Role of pheromones and chemical secretion in bees

Introduction

Communication in bees is a vital aspect of their social organization, enabling them to function as highly efficient and cooperative colonies (Seeley, 1989) [51] . Honeybees rely on a combination of physical and chemical communication mechanisms to coordinate their complex social behaviours. Chemical signals primarily pheromones, play a key role in maintaining colony structure and alarm pheromones alerting workers to threats (Schmidt, Pheromones in honey bees influence olfactory learning and memory by modulating appetitive motivation rather than directly altering odor processing. Geraniol enhances, while 2-heptanone impairs, these cognitive processes through their effects on motivational circuits (Baracchi et al., 2020) [6] . By understanding the chemical communication in bees provides insights into improving beekeeping techniques and conserving bee population.

Effects of the queen signal

Pheromones that cause immediate behavioural response (Releaser effect) in honey bee where mating occurs in specific areas called drone congregation areas (DCAs), where drones gather in anticipation of a queen. The queen releases a potent pheromone 9-ODA (Oxodecanoic acid) which attracts drones from nearby colonies and drones use a combination of olfactory cues and visual orientation to find the queen. Once in flight, drones chase the queen, and multiple matings take place mid-air. After mating, the queen returns to her hive, while the drones die shortly afterward due to the mating process (Mariette et al., 2021) [35] . Retinue behaviour in bees involves worker bees surrounding the queen, attracted by her pheromones like 9-ODA, coniferyl alcohol (CA), and methyl oleate (MO) to care for and attend to her (Carroll et al., 2023) [12] . Swarm clustering is the aggregation of bees into dense, temporary clusters during the swarming process, a natural reproductive behaviour in which a colony divides and a portion of the bees leave with a queen to establish a new colony (Janson et al., 2005) [24] . Another response is Primer effect where it shows long-term changes in physiology or behaviour triggered by chemical signals from the queen (Conte and Hefetz, 2008) [14] . These effects include Queen rearing where the queen pheromones inhibit the development of new queens by suppressing the growth of larvae into queens. These pheromones suppress ovary development in worker bees, preventing them from laying eggs and enhance various worker bee tasks such as comb building, brood feeding, guarding, and foraging (Bortolotti and Costa, 2014) [9] .

Pheromone-secreting glands

Mandibular Gland is situated in the head near the mandibles. In worker bees, this gland secretes compound involved in larval feeding and in the production of alarm pheromones. In queen, these glands are responsible for secreting queen mandibular pheromone (QMP) (Table 1), which plays a critical role in maintaining the colony social structure and inhibiting worker reproduction (Tan et al., 2015) [55] . The biosynthesis pathway of honey bee mandibular gland secretion involves differentially expressed genes with varied expression levels between queen and worker libraries, reflecting their roles in pheromone production (Wu et al., 2017) [62] . Tergal glands are located underneath the abdominal tergites and their ducts open through the cuticle in the tergite posterior edge region. These gland cells in queens are more developed and numerous, aiding in pheromone production, which is crucial for colony regulation (Strachecka et al., 2022) [53] . Dufour's gland is in the sting shaft and is found in queens and workers. Extract contains chemicals that can partially mimic the queen's eggmarking pheromone, reducing the likelihood of worker-laid eggs being removed by the colony (Martin et al., 2005) [36] . The worker repellent pheromone from young virgin queens identified as o-aminoacetophenone causes workers to move away, groom themselves, and stay idle, likely preventing interference in queen fights (Bortolotti and Costa, 2014) [9] . Lopez incera et al. (2021) [31] bees exhibit response to alarm pheromones, increasing aggression with rising concentrations but reducing it at very high levels. This behaviour modeled through Projective Simulation, highlights a balance between reacting to genuine threats and avoiding false alarms, optimizing aggression to prevent unnecessary worker loss, especially in environments with low predator density. Different chemicals secreted by bees that may smell differently to humans such as Isoamyl acetate smell like banana indicates attack, Citral as lemon signals for swarming, heptanone as cheesy smell triggers alarm, and an ODA as undetectable scent from queen bees attracts males. The Nasonov gland is located at the tip of a honey bee abdomen. It releases a pheromone that helps bees orient and gather especially during swarming or when locating the hive (Strachecka et al., 2022) [53] . It also serves as a potential source of death cue (Klett et al., 2021b) [27] The worker footprint pheromone secreted from the tarsal glands on bee feet helps to mark the hive entrance. Honey bees secrete beeswax from abdominal glands to build the hive, while venom from the sting gland serves as a defense mechanism. Brood pheromone is vital sign attracts hygienic workers which detect the non-volatile death cue upon direct contact with the brood (Alison Mcafee, 2017) [4] . Insects detect odors through olfactory receptors in their antennae, which activate cellular cascades and generate action potentials upon binding with odorant molecules (Bortolotti and Costa, 2014) [9] . Ma et al. (2018) [32] observed that both nurse and forager bees detect BP and EBO, with nurses reacting more strongly, and these pheromones act as global signals influencing the entire colony, potentially as parts of a larval needs.

Factors Affecting Pheromone Communication

Impact of pesticides on pheromone production and reception in honey bees and other pollinators is profound. Many pesticides, especially neonicotinoids and organophosphates, interfere with the neurobiological systems of insects, disrupting their ability to synthesize, release, or detect pheromones (Manzoor and Pervez, 2021, Tasman et al., 2021) [34,55] . Exposure to sublethal doses of pesticides has been shown to impair these processes, leading to disorganized colony behavior, reduced foraging efficiency, and even a diminished ability to respond to alarm signals (Bartling et al., 2023) [7] . This disruption in chemical communication weakens colony cohesion and can contribute to colony collapse, as bees fail to perform essential tasks or communicate effectively with one another. Climate change also poses a significant threat to the production and reception of pheromones. Shifts in temperature, humidity, and seasonal patterns affect both the bees and the plants they rely on. Warmer temperature can accelerate the breakdown of pheromone molecules in the environment, shortening their active period and reducing their efficacy (Willmer and Stone, 2004) [60] . Additionally, changes in flowering times and plant-pollinator interactions can lead to misalignment between bees reproductive cycles and the availability of critical resources. The stress caused by extreme weather events, such as heatwaves and droughts, can further affect pheromone production, particularly in queen bees, potentially altering reproductive success and colony health (Przybyla et al., 2021) [44] . Habitat changes including habitat fragmentation, urbanization and agricultural expansion limit the availability of diverse floral resources that are crucial for maintaining bee nutrition and pheromone production. The loss of natural habitats reduces foraging options, which directly affects bees ability to gather the necessary nutrients to support pheromone synthesis (Kendall et al., 2022) [26] . Furthermore, habitat fragmentation can isolate colonies, hindering the exchange of chemical signals between individuals and neighbouring colonies. This isolation weakens genetic diversity and can lead to inbreeding, which further impacts the integrity of pheromone systems (Rodriguez, 2021) [46] . The reduction in floral diversity also impacts the production of specific pheromones linked to foraging and mating behaviors, undermining overall colony resilience.

Applications of Bee Pheromones in Pest Control

Bees themselves are not directly used for pest control, pheromones from bees or bee-related technologies have applications in pest management, particularly in Integrated Pest and Pollinator Management (IPPM) systems (Okosun and Reddy, 2022) [40] . Some pheromones produced by bees, especially alarm pheromones can deter herbivorous pests from damaging crops. when bees perceive a threat, they release an alarm pheromone (like isoamyl acetate) which can signal danger, causing certain pests to avoid those areas. Synthetic pheromones are being used to disrupt the mating patterns of parasitic varroa mites (Varroa destructor) (Ziegelmann and Rosenkranz, 2014) [64] . Queen mandibular pheromone (QMP) significantly suppresses early-stage Nosema ceranae infections, offering potential for improved honey bee disease management (Huang et al., 2024) [23] . Additionally, Braula coeca selects host honey bees using olfactory cues primarily mandibular gland pheromones, favoring workers with higher queen-like pheromone levels. This enhances the lice ability to secure food through trophallaxis (Yusuf et al., 2024) [63] . Pollinators like bees can influence the foraging behavior of natural enemies (parasitic wasps) by interacting with the ecosystem chemical signals. Bee foraging activity or pheromone release might indirectly attract beneficial insects that control pests (Pickett et al., 2012) [43] . Synthetic pheromones can be designed to mimic those of pollinators like bees to create pheromone traps for monitoring or mass trapping of pest insects. These traps help reduce pest populations by disrupting mating or catching pests before they can harm crops. The presence of pollinators and the pheromones they release can trigger indirect plant defense mechanisms, such as increased volatile emissions that attract pest predators, helping to naturally reduce pest populations (Bezerra et al., 2021) [8] .

Role of pheromones in Hive Hygiene and Disease Resistance

Pheromones are essential for maintaining hive hygiene and promoting disease resistance in honey bee colonies. One of the most important examples is brood pheromones, which are released by larvae and pupae. These pheromones communicate the health status of developing bees to worker bees. When workers detect abnormal brood pheromones, indicating disease or infection, they perform hygienic behaviors such as uncapping cells and removing infected or dead larvae and pupae (Spivak and Gilliam, 1998) [52] . This targeted removal of unhealthy brood helps prevent the spread of diseases like American Foulbrood (AFB) or chalkbrood, making it a key defense mechanism in hive hygiene (Owen et al., 2023) [41] . E-b-ocimene accelerates the behavioral maturation of worker bees, promoting early foraging to optimize food collection and brood care. It also inhibits worker ovary development, maintaining social harmony and productivity within the hive (Maisonnasse et al., 2010) [3] . Queen pheromones particularly the queen mandibular pheromone (QMP), also play a significant role in disease resistance by maintaining colony harmony and encouraging worker bees to engage in hygiene-related tasks. QMP suppresses the development of egg-laying workers, ensuring that the queen remains the sole reproductive individual. This stability allows worker bees to focus on maintaining the health of the colony, including cleaning tasks, brood care, and disease prevention (Hefetz, 2019) [19] . A strong queen with healthy pheromone production can enhance the overall cleanliness of the hive, reducing the likelihood of pathogen outbreaks.

Role in Colony Defense

Bees particularly honeybees (Apis mellifera) use pheromones to coordinate their defense response and aggression toward intruders. Bees use pheromones particularly alarm pheromones to coordinate defense and aggressive responses toward intruders (Nouvian et al., 2016) [39] . When a bee senses a threat, it releases these chemical signals to alert and mobilize the rest of the colony. The main pheromone involved in this process is isopentyl acetate (IPA), which is released from the sting gland when a bee stings (Gong et al., 2017) [17] . This pheromone signals nearby bees to become more aggressive and directs them to the source of the threat. Alongside IPA, 2-heptanone, another pheromone released from the mandibular glands which helps reinforce the alert in close proximity to the intruder (Schorkopf et al., 2009) [49] . These pheromones trigger a coordinated attack, with bees rushing toward the threat and stinging it to neutralize the danger. Guard bees stationed at the hive entrance are particularly sensitive to alarm pheromones and play a critical role in initiating the colony defense. When alarm pheromones are detected, guard bees become more vigilant and aggressive, while foragers and other worker bees are also recruited for defense (Nouvian et al., 2016) [39] . This pheromone-driven coordination ensures that the entire hive can rapidly respond to threats. The aggressive response is modulated based on factors like the colony's strength and the bees age, with older bees typically being more responsive (Kastberger et al., 2009) [25] . These chemical communication systems allow bees to work collectively to protect their hive, providing an evolutionary advantage by quickly neutralizing predators or intruders. [12] ; Walsh et al., 2020 [58] Brood Pheromone Ethyl linoleate Methyl linolenate Methyl oleate Stimulates workers to feed larvae, regulate brood care, and modulate foraging behavior Hu JingHua et al., 2018 [21] Nasonov Pheromone Geraniol Citral (neral and geranial) Nerol Farnesol

Used for orientation and recruitment of workers during swarming or foraging Adams, 2014 [2] ; Deshpande and Naik, 2016) [16] . Footprint pheromone or Trail pheromone alkanes, alkenes, alcohols, organic acids, ethers, esters and aldehydes to mark paths and guide others toward food sources or nesting sites Lensky et al., 1987 [30] Alarm Pheromone

Isoamyl acetate 2-heptanone Octyl acetate Benzyl acetate

Released by guard bees to signal danger and attract other bees to defend the hive Costa et al., 1996 [15] Collins and Blum, 1982 [13] .

Alkanes Alkenes Esters

Involved in nestmate recognition and marking the brood cells Wheeler et al., 1985 [59] worker repellent pheromone o-aminoacetophenone Released from young virgin queens which causes workers to stay away, prevent groom interference in queen fights Bortolotti and Costa, 2014 [9] Retinue Pheromone Coniferyl alcohol (CA) Methyl oleate (MO) (E)-9-oxodec-2-enoic acid Draws workers to attend the queen, enhancing her grooming and feeding Lan Keeling, 2001 [29] Drone Attractant Pheromone 9-ODA (also in QMP) 9-HDA Attracts drones to the queen during mating flights.

Villar and Grozinger, 2017 [57] Egg Marking Pheromone Hydrocarbons such as alkanes and alkenes Allows worker bees todistinguish between queen-laid and worker-laid eggs Ayasse et al., 1999 [5] Wax secretion Hydrocarbons, Palmitic acid, oleic acid, and myristic acid. Myricyl palmitate, 1-Triacontanol and octacosanol

Beeswax gives its strength, flexibility, and hydrophobic properties essential for honeycomb construction. Buchwald et al., 2009 [10] Venom secretion Mellitin, secapin, apamin, tertiapin, adolapin Cause pain, defend against microbes, and modulate nerve and muscle activity during defense.

Abd El-Wahed et al., 2019 [1] Techniques to detect pheromones from bees Detecting bee pheromones require sensitive techniques with Gas Chromatography-Mass Spectrometry (GC-MS) being one of the most used methods. It separates and identifies chemical compounds with high accuracy, though it is slow for real-time monitoring (Hites, 1997) [20] . Another method Electroantennography (EAG), measures the electrical response of a bee antenna to pheromones, providing realtime data specific to what bees can detect, but not quantifying pheromones in the environment (Mas et al., 2020) [37] . Solid-Phase Microextraction (SPME) paired with GC-MS is non-invasive and ideal for field studies, collecting airborne pheromones, though it's less precise in real-time (Wilson et al., 2018) [61] . Artificial Neural Networks (ANNs) handle large datasets from methods like GC-MS or EAG to classify pheromones, although they need extensive training data (Butcher et al., 2013) [11] . Electronic noses (e-Noses), which mimic the olfactory system, provide real-time detection but can be sensitive to environmental conditions (Hu et al., 2019) [22] . An olfactometer is an essential tool for studying how bees respond to pheromones, which are critical for their communication and social organization. This device allows to create controlled environments where bees can be exposed to specific odors while their behaviors are observed and recorded. [42,45] .

Conclusion

Pheromones play a crucial role in honeybee colony functioning, affecting reproductive control, foraging, defense, and communication. External factors like pesticides and climate change significantly impact pheromone production and reception, potentially leading to colony collapse. Understanding these chemical signals opens opportunities for enhancing pest control and disease management in beekeeping.

Future thrust

Bees rely on a complex communication system, primarily through pheromones, to coordinate activities such as foraging and responding to threats.

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