Published online January 21, 2022
Journal of Ecology and Environment (2022) 46:03
© The Ecological Society of Korea.
1Department of Plant Medicals, Andong National University, Andong 36729, Republic of Korea
2Department of Pharmaceutical Chemistry and Pharmacognosy, School of Pharmacy, Addis Ababa University, Addis Ababa P.O. Box 1166, Ethiopia
3Agriculture Science and Technology Research Institute, Andong National University, Andong 36729, Republic of Korea
Correspondence to:Daniel Bisrat
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Background: Bees and flowering plants associations were initially began during the early Cretaceous, 120 million years ago. This coexistence has led to a mutual relationship where the plant serves as food and in return, the bee help them their reproduction. Animals pollinate about 75% of food crops worldwide, with bees as the world’s primary pollinator. In general, bees rely on flower scents to locate blooming flowers as visual clue is limited and also their host plants from a distance. In this review, an attempt is made to collect some relevant 107 published papers from three scientific databases, Google Scholar, Scopus, and Web of Science database, covering the period from 1959 to 2021.
Results: Flowering plants are well documented to actively emit volatile organic compounds (VOCs). However, only a few of them are important for eliciting behavioral responses in bees. In this review, fifty-three volatile organic compounds belonging to different class of compounds, mainly terpenoids, benzenoids, and volatile fatty acid derivatives, is compiled here from floral scents that are responsible for eliciting behavioral responses in bees. Bees generally use honest floral signals to locate their host plants with nectar and pollen-rich flowers. Thus, honest signaling mechanism plays a key role in maintaining mutualistic plant?pollinator associations.
Conclusions: Considering the fact that floral scents are the primary attractants, understanding and identification of VOCs from floral scent in plant-pollinator networks are crucial to improve crop pollination. Interestingly, current advances in both VOCs scent gene identification and their biosynthetic pathways make it possible to manipulate particular VOCs in plant, and this eventually may lead to increase in crop productivity.
Keywords: flowering plant, pollination, bees, flower scent, honest floral signal
Animal pollinators are responsible for aiding over 80% of the world’s flowering plants to reproduce, including 75% of all crops, and about 35% of the world’s food crop (Klein et al. 2007; Potts et al. 2016). Among them, bees (Hymenoptera, Apoidea), are considered as the most important pollinator. They are characterized by their high degree of diversity, with about 20000 species worldwide (Michener 2007). Bees can be broadly grouped as either specialists or generalists depending on the diversity of floral resources they forage from. Specialist bees account 20%–30% bee species, collecting pollen from members of a single plant family or a genus (oligolectic) (Minckley and Roulston 2006), whereas most bees are generalist bees, which collect pollen from a broad variety of plant species belonging to various families (Cane and Sipes 2006). Honeybees, bumblebees and many mason bees, including
Mutual coexistence between insects and flowering plants for over 120 million years has led to a mutual relationship where the plant serves as food and in return the insect help them with their reproduction (Bascompte 2019; Engel 2000; Poinar and Danforth 2006). Pollinators, particularly bees learn associations between floral features (scent, color, shape, texture, and other floral signals) and the reward (nectar and pollen), and use these effectively to locate their host flowering plants (Clarke et al. 2013; Muth et al. 2016; Whitney et al. 2009). For these interactions, each part has evolved differential adaption to enhance the performance (Fig. 1). Olfactory cues are often of major importance to bees to make flower choices, because olfactory cues are easily learned and remembered by pollinators (Wright and Schiestl 2009). Olfactory cues are also important when visual signal is limited, such as foraging on night-blooming flowers and to locate their host plants from a distance (Raguso et al. 2003; Raguso and Willis 2002). In return, pollinators are equipped with behavioral and morphological adaptions to better serve the plant needs.
The notion that volatiles emitted by the plants mediate communication between plants and animals has long been acknowledged (Fraenkel 1959). The idea of volatile compounds mediation has been entertained since then by many other studies (Dötterl et al. 2014; Cheng et al. 2019; Knudsen et al. 2006). In general, flowering plants emit volatile organic compounds (VOCs), which are diverse and very complex. VOCs are lipophilic in nature, and possess high vapor pressure at ambient temperatures, as they are composed of low molecular weight. Indeed, plants belonging to 90 families have been reported to possess over 1700 individual volatile organic compounds (Knudsen et al. 2006). The composition of floral VOCs depend on many factors, including flower age, plant genotype, pollination status and others (Rodriguez-Saona et al. 2011; Klatt et al. 2013; Cheng et al. 2019). Previous studies showed that bees, especially honeybees and bumblebees, possess the capability to differentiate between individual and blends of VOCs (Laloi and Pham-Delègue 2004; Paldi et al. 2003; Wright et al. 2002).
Pollinators have a set of behavioral preferences, both innate and learned. Although naïve bees possess innate preferences for some floral signals, bees have a quick ability to learn association between volatile component(s) and food rewards (Milet-Pinheiro et al. 2013; Raguso 2008). Associative learning preference are largely beneficial for the pollinator because it has been credited to rapid floral diversification in both floral signals and floral rewards (Schiestl and Johnson 2013). Several studies over the years have indicated the importance of olfactory cues in bee-flowering plants interactions (Raguso 2008; Williams 1983). Bees possess one of the highest number of chemoreceptors (e.g., honey bees = 170; fruit flies = 62; mosquitoes = 79) in the insect kingdom that make them superior to recognize diverse floral odors (Robertson and Wanner 2006).
VOCs produced by the plants may have a wide variety of biological activities, such as antibacterial, antifungal (Hammer et al. 2003; Huang et al. 2012) and repellent activities against florivores (Junker et al. 2011). Given the vital role of effective pollination to many important crop yields, the pollinators of such crops are also linked to their VOCs of the floral scents. To this end, in this review, we compile fifty-three VOCs that mediate between bees and their flowering plant host.
In this review, an attempt is made to collect all relevant papers from three scientific databases (Google Scholar, Scopus, and Web of Science database), covering the period from 1959 to 2021. The following search terms were used: “flower scent”, “bee pollination”; “bee-flower scent interaction”, “flower volatile composition”; “honest floral signal”. Additional articles were also identified from the first search reference lists. From this search, we listed 53 VOCs compounds (Table 1) from 107 published papers.
Bees in general pollinate a wide variety of plants that differ in floral morphology (size, shape), color, and scent. Understanding of floral scents are key in bee-plant pollination network as bees heavily rely on floral scents to locate their host plants (Endress 1996; Proctor et al. 1996). Flowers can emit a variety of odor blends, which can be learned and recognized by their visiting pollinators (Dobson 2006). Flowering plants are well recognized to actively emit specific floral scent signals to attract pollinators (Knudsen et al. 2006; Williams 1983). In this review, an attempt is made to compile fifty-three volatile organic compounds (Table 1) from floral scent that are responsible for eliciting behavioral responses in bees. These VOCs belongs to different class of compounds, mainly terpenoids, benzenoids and volatile fatty acid.
Terpenoids comprise structurally diverse and the largest class of plant secondary metabolites present in all living organisms, particularly in flowering plants (Pichersky and Raguso 2018). In addition to attracting pollinators, terpenoids also play crucial role in plant’s defense against herbivorous (Abbas et al. 2017). Terpenoids presented over 50000 well known naturally produced compounds across all kingdom of life (Belcher et al. 2020). Isopentenyl diphosphate and dimethylallyl diphosphate, the two building blocks for terpenoid biosynthesis, are generally synthesized via two pathways: the mevalonate pathway (Liao et al. 2016) and the 2-
Floral scents of many flowering species are dominated by terpenoids (Fig. 3), which are known to attract generalist bees, including in
Orchids of the genus
Terpenoids are highly diverse in nature because a single terpenoid is susceptible to undergo several reactions (e.g., carbocation cyclization, rearrangement, and elimination reactions), lead to multiple products (Christianson 2018; Karunanithi and Zerbe 2019). It has been also demonstrated that the occurrence of multi-substrate terpenoids depend on the physiological and development status of plants. This suggests that terpene/terpenoids may be the plant’s preference in response to fluctuations in the environment (Pazouki and Niinemets 2016).
Benzenoids, also known as phenylpropanoids, constitute the second largest class of plant VOCs (Knudsen et al. 2006). They are exclusively derived from the aromatic amino acid phenylalanine, which is synthesized via the shikimate/phenylalanine biosynthetic pathways (Yoo et al. 2013). Benzenoids are biosynthesized via the shikimate pathway, involving a sequence of seven metabolic steps beginning with the condensation of phosphoenolpyruvate and erythrose 4-phosphate to form chorismate, the precursor of the aromatic amino acids and many aromatic secondary metabolites (Fig. 2) (Peled-Zehavi et al. 2015; Tzin and Galili 2010).
Male bees in Euglossini widely pollinate flower species belonging primarily to the Orchidaceae family (Endress 1996). Among the common VOCs that eliciting response in euglossine bees were benzenoids (Fig. 4) from
Many different oligolectic bee species are usually attracted to the flowering species belonging to the genus
Fatty acid derivatives are the third largest class of flower VOCs (Fig. 5), which derive from the unsaturated C18 fatty acids (linolenic and linoleic) (Muhlemann et al. 2014). Volatile fatty acids are synthesized and relied on a plastidic pool of acetyl-CoA derived from pyruvate, the final product of glycolysis (Feussner and Wasternack 2002).
Most of the oil-producing flowers and their frequent visitors (flower-oil-collecting bees) are neotropical. Oil-collecting bee species, such as
Several previous studies also demonstrated that volatile fatty acid derivatives such as (
Flowering plants are known to emit wide range of VOCs from being relatively rare to common. In general, specialized pollinators are attracted to flowering plants emitting rare VOCs (Fig. 6). One good example is
Mostly hydrocarbons produced by
In plant-pollinator relationship, pollinators prefer to visit flowering plants with honest floral signals that correlate positively with the reward status (food amount) (Bolstad et al. 2010). Honest signals could be either olfactory, visual, size, shape or any floral signal of the flower. In fact, pollinators are mostly guided to their host flowering plants by innate preferences or their ability to learn association between VOCs and food rewards (Arenas and Farina 2012; Raguso 2008).
There are several cases where bees make their decision to visit flowers based on the amount of the volatile components released by the flowers, and their association with the reward (Dobson et al. 1999; Dötterl and Jürgens 2005; Mena Granero et al. 2005). For example, level of phenylacetaldehyde (40) in
Nectar-depleted flowers can also emit distinct volatiles to repel pollinators and non-pollinator herbivores (Galen et al. 2011). The
In fact, flowering plants are rich with secondary metabolites. Terpenoids (such as
Over the years, several attempts have been made to modulate plant VOCs profiles and their effect on insect behavior. Numerous strategies have been implemented, such as by the modification of existing pathways, or by blocking the competing pathways or by introducing new gene(s) (Lange and Ahkami 2013). One success story of the strategy is that plant defense mechanism was highly improved by producing the volatile patchoulol along with additional sesquiterpene products in transgenic tobacco, overexpressing Pogostemon cablin patchoulol synthase (Wu et al. 2006).
Floral scents are composed of hundreds of diverse and complex volatile molecules. Understanding the function of these floral scent alone (Pichersky and Raguso 2018) or in synergy with other floral signals (e.g., visual cues) (Kunze and Gumbert 2001; Raguso and Willis 2002) is crucial in plant–pollinator mediations. Flowers generally use honest floral signals, and bees are able to correlate floral signals with nectar and pollen-rich flowers (Howell and Alarcón 2007). Thus, honest signaling mechanism plays a key role in maintaining mutualistic plant–pollinator associations (Knauer and Schiestl 2015). It was also indicated by previous studies that flowers with high level of floral VOCs can improve pollination service (Majetic et al. 2009; Parachnowitsch et al. 2012). For instance, field trials with flower scent manipulation to increase honeybee’s visitation to kiwifruit flowers led to some success (Pinzauti 1990; Tsirakoglou et al. 1997). Thus, crop production may be improved through genetic manipulation of the floral scent (Henning and Teuber 1992; Kobayashi et al. 2012; Twidle et al. 2015).
Given the role of chemical communication in plant-pollinator interactions, understanding and identification of VOCs from floral scent are crucial in improving crop pollination. Interestingly, current advances in both VOCs scent gene identification and their biosynthetic pathways make it possible to manipulate particular VOCs in plant. Thus, this eventually may lead to increase in crop productivity.
DB and CJ are deeply grateful to Insect ecology lab in Andong National University, South Korea.
DAHP: 3-Deoxy-D-arabinoheptulosonate-7 phosphate
DMAPP: Dimethylallyl pyrophosphate
E4P: Erythrose 4-phosphate
FPPS: Farnesyl pyrophosphate synthase
FPP: Farnesyl pyrophosphate
GGPP: Geranylgeranyl pyrophosphate
GPP: Geranyl pyrophosphate
IPP: Isopentenyl pyrophosphate
MEP: Methylerythritol phosphate
MVA: Mevalonic acid
VOCs: Volatile organic compounds
DB reviewed and wrote the manuscript. CJ designed, analyzed and edited the manuscript. All the authors approved the manuscript.
This study was funded by the BSRP through the National Research Foundation of Korea (NRF), Ministry of Education; Grant number NRF-2018R1A6A1A 03024862.
All data reviewed in this study are available from the corresponding author on request.
The authors declare that they have no competing interests.