., 2018; Martínez-Medina et al., 2017). (-)-Loliolide, a carotenoid metabolite, has been found to be the most ubiquitous monoterpenoid lactone in plant families (Grabarczyk et al., 2015) and may act as a signaling chemical in plant defenses against pathogens (Pan et al., 2009) and herbivores (Murata et al., 2019).

Root exudates have been shown to play a crucial role in plant defense against insect herbivores by producing chemical signals that attract predators or parasitoids that feed on herbivores, thereby providing indirect defense (Khashiu Rahman, Zhou & Wu, 2019). Additionally, root exudates can stimulate the emission of volatile organic compounds, which attract beneficial insects or repel herbivores, while also influencing the composition of the rhizosphere microbiome and its impact on plant defense. Furthermore, root exudates facilitate plant-microbe interactions, enabling microorganisms to produce compounds that are toxic to herbivores or enhance plant defense mechanisms. Finally, root exudates can contain species-specific signals that convey information about local conditions and influence plant defense against insect herbivores. Despite advances in the study of root exudate, the key aspects remain poorly understood. The chemical composition, timing, and spatial distribution of exudates, as well as insect detection mechanisms have not been thoroughly investigated. Microbial influences on exudate chemistry and functional significance of interactions are also unknown. To advance knowledge, interdisciplinary research is needed to address these gaps and integrate expertise from plant physiology, ecology, entomology, microbiology, and analytical chemistry.

Environmental factors influencing plant odor emission and insect orientation

Plant odors, referred to as ’volatile packages’, contain behaviorally important compounds and can be influenced by several biotic and abiotic factors. Biotic factors include presence of herbivores, microbial interactions and competition with neighboring plants, while abiotic factors are temperature, light, humidity, wind speed and direction (Reinecke & Hilker, 2014). The diversity of plant species in a particular habitat can impact how insects locate resources by affecting the filtering of volatile compounds that indicate the presence of resources from a complex background of odors (Randlkofer et al., 2010). For example, insects like bark beetles may avoid volatiles emitted by plants that are not suitable hosts when searching for appropriate hosts (Zhang & Schlyter, 2004). However, the overall odor of the habitat can also play a role in guiding insects towards key volatiles, with plant odors potentially masking the scent of host plants and influencing orientation. The structure of vegetation, including the number and size of plants, can impact how odors spread and how insects navigate towards them (Randlkofer et al., 2010).

Plant odors can resemble pheromone plumes in terms of containing behaviorally important compounds in varying sizes and quantities (Beyaert & Hilker, 2014). The quality and quantity of plant odors can be influenced by biotic factors such as pathogens and herbivores. Changes in plant odors induced by stress, such as herbivory or egg deposition, can be observed in both leaf and root emissions (Hilker & Meiners, 2010). Additionally, the scent of floral parts of a plant can change in response to factors like pollination. The ways in which insects respond to plant odors can vary based on the specific characteristics of the insect perceiving the scent. This adaptability in insects’ responses to plant odors highlights their ability to adjust to changes in their environment. While significant research has been conducted on the relationship between environmental factors and plant odor emission and insect orientation, several gaps remain unclear. These include the effects of high-altitude and high-latitude environments, desert and arid ecosystems, urban pollution, and the interactions between multiple environmental factors. Long-term studies and species-specific responses also needs further investigation to comprehensively understand these complex relationships.

The influences of experience on insects’ behavior and responses to plant odors

The sensory and olfactory recognition of host plants in insects is influenced by their past experiences, enabling them to link scents with either beneficial resources or negative consequences (Gupta & Stopfer, 2011). While previously believed to be primarily essential for insects with diverse diets, the ability to associate plant odors is also critical for insects that specialize in feeding on specific plant species. The impact of odor encounters on insect behavior can manifest rapidly or persist over extended periods (Gupta & Stopfer, 2011). According to the Hopkins host selection principle, insects tend to prefer the odors of host plants they encountered during their larval stage once they reach adulthood (Schoonhoven, Van Loon & Dicke, 2005), although the transferability of this preference across developmental stages is a subject of debate. Conversely, the Neo-Hopkins host selection principle suggests that odors experienced post-pupal stage can influence adult preferences. Recent research indicates that experiences during the larval stage can affect the adult insects’ responses to odors (Blackiston, Casey & Weiss, 2008). The impact of experience on insects’ behavioral responses to plant odors has been extensively investigated. However, several aspects like individual variability in plasticity, long-term effects, interactions between sensory modalities, and the evolutionary pressures shaping experience-dependent plasticity require further exploration to fully understand its mechanisms and implications.

Sick insects and their responses to plant odor

Infection of insects by entomopathogens or infestation by parasites can induce changes in their phenotype, potentially impacting their olfactory responses. For instance, Mallon, Brockmann & Schmid-hempel (2003) found that honey bees exhibited reduced odor learning abilities following immune challenge, and Schütte et al. (2008) observed decreased attraction of the predatory mite Phytoseiulus persimilis Athias-Henriot (1957) to plant volatiles when infected. Another study showed that, infection with bacteria and fungi can lead to changes in gene expression of odor-binding proteins in Anopheles gambiae mosquitoes (Aguilar et al., 2005). Infection with the bacterium Wolbachia sp. has been shown to influence insect behavior and fitness (Werren, Baldo & Clark, 2008), while Peng & Wang (2009), Vosshall & Hansson (2011) demonstrated that Wolbachia sp. infection can change olfactory behavior and gene expression in Drosophila flies. Parasitization of Manduca sexta Linnaeus (1763) larvae by a wasp Cotesia glomerata Linnaeus (1758) was found to impact larval mobility and levels of octopamine (Adamo, 2002). Elevated octopamine levels have been linked to increased pheromone sensitivity in moths and altered responses to non-pheromonal compounds in Periplaneta americana Linnaeus (1758) (Zhukovskaya, 2012). Despite the considerable research on how pathogens and parasites influence insect behavior, the underlying mechanisms driving changes in olfactory responses remain poorly understood (Baverstock, Roy & Pell, 2010). Furthermore, several areas like the chemical signals exchanged between sick insects and plants, and the impact of climate change on sick insect-plant interactions remain underexplored. Thus, further research is needed to elucidate the complex relationships between insects, plants, and diseases and inform sustainable pest management strategies.

The Influence of Age on insects’ responses to plant odor

Insects change their response to plant odors based on their age, as demonstrated by Devaud et al. (2003), in their study on Drosophila melanogaster Meigen (1830). They found that the behavioral response to benzaldehyde decreases with age, correlated with structural changes in the antennal lobe. These changes could be influenced by accumulated experiences and age-related hormone fluctuations. The attractiveness of a volatile compound is not solely determined by its chemical composition; rather, it can be influenced by factors such as the individual’s physiological condition (e.g., age, hormonal or mating status) and environmental conditions. For instance, in moths and locusts, behavioral responses to pheromones were altered by age and juvenile hormone levels (Anton, Dufour & Gadenne, 2007). While there is a significant body of research on insects’ responses to plant odors, there are still many aspects that have not been thoroughly studied, particularly in the context of age. For example, the mechanisms by which older insects perceive and interpret plant odors, as well as the distinct responses of different developmental stages (such as larvae, pupae, and adults) to these odors have not been fully elucidated. Furthermore, the responses of various insect species to plant odors throughout their lifespan, as well as the impact of environmental factors such as temperature and humidity on these responses, remain largely unexplored. Finally, the molecular mechanisms underlying changes in insect responses to plant odors across their lifespan have not been fully elucidated, and practical applications of this knowledge in pest management, conservation, and agriculture are yet to be explored.

Modifying responses to plant odor based on needs

The perception of plant odors by insects is significantly influenced by hunger and mating. When parasitoid wasps are hungry, they show a preference for the odors of flowers that serve as food sources, while fed wasps favor odors from leaves infested with host larvae for choosing oviposition sites (Uefune et al., 2013). Similarly, starved Colorado potato beetles and Western flower thrips exhibit heightened olfactory responses (Davidson, Butler & Teulon, 2006). In the case of starved Drosophila melanogaster flies, increased success in locating food sources is linked to neuropeptides and insulin signaling. Mating triggers a change in olfactory preferences in female moths, potentially guiding them towards suitable oviposition sites. Mating influences the sensitivity of central olfactory neurons, with neuromodulators like biogenic amines, neuropeptides, and hormones potentially playing a role in these alterations. In the fruit fly, Ceratitis capitata Wiedemann (1824) , females’ attraction to male-produced pheromone changes behaviorally after mating: mated females shift from being attracted to the sex pheromone to being attracted to plant odors (Anton, Dufour & Gadenne, 2007; Jang, 1995).These shifts in response to plant odors may involve modifications in central olfactory neurons and sensitivity of antennae (Saveer et al., 2012).

Discrimination of odor stimuli

Insects have separate pathways for processing pheromone and non-pheromone olfactory stimuli, which allows for functional partitioning (Leal, 2013; Mweresa et al., 2020). This differentiation is facilitated by the differences in structure, function, and location of odor and pheromone binding proteins in the antennae and labial palps. In terms of glomerular activation patterns, odor stimuli are categorized based on their temporal and spatial characteristics (Mweresa et al., 2020). Many insects, like moths, tsetse flies, and mosquitoes, exhibit a flight or walking response towards the source of intermittent odor flow. The composition, concentration, and ratio of synthetic and natural odor blends are crucial in determining the selective detection and behavioral responses of insects to semiochemicals (Grünbaum & Willis, 2015). Selectivity at the neural level depends on various factors such as compound length, position of double bonds, and types and positions of functional groups (Galizia & Rössler, 2010). The speed of air flow and temporal dynamics of odor stimulation also significantly influence odor representation (Grünbaum & Willis, 2015). Understanding the dynamics involved in discriminating semiochemical stimuli is important for selecting and optimizing potentially behaviorally active compounds, which can be used to manipulate specific insect species (Reisenman, Lei & Guerenstein, 2016; Watentena, Amos Watentena & Ikem Okoye, 2019). These compounds may have the potential to develop novel attractant or repellent blends for insect control purposes.