ArticlePDF AvailableLiterature Review

Overview of Bee Pollination and Its Economic Value for Crop Production

Insects

July 2021
12(8):688

DOI:10.3390/insects12080688

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Authors:

Aida A. Abd Elwahed

Plant Protection Research Institute (PPRI)

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Simple Summary: There is a rising demand for food security in the face of threats posed by a growing human population. Bees as an insect play a crucial role in crop pollination alongside other animal pollinators such as bats, birds, beetles, moths, hoverflies, wasps, thrips, and butterflies and other vectors such as wind and water. Bees contribute to the global food supply via pollinating a wide range of crops, including fruits, vegetables, oilseeds, legumes, etc. The economic benefit of bees to food production per year was reported including the cash crops, i.e., coffee, cocoa, almond and soybean, compared to self-pollination. Bee pollination improves the quality and quantity of fruits, nuts, and oils. Bee colonies are faced with many challenges that influence their growth, reproduction , and sustainability, particularly climate change, pesticides, land use, and management strength, so it is important to highlight these factors for the sake of gainful pollination. Citation: Khalifa, S.A.M.; Elshafiey, E.H.; Shetaia, A.A.; El-Wahed, A.A.A.; Algethami, A.F.; Musharraf, S.G.; AlAjmi, M.F.; Zhao, C.; Masry, S.H.D.; Abdel-Daim, M.M.; et al.

Factors that influence bee visitation.

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Challenges faced in bee pollination.

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Insects 2021, 12, 688. https://doi.org/10.3390/insects12080688 www.mdpi.com/journal/insects

Review

Overview of Bee Pollination and Its Economic Value for

Crop Production

Shaden A. M. Khalifa

*, Esraa H. Elshafiey

, Aya A. Shetaia

, Aida A. Abd El-Wahed

Ahmed F. Algethami

, Syed G. Musharraf

, Mohamed F. AlAjmi

Chao Zhao

, Saad H. D. Masry

8,9

Mohamed M. Abdel-Daim

, Mohammed F. Halabi

, Guoyin Kai

, Yahya Al Naggar

13,14

, Mokhtar Bishr

Mohamed A. M. Diab

and Hesham R. El-Seedi

2,17,18,

Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University,

S-10691 Stockholm, Sweden

Department of Chemistry, Faculty of Science, Menoufia University, Shebin El-Kom 32512, Egypt;

esraaelshafiey8@gmail.com (E.H.E.); aya.shetaia@gmail.com (A.A.S.)

Agricultural Research Centre, Department of Bee Research, Plant Protection Research Institute,

Giza 12627, Egypt; aidaabd.elwahed@arc.sci.eg

Alnahalaljwal Foundation Saudi Arabia, P.O. Box 617, Al Jumum 21926, Makkah, Saudi Arabia;

ahmed@alnahalaljwal.com.sa

International Center for Chemical and Biological Sciences, H.E.J. Research Institute of Chemistry, University

of Karachi, Karachi 75270, Pakistan; musharraf@iccs.edu

Department of Pharmacognosy, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia;

malajmii@ksu.edu.sa

College of Food Science, Fujian Agriculture and Forestry University, Fuzhou 350002, China; zhchao@live.cn

Department of Plant Protection and Biomolecular Diagnosis, Arid Lands Cultivation Research Institute

(ALCRI), City of Scientific Research and Technological Applications, New Borg El-Arab City,

Alexandria P.O. Box 21934, Egypt; saad.masry@adafsa.gov.ae

Abu Dhabi Agriculture and Food Safety Authority (ADAFSA), Al Ain 52150, United Arab Emirates

Pharmacology Department, Faculty of Veterinary Medicine, Suez Canal University, Ismailia 41522, Egypt;

abdeldaim.m@vet.suez.edu.eg

Al-Rayan Research and Innovation Center, Al-Rayan Colleges, Medina 42541, Saudi Arabia;

m.halabi@amc.edu.sa

Laboratory of Medicinal Plant Biotechnology, College of Pharmacy, Zhejiang Chinese Medical University,

Hangzhou 310053, China; kaiguoyin@zcmu.edu.cn

General Zoology, Institute for Biology, Martin Luther University Halle-Wittenberg, Hoher Weg 8,

06120 Halle, Germany; yehia.elnagar@science.tanta.edu.eg

Zoology Department, Faculty of Science, Tanta University, Tanta 31527, Egypt

Arab Company for Pharmaceuticals and Medicinal Plants, (Mepaco-Medifood), El-Sharqiya 11361, Egypt;

m-bishr@mepaco-pharma.net

EWG Company, Menoufia, Shebin El-Kom 32512, Egypt; Mmmdiab82@gmail.com

Pharmacognosy Group, Biomedical Centre, Department of Pharmaceutical Biosciences, Uppsala University,

Box 591, SE 75124 Uppsala, Sweden

International Research Center for Food Nutrition and Safety, Jiangsu University, Jiangsu 212013, China

* Correspondence: shaden.khalifa@su.se (S.A.M.K.); hesham.el-seedi@farmbio.uu.se (H.R.E.-S.);

Tel.: +46-700-10-11-13 (S.A.M.K.); +46-700-43-43-43 (H.R.E.-S.)

Simple Summary: There is a rising demand for food security in the face of threats posed by a grow-

ing human population. Bees as an insect play a crucial role in crop pollination alongside other ani-

mal pollinators such as bats, birds, beetles, moths, hoverflies, wasps, thrips, and butterflies and

other vectors such as wind and water. Bees contribute to the global food supply via pollinating a

wide range of crops, including fruits, vegetables, oilseeds, legumes, etc. The economic benefit of

bees to food production per year was reported including the cash crops, i.e., coffee, cocoa, almond

and soybean, compared to self-pollination. Bee pollination improves the quality and quantity of

fruits, nuts, and oils. Bee colonies are faced with many challenges that influence their growth, re-

production, and sustainability, particularly climate change, pesticides, land use, and management

strength, so it is important to highlight these factors for the sake of gainful pollination.

Citation: Khalifa, S.A.M.; Elshafiey,

E.H.; Shetaia, A.A.; El-Wahed,

A.A.A.; Algethami, A.F.; Musharraf,

S.G.; AlAjmi, M.F.; Zhao, C.; Masry,

S.H.D.; Abdel-Daim, M.M.; et al.

Overview of Bee Pollination and Its

Economic Value for Crop

Production. Insects 2021, 12, 688.

https://doi.org/10.3390/

insects12080688

Academic Editors: Michelle T.

Fountain, Ignazio Floris and

Mariano Higes Pascaul

Received: 16 April 2021

Accepted: 23 July 2021

Published: 31 July 2021

Publisher’s Note: MDPI stays neu-

tral with regard to jurisdictional

claims in published maps and institu-

tional affiliations.

censee MDPI, Basel, Switzerland.

This article is an open access article

distributed under the terms and con-

ditions of the Creative Commons At-

tribution (CC BY) license (http://crea-

tivecommons.org/licenses/by/4.0/).

Insects 2021, 12, 688 2 of 25

Abstract: Pollination plays a significant role in the agriculture sector and serves as a basic pillar for

crop production. Plants depend on vectors to move pollen, which can include water, wind, and

animal pollinators like bats, moths, hoverflies, birds, bees, butterflies, wasps, thrips, and beetles.

Cultivated plants are typically pollinated by animals. Animal-based pollination contributes to 30%

of global food production, and bee-pollinated crops contribute to approximately one-third of the

total human dietary supply. Bees are considered significant pollinators due to their effectiveness

and wide availability. Bee pollination provides excellent value to crop quality and quantity, improv-

ing global economic and dietary outcomes. This review highlights the role played by bee pollina-

tion, which influences the economy, and enlists the different types of bees and other insects associ-

ated with pollination.

Keywords: bees pollination; economic; crop production; bee visitation; challenges; impact

1. Introduction

Pollination plays a vital role in maintaining the natural balance of ecosystems and is

the cornerstone of crop production, providing a link between agriculture and the cycle of

life. Consequently, pollination has a role in the economic sector owing to the improvement

of quality and quantity [1–3].

Pollination is defined as the process by which pollen moves from the male anthers to

the female stigmata, either within the same flower (self-pollination) or between plants

(cross-pollination) [4,5]. Pollinators are the key players of the crop yield process since

plants completely rely on vectors to transfer their pollen in cross-pollination. For instance,

incorporating both wild and managed bee species in a region could enhance cross-polli-

nation [6]. Possible other vectors include water and wind, and animal pollinators involve

bats, birds, butterflies, hoverflies, wasps, thrips, diptera, and other animals [6–9].

Animal pollinators contribute to the production of 87 global crops, including cocoa

(Theobroma cacao), kiwi (Actinidia deliciosa var. deliciosa), passion fruit (Passiflora edulis),

and watermelon (Citrullus lanatus) from 200 countries. Thirty percent of these crops par-

ticipate in global economic food production. Global pollination’s economic value aver-

aged EUR 153 billion, which is worth 9.5% of the world’s agricultural production of hu-

man food in 2005. The leading categories of insect-pollinated crops are vegetables and

fruit, making around EUR 50 billion each, followed by edible petroleum crops, stimulants,

nuts and spices. The one ton of crop production that is not dependent on insect pollination

is valued at about EUR 151, compared to an average of EUR 761 for crops dependent on

pollinators [10]. Pollination by insects is a key element in the production of a large number

of agricultural products worldwide, including aromatic and medicinal plants such as

black cumin (Nigella sativa linn), cumin (Cuminum cyminum linn) [11], anise (Pimpinella

anisum linn) [12], sunflower (Helianthus spp.) [13], and coriander (Coriandrum sativum linn)

[14]. Each season, honey bees, local bees, and flies pollinate 48 crops of the world's most

valuable commodities, contributing significantly to the global economy. [15]. For instance,

in the USA alone, pollination results in USD 16 billion annually with USD 12 billion at-

tributable solely to the accessibility of honey bees [16,17].

The Western honey bee (Apis mellifera L.) is the main species responsible for bee pol-

lination worldwide and meets, for instance, 34% of pollination service demands in the

United Kingdom [2,18]. Although several other bee species also contribute to pollination,

researchers have focused on only a limited number of these to date, particularly the bum-

ble bee (Bombus spp.) [19,20]. In comparison to wild bees alone, Greenleaf and Kremen

observed that interactions between wild bees and honey bees doubled pollination rates

and enhanced the prevalence of hybrid sunflowers by five-fold [21].

Insects 2021, 12, 688 3 of 25

This review aims to highlight the role of the bee in plant pollination and its impact

on the economy. The factors influencing bee visitation of flowers and plants, in addition

to a comparison of bees and other insect pollinators, are reported.

2. Effect of Bee Pollination on the Economy

There is an ever-increasing demand for food security in the face of challenges such

as climate change, land-use changes, habitat transformation, and the expanding human

population. Proper pollination can improve the quantity and quality of fruits, nuts, oils,

and other crops produced [22]. According to market prices, pollination by animals im-

proves the global crop output by an additional USD 235–577 billion annually, with the

greatest economic benefits having been seen in the Mediterranean, Southern and Eastern

Asia, and Europe [23]. However, greater production also leads to an increased demand

for pollination services [24]. Around the world, 5–8% of crop production would be lost

without animal pollination [25], and pollination also provides many services to ecosys-

tems, such as enhancing biodiversity and increasing food production without threatening

the environment [26].

Bees are the main pollinators of plants. According to Gallai et al., insect pollination

provided EUR 153 billion, representing 9.5% of the total economic value of agricultural

production used directly for human food [10]. Consequently, countries that grow cash

crops such as coffee (Coffea spp.), cocoa, almond (Prunus dulcis ((Mill.)), and soybeans (Gly-

cine max L.) have a much greater reliance on pollination in agriculture at a large scale [27–

29]. Scientists have used several methods to estimate the annual benefit of certain ecolog-

ical costs incurred by native insects in the USA, which have been shown to amount to

more than USD 57 billion, USD 3.07 billion of which is a result of bee pollination [30]. The

pollination services of non-apis pollinators were valued at USD 3.44 billion, but honey

bees contributed approximately USD 11.68 billion by 2009 in USA [16]. Honey bees are

responsible for pollinating over 100 commercial crops in North America [3]. Both honey

bees and wild bees are also economically important for sunflower seed production, which

is an uprising industry estimated at approximately USD 10.4 million annually [21].

Bee pollination also increases the yield of crops cultivated in farmland. For instance,

in sub-Saharan Africa, which is considered the main producer of cotton [29,31], bee polli-

nation increases the cotton yield to 62% compared with an estimated 37% without bee

pollination [32]. In addition, economic returns from bee pollination have been recorded in

smallholder farming systems in Kakamega (western Kenya), where several crops benefit

from pollination, including green gram (Vigna radiata), beans, cowpea (Vigna unguiculata L.

Walp), sunflower, tomato (Solanum lycopersicum linn), bambara groundnut (Voandzeia sub-

terranean L.), passion fruit, and capsicum, with pollination dramatically improving the

production rate and being responsible for almost 40% of the annual crop production [33].

The estimated annual value of pollination services rendered by bees in Brazil’s pro-

tected areas in 2016 was approximately USD 564,000 in the north (Serra da Bocaina,

Pará) and USD 246,000 in the southeastern region (Mata do Jambreiro) [34]. Of t he 36 c rops

produced in the state of Pará, 20 (55%) are dependent on animal pollinators, and the over-

all value of pollination services was USD 983.2 million in 2016, equating to 33% of the total

value of crop production (USD 2.95 billion). Four groups represented for 96% of Pará’s

pollination service value including; cocoa (USD 187.6 million), Acaí palm (USD 635.6 mil-

lion), watermelon (USD 26.1 million), and soybean (USD 98.4 million) [35]. In the USA,

wild bees and honey bees have produced comparable quantities of pollination for most

crops, including in agriculturally-intensive areas. The annual production value of wild

pollinators for seven crops is over USD 1.5 billion. The value of wild pollinators is esti-

mated to be the largest in apples, with a value of USD 1.06 billion while the approximate

values of watermelon (USD 146 million), blueberry (USD 50 million), sweet cherry (USD

145 million), art cherry (USD 32 million), and pumpkin (USD 101 million) are evidentially

high. The economic value of honey bees on yield across these crops is about USD 6.4 bil-

lion [36].

Insects 2021, 12, 688 4 of 25

3. Role of Bee Pollination in Crop Production (Quality and Quantity)

The number of visits and the aggregate effects of various bee species influence not

only the quantity of crops produced but also their quality, which is important mainly from

an economic perspective [37]. Plant pollination by more than one bee species, including

honey bees, carpenter bees, stingless bees, bumble bees, long-tongued bee, feral bees, so-

cial bees, and solitary bees, results in a better pollination/vegetation process, as shown in

Table 1.

3.1. Honey Bees

Western honey bee have been widely used as pollinators since the application of pol-

lination services began, and are the primary managed species worldwide for both honey

production and crop pollination [38]. Indeed, the Western honey bee ranks as the single

most popular species of pollinator for crops globally [39], and is the most effective crop

visitor worldwide, contributing approximately 13% of floral visits to 5% of plant species

across all plant networks [40]. However, there are at least eight other honey bee species in

the genus Apis, such as A. florea Fabr., A. cerana Fabr., A. andreniformis, and A. dorsata Fabr

[41]. In 2009, it was estimated that honey bees contributed USD 11.68 billion to agriculture

in the USA [16].

Honey bees are considered significant pollinators due to their effectiveness and wide

availability [16]. The mutualistic relationship between plants and honey bees results from

the exchange of nectar and pollen. Bees play a vital role in the pollination of plants [40],

and plants secrete a rich liquid sugar similar to nectar from their glands to attract pollina-

tors to their flowers so that the pollen can adhere to bee-collected pollen grains [42]. Re-

searchers have found that honey bees (A. mellifera L.) appear to prefer crops rich with

nectar and pollen in order to store large quantities of food, thus sustaining the colony

growth and improving foraging performance [43,44].

Many countries have used honey bees and achieved great results in terms of the qual-

ity and quantity of crops, as shown in Table 1. In the USA, the pollination activity of honey

bees is well recognized for three species of crops: cucumber (Cucumis sativus Linn), for

which there has been a 10% increase in yield and the number of colonies has increased

from 40,000 to 45,000; cranberry (Vaccinium oxycoccos Linn), which experienced an increase

in yield from 3.7 million in 1989 to 5.4 million in 1998 [45], and pear (Pyrus communis Linn),

which exhibited a 7% increase in fruit size and a net income increase of $400 per hectare

[46]. In India, the use of honey bees as pollinators improved the fruit quality of guava

(Psidium guajava Linn), as well as the fruit length and girth of coconut (Cocos nucifera Linn)

and citrus (Citrus spp.) compared with the controls [47,48]. In Egypt, honey bees have

significantly improved the seed set percentage and seed yield in onion (Allium cepa Linn)

crops compared with other insects [49]. Furthermore, in Burkina Faso, the production of

sesame (Sesamum indicum Linn) seeds tripled after using honey bees as pollinators [32].

The pollination of oilseed rape (Brassica napus Linn), buckwheat (Fagopyrum esculen-

tum Moench), and strawberry (Fragaria × ananassa (Duchesne ex Weston) Duchesne ex

Rozier) have clearly been dominated by honey bees, which have improved their quality

and yield [50]. Similarly, black cumin flowers are attractive to a range of pollinators, such

as Hemiptera (true bugs), Coleoptera (beetles), Diptera (flies), and Hymenoptera (bees)

[51]. However, honey bees are the most abundant pollinators affecting its productivity

and quality [11], with their pollination activity increasing the number of seeds and affect-

ing the total yield, which has led to the recommendation that beekeepers place bee colo-

nies near black cumin fields for better pollination [52].

The yield of anise also significantly relies on pollinator activity. One study showed

that honey bees exhibited a daily peak in anise pollination activity between 12 noon and

2 pm, and increased the yield above levels seen with insect exclusion, though levels were

Insects 2021, 12, 688 5 of 25

below those obtained with open pollination [12]. Honey bees and six species of Andreni-

dae are the main pollinators of coriander, with 63% of honey bee visits and 100% of the

visits by three species of Andrenidae resulting in pollinating activity [53].

For the apple (Malus domestica Borkh), increased flower visitation rates by high-qual-

ity honey bee colonies increased fruit set by 15%, as well as the fruit sugar content and

seed set compared with visits by conventional colonies, resulting in the farmer’s profits

increasing by 70%. Pollination by high-quality colonies also increased fruit weight by ap-

proximately 20% [54]. In the fruit of cape gooseberry (Physalis peruviana Linn), western

honey bees’ pollination improved the equatorial diameter by a mean of 13.3%, fruit mass

by 30.3%, seed variety by 7%, and seed mass by 8.4% compared with self-pollination [55],

while the use of honey bees for almond pollination increased fruit set by 60% compared

with bee-remote trees, which translated into a 20% increase in yield [29]. Observations of

blueberry (Vaccinium corymbosum Linn) pollination in the presence of wild bees (Bombus

spp., Halictids bees, Andrenids bees, and Xylocopa virginica) and controlled honey bees in

small isolated and large fields in Michigan, USA, showed that wild bees were the primary

pollinators in the small fields, accounting for 58% of flower visits, whereas honey bees

were the main pollinators in the large fields, accounting for 97% of visits. Furthermore, it

was found that flowers in the large fields were visited by four times as many bees as flow-

ers in the small fields. The weight of the fruit was affected by the level of bee pollination

and the abundance of bees, and the weight of berries was twice as high in the large fields

compared with the small fields [56].

3.2. Bumble Bees

Bumble bees (Apidae: Bombini) are vital pollinators for agricultural and wild plants

worldwide, and their pollination supports food security [57]. Five species of bumble bees

are generally used for pollination of commercial crops: Bombus terrestris Linn (in Europe,

North Africa, Asia, and Australasia), B. occidentalis Greene (in western North America), B.

ignitus and B. lucorum Linn (in East Asia), and B. impatiens Cresson (in North America)

[58].

The strong adaptation to different climates and habitats of bumble bees explains their

ability to continue foraging even in high and low temperatures [59]. Bumble bees have

contributed to the crop pollination via increasing the yield and enhancing the quality of

fruits [60]. Indeed, fruit growers gain many benefits from pollination by bumble bees,

which are good pollinators of several crops, such as kiwifruit (Actinidia Deliciosa) [61],

sweet pepper (Capsicum annum Linn) [62,63], and red clover (Trifolium pretense Linn) (Ta-

ble 1) [19] .

Bumble bees are important pollinators of a diverse range of crops, including buzz-

pollinated crops, such as blueberry and tomato, as well as both large-flower and small-

flower crops, giving them the potential to be sufficient pollinators in open fields and

greenhouses [64,65]. It has also been shown that buzz pollination by Bombus haemorrhoi-

dalis Smith in India leads to bigger, longer, heavier, and healthier fruits, especially in kiwi

fruit [61].

Pollination by bumble bees enhances the quality and quantity of tomato fruit, includ-

ing the number of fruit per cluster, the number of fruit per plant, fruit length, fruit fresh-

ness, fruit breadth, and fruit yield (Table 1) [65]. In addition, pollination of sweet pepper

by bumble bees results in a larger number of pollen grains and a higher level of seed set

on the fruit than self-pollination, such that flowers visited by bumble bees produce larger

and heavier fruit than non-visited flowers [63]. Finally, bumble bees have provided max-

imum pollination services to hybrid leek (Allium porrum Linn), resulting in a 25% increase

in plant quality, which has influenced the plant quality and crop price value by an esti-

mated USD 18,007 and USD 17,174 hectare, respectively [60]. In some cases, wild pollina-

tors give better pollination than honey bees, as seen in apple crops pollinated by bumble

bees, because all wild bee species are able to hold and deposit more apple pollen than

honey bees [66].

Insects 2021, 12, 688 6 of 25

3.3. Stingless Bees

Stingless bees (Apidae: Meliponini) are common floral visitors in tropical and sub-

tropical areas around the world. They exhibit greater dietary diversity and intensity in

their foraging behavior than honey bees and so are likely to influence the future develop-

ment of pollination solutions that are best suited to the needs of particular crops and hab-

itats [67].

Stingless bees are a large, diverse group of eusocial bees, making them good candi-

date pollinators. They vary widely in their body size, being described as small- to me-

dium-sized, and have vestigial stings [67]. Some species tend to be large and smooth, with

long hairs that help to bring pollen and other products to the colony [68]. The physiology

of stingless bees is suited to flower pollination [69] because they have suitable structures

for collecting pollen, nectar, and an absence of stinging behavior, making them easier to

handle than the majority of honey bees. Some stingless bees, such as those in the genus

Melipona, exhibit vibration behavior to extract the pollen, which is needed in crops with

poricidal anthers, such as tomato and pepper [70].

The neotropical stingless bee Melipona quadrifasciata Lepeletier is used to pollinate

greenhouse tomatoes, and has improved the production of fruit with lower levels of me-

chanical injury [71]. Stingless bees also play a prominent role in the pollination of green-

house cucumber crops, improving both the fruit weight and yield [72]. The pollination of

cucumbers by the stingless bee Heterotrigona itama and manual cross-pollination improved

crop quantity and fruit quality, allowing heavier, longer, and wider fruit to be produced

[73]. Similarly, the pollination of rockmelon (Cucumis melo var. reticulatus) by stingless

bees and manual cross-pollination had a positive effect on fruit set and the number of

seeds per fruit compared with self-pollination [74], and the pollination of strawberries in

greenhouses by stingless bees increased the quality and commercial value of the fruit com-

pared with a control group [75]. Furthermore, the pollination of eggplant (Solanum

melongena Linn) by Melipona fasciculata Smith in greenhouses increased fruit set by 29.5%

and increased fruit quality (measured as fruit weight) compared with self-pollination [76].

3.4. Carpenter Bees

Large carpenter bees are a group of bees that occur in tropical and subtropical areas

and belong to the genus Xylocopa in the tribe Xylocopini (Apidae: Xylocopinae) [77].

Compared with other non-Apis bees, carpenter bees have numerous advantages in crop

pollination, as they feed on a broad range of plant species during their long activity sea-

sons. They also have the ability to buzz-pollinate flowers, making them even more diverse

crop pollinators [78]. However, there is a great need for a sufficient breeding program to

be developed that involves the selection of genotypes, controlled mating, and nest foun-

dation [79].

Carpenter bees are known for their ability to make their nests in tunnels in hard

wood, logs, stumps, or the dead branches of trees [80]. In India, carpenter bees are active

throughout the year and forage on a variety of flowers during the day and sometimes

even work through moonlit nights. It has been noticed that flowers visited by carpenter

bees produce nectar that is odoriferous, so it is possible that these bees use this odor as a

cue to visit the correct flowers [81].

The use of carpenter bees for pollination services is necessary to guarantee adequate

pollination for several crops, including passion fruit (Passiflora edulis f. flavicarpa), cucur-

bits, and other vegetables and fruits, as observed in the Philippines, Brazil, USA, and Ma-

laysia [82,83]. Yellow passion fruit is satisfactorily pollinated when the flowers are only

visited by native bees, especially carpenter bees [84]. Furthermore, when native carpenter

bees (Xylocopa (Lestis)) were used as an alternative to bumble bees for tomato pollination

in a greenhouse, the females visited and buzz-pollinated the flowers and the resulting

fruit were heavier and contained more seeds than those that were not pollinated by these

Insects 2021, 12, 688 7 of 25

bees [85]. The carpenter bee Xylocopa pubescens Spinola is also used to pollinate green-

house-grown honeydew melons (Cucumis melo Inodorus Group), as it was noticed that

while this species had shorter visit durations per flower than the honey bee, pollination

by both bees resulted in a similar fruit mass and seed numbers, and X. pubescens pollina-

tion increased fruit set three-fold compared with honey bee pollination [86].

3.5. Solitary Bees

Solitary bees comprise the majority of bee species in the world. Solitary bee species

account for 85 % of all bee species [87].The majority of solitary bees are polylectic (i.e.,

collect pollen from numerous plant species), while a smaller number are oligolectic (use a

narrow range of plants) and very few are monolithic (use only a single plant species). In

recent decades, there has been a decline in monolithic and oligolectic species in Britain

[88]. Solitary bees play a major role in pollination, and it has been demonstrated that wild

bees contribute USD 3251/hectare for their pollination services worldwide, seven out of

ten of which are solitary [89]. Solitary bees are more effective pollinators than honey bees

for some crops that depend on pollinators for their reproduction, such as apple. Indeed,

in the United Kingdom, the economic gains of using solitary bees for apple production

were estimated to be € 51.4 million compared to honey bees of € 21.4 million [90].

Table 1. The impact of bee pollination on crop quality and productivity in various countries.

Crop (Species) Bee Pollinator Impact on Crop Yield Country Reference

Fruits

Apple

(Malus

domestica L.)

Honey bees (Apis mellifera L.)

Enhancing fruit production with high

yield and quality (fruit size and number

of seeds).

Pakistan [91]

Wild bees and honeybees (

mellifera)

Seed number increased with bee abun-

dance which consequently increased fruit

quality.

China [92]

Stingless bees

(Melipona quadrifasciata

anthidioides Lepeletier)

Africanised honeybee (A.

mellifera)

Both stingless bees (12 hives/hectare) and

Africanized honeybees (7 hives/ hectare)

provided higher seed and fruit produc-

tion than supplementation with honey-

bees alone.

Brazil [93]

Honey bee (A. mellifera)

Increased fruit set by 15%, seed set and

content of fruit sugar, and farmer’s prof-

its by 70%.

Argentina [54]

Bumble bees (B. impatiens)

and honey bee (A. mellifera)

The quantity and quality of fruits pro-

duced from pollination from both species

were equivalent.

Canada [66]

Wild bees Fruit set increased USA [94]

Coconut

(Cocos nucifera L.)

Honey bees (A. mellifera) Increased fruit set Mexico [48]

Honey bees (A. mellifera) Effective pollinators compared to wasp Jamaica [95]

Watermelon (Cit-

rullus lanatus

Thunb.)

Honey bees

(A. mellifera)

Fruit set, fruit numbers and weights per

plot increased linearly as number of

honey bees visits increased.

USA [96]

Tart cherry

(Prunus cerasus L.) Osmia lignaria solitary bee Cherry weight increased by 2.8% com-

pared to the control. Utah [97]

Cape gooseberry

(Physalis peruviana

L.)

Honey bees (A. mellifera)

Improvement of fruit mass by 30.3%,

equatorial diameter by 13.3%, seed vari-

ety by 7%, and seed mass by 8.4%.

Colombia [55]

Insects 2021, 12, 688 8 of 25

Sweet cherry

(Prunus avium L.) Wild bees and honey bees Fruit set was enhanced compared to

open pollination. Germany [98]

Almond (Prunus

dulcis (Mill.)

D.A.Webb)

Honey bees

(A. mellifera)

Increased fruit set by 60% and kernel

yield by 20% compared to self-pollina-

tion.

USA [29]

Solitary Bee

(O. cornuta)

Increased fruit production was parallel

with increased visits by O. cornuta. Spain [99]

Avocado

(Persea americana-

Mill.)

Honey bees (A. mellifera)

High pollination efficiency for fruit set,

increased the production, and improved

the weight of the fruit.

In Central

America [100]

Passion fruit

(Passiflora edulis

Sims. f. flavicarpa

Deg)

Honey bees (A. mellifera),

and carpenter bees (Xylo-

copa spp.)

The diversity of bee species affected the

fruit set and fruit quality and led to a

higher reproductive efficiency.

Australia and

Philippins [82,83]

Native Brazilian bees (Xylo-

copa spp.)

Production costs lowered by 58%.

Average production was 7000 kg/hec-

tare/year.

Brazil [101]

Citrus (Citrus sinen-

sisL.) Honey bees (A. mellifera) Lead to heavier fruit with less acid con-

tent and fewer seeds per bud. Brazil [102]

Mango (Mangifera

indica L.) Honey bees (A. cerana) Fruit setting was 42.29% compared to

open pollination 33.36%. India [103]

Guava (Psidium

guajava L.) Honey bees (A. mellifera) Increased fruit set; improved the quality

of fruit length and girth. India [47]

Strawberry

(Fragaria × ananassa

DUCH)

Osmia bicornis L.

Increased commercial value by 54.3%

compared with self-pollination and by

38.6% compared with wind pollination.

Number of fertilized achenes increased,

and improved post-harvest quality oc-

curred (more intensive red colour and

lower sugar acid ratios).

Germany [104]

Bees Quantity and quality improved.

Yield increased 20%. Germany [50]

European orchard bee (Os-

mia cornuta Latr)

Fruit weight was higher than the control

treatment. Germany [105]

Kiwifruit (

ctinidia

Deliciosa)

Honey bees (A. mellifera) Increased fruit set and yield. Australia [106]

Bumble bee

(Bombus haemorrhoidalis

Smith)

Higher fruit breadth, longer fruits, heav-

ier fruits, higher healthy fruits, and

higher fruit set.

India [61]

Pear (Pyrus com-

munis L.) Honey bees (A. mellifera)

Fruit size increased by 7% and lead to

USD 400 per hectare net increase in in-

come.

USA [46]

Cranberries (Vac-

cinium oxycoccos L.) Honey bees (A. mellifera ) Production increased from 3.7 million in

1989 to 5.4 million in 1998. USA [45]

Vegetables

Cucumbers (Cu-

cumis sativus L.)

Honey bees (A. mellifera) 10% increase in production. USA [45]

Stingless bee (Heterotrigona

itama)

Lead to larger, heavier, and longer cu-

cumbers. Terengganu [73]

Sweet pepper (Cap-

sicum annuum L.)

Bumble bee (Bombus impati-

ens Cr.)

Increased fruit weight, width, and vol-

ume.

Increased seed weight and reduced har-

vesting time.

Canada [62]

Insects 2021, 12, 688 9 of 25

Bumble bees (Bombus ter-

restris L.)

Increased yields, fruit weight, and qual-

ity of seed, and fruits under unheated

greenhouse conditions.

Seed set was 49.8% compared to 27.5% of

the control (self-pollination) treatment.

Spain [63]

Tomatoes

(Solanum lycopersi-

cum L.)

Bumble bee (Anthophora ur-

bana Cresson and Bombus

vosnesenskii Radoszkowski)

Lead to higher yield and improved the

quality of fruits. USA [107]

Bees (Exomalopsis analis Spi-

nola, Centris tarsata Smith,

Bombus morio Swederus, Eu-

laema nigrita Lepeletier and

Epicharis sp.)

Increased fruit production and quality. Brazil [108]

Aromatic and medicinal plants

Anise (Pimpinella

anisum L.) Honey bees (A. mellifera)

Increasing seed yield/feddan to 781.55 kg

compared to 300.24 Kg for control group

(insect exclusion).

Egypt [12]

Black Seed (Nigella

sativa L.) Honeybee (A. mellifera)

Increased yield and seed setting but no

effect on the weight of the seed pro-

duced.

Pakistan [109]

Cumin (Cuminum

cyminum L.)

Apis florea F., A. mellifera and

A. dorsata

Enhanced yield by 40.03% compared to

41.37% for open pollination. India [11]

Sunflowers (Helian-

thus annuus L.)

Wild bees and honey bees

(A. mellifera)

Interactions between wild and honey

bees increased the efficiency of pollina-

tion up to 5-fold compared to honey bees

only.

USA [21]

Africanized honey bees (A.

mellifera)

The average yield of seeds was 43%

higher compared to the control. Brazil [13]

Honey bees (Apis mellifera L.) Played a significant role in pollination

compared to moths and wind.

Central Dar-

ling Downs [110]

Coriander (Corian-

drum sativum Lin-

naeus.)

Apis cerana Fabricius

The seed set was significantly higher by

69.51% compared to 54.89% in the control

group. The yield was 14.57 q/hectare vs

11.66 q/hectare in the control group.

India [14]

Other plants

Cotton Gossypium

hirsutum L.)

Honey bees

(A. mellifera)

Increased production by more than 12%

for fiber weight and over 17% for seed

number.

Brazil [111]

Honeybees and wild bees

Significantly increased yield quantity

and quality by an average of 62%. The

average yield was 953.91 kg/hectare.

West Africa [32]

Pumpkins (Cucur-

bita maxima L.) Honey bees (A. mellifera)

Fruit set, fruit size, weight, and number

of seeds increased linearly with the num-

ber of visits.

Brazil [112]

Soyabean (Glycine

max L.)

Honey bees

(A. mellifera)

Yield increase was associated with an in-

crease of the seed number. Argentina [113]

Honey bees

(A. mellifera) Increased yield by 18.09%. Brazil [114]

Sesame (Sesamum

indicum L.)

Honeybees (A. mellifera) and

wild bees

The mean yield of seed was 202.20

kg/hectare. West Africa [32]

Insects 2021, 12, 688 10 of 25

The exclusion of pollinators caused an

average yield gap of 59%.

C. canephora L Apis dorsata F. Bees increased fruit production of coffee

by 50% more than wind. South India [115]

Cowpea (Vigna un-

guiculata L. Walp) Honey bees and bumble bees NR Nigeria [116]

Red clover seed

(Trifolium pratense

L.) legume

Bumble bee (B. vosnesenskii) High yield and most production of seeds. USA [19]

Pineland golden

trumpet (Angadenia

berteroi (A.DC.)

Miers)

Long-tongued bee (Megachile

georgica Cresson and

Melissodes communis com-

munis)

NR USA [117]

Mustard

(Brassica juncea L.)

Honey bees (A. mellifera)

Increased fruit set, viability of seed, seed

yield, and oil nutrient contents in the

seed.

India [118]

Honey bees (A. cerana)

Increased siliqua/panicle by 20.8%,

seeds/silique by 9.4%, and seed yield by

17.1% compared to open pollination.

India [119]

Green grams

(Vigna radiate L.)

and Bambara

groundnut (Voan-

dzeia subterranean

L.)

Feral bees Enhanced yield and improved the qual-

ity of crops. Kenya [33]

Coffee (Coffea ara-

bica L.) Solitary bees and social bees Significantly increased fruit set. Indonesia [120]

Acai palm (Euterpe

oleracea Martius)

Stingless bee (Scaptotrigona

aff. postica)

Increased the production reach to 2.5

times. The increase was evident as per

the number of fruits per bunch and fruit

size.

Brazil [121]

Oilseed rape (Bras-

sica napus L.)

Solitary mason bee (Osmia

rufa L.)

Increased fruit set, yield, and the number

of seeds per pod by bee density. Germany [122]

Honey bees (A. mellifera) Increased oil and decreasing chlorophyll

content. Sweden [50]

Honey bees (A. mellifera),

and wild bees (Lasioglossum

spp.).

Average yield was increased up to 37.5%. France [123]

NR: Not reported.

4. Bee Visitation

Pollination is carried out by bees and other insects for a variety of plants. Because

pollination is so important to plants, they adapt to be more appealing to pollinators

[124,125]. Plants possess several means to attract bees, including flower color [126,127],

flower motion as in the case of bumble bees [128], the type of plant cells (e.g., conical

epidermal cells) as in bumble bees [129], visual and olfactory cues as in honey bees and

apple pollination [130] and the production of nectar and pollen grains [131,132], as shown

in Figure 1. Thus, plants play an important role in influencing the visitation rate of their

pollinators [133].

Insects 2021, 12, 688 11 of 25

One of the most important properties of plants that attracts bees is the color of the

flowers [134,135]. Bees have a trichromatic visual system that is sensitive to green, ultra-

violet, white, and blue wavelengths, allowing them to see numerous colors. Bees often

visit blue or purple flowers but mostly prefer blue flowers [136,137]. By contrast, bees are

less attracted to red flowers, though they will sometimes visit red flowers that reflect ul-

traviolet light [138].

The motion of flowers is also crucial for enhancing attractiveness to bees, as this is

integral to their three-dimensional vision. The relative motion of the flowers increases the

number of opposing stimuli on the bee‘s eye. Conical epidermal cells have multiple func-

tions, such as promoting the perception of flower color and reducing the wettability of the

petal, which increases the effectiveness of the pollination process. Consequently, bees usu-

ally prefer to visit conical-celled Petunia flowers, particularly those that are most attractive

with motion [139,140]. Indeed, higher numbers of bees occur on the moving portion of a

flower bed due to their positive response to optical stimulation [139]. In addition, floral

volatile compounds affect the orientation of bees [141], as well as pollen collection and

behavior in bumble bees [142]. Flower size has a special function for attracting pollinators

[141]; bumble bees (Bombus diversus Smith) prefer large floral displays [143].

Finally, the quantity and/or quality of pollen and nectar produced may affect the vis-

itation of flowers by bees. Nectar and pollen are sources of energy, protein, and lipids for

bees, and other pollinators [144] and bees are drawn to plants to provide food for their

young [145]. Solitary bees search for pollen but rarely nectar [132], whereas honey bees

search for flowers with larger amounts of nectar [146]. It has previously been shown that

the composition of wild bee populations that visit various plants can best be explained by

variations in the flowering areas, height of the flowers, and amount of pollen deposited

in the flowers [147]. For example, British bumble bees differentiate between Mimulus gut-

tatus plants on the basis of their pollen content and quality, with a significant association

between visitation and pollen content [148]. Furthermore, both wild bees and honey bees

forage on sunflowers for their nectar sugar, with the number of flower visits increasing

significantly with an increasing nectar sugar level and decreasing during the corolla pe-

riod but seeming to be unaffected by nectar sugar composition. Wild bees make more

visits to sunflowers that provide pollen (male-fertile plants) and honey bees favor pollen-

free flowers (male-sterile plants) [146]. Cover crops, particularly low-diversity mixes that

include buckwheat and Phacelia spp., provide a high abundance of flowers throughout the

summer, resulting in excessive bee visitation rates, with Phacelia spp. being more appeal-

ing to honey bees and bumble bees, while sunflowers and local wildflowers are more ap-

pealing to solitary bees [149].

Honey bees visit native and cultivated plants at comparable average rates that are

independent of floral abundance, therefore increasing their visitation rates for the highly

abundant plants, whereas the visitation rate of wild pollinators is higher for cultivated

plants than for native plants. For example, knapweed (Centaurea spp.) is a widespread

and often locally important plant for honey bees, as it is favored and regularly visited for

its pollen and nectar [150]. In France, the visitation ratio of large solitary bees, wild beetle

pollinators, and bumble bees was negatively impacted by the abundance of honey bees

colonies [151].

One behavior that some bees have developed during their visitation is buzz pollina-

tion, whereby the bees make vibrations to remove and collect the pollen from the fruit set,

fruit mass, and flowers during fertilization [152]. About half of bee species can perform

buzz behavior, such as large carpenter bees, minute sweat bees and bumble bees, but they

differ in their buzz properties [153,154]. This vibration is the best means for extracting

pollen from plant species that have small pores on their anthers [155]. During this behav-

ior, the bee bites the anther of the flower and makes vibrations with its thoracic muscles

while in direct contact with the flower, causing the vibrations to be transmitted into the

flower [156]. There are several ways of performing this buzzing behavior. For example,

the flowers of Pedicularis spp. have long anthers and narrow corolla tubes, so bees make

Insects 2021, 12, 688 12 of 25

their vibrations on these corolla tubes for rapid pollen extraction [157,158]. Therefore, this

behavior is related to the functional specificity of flowers, particularly in those flowers in

which pollen release requires modification of the stamens. Buzz pollination takes its name

from the audible sound made during the vibration and is also often called sonication [157].

It is currently believed that this vibration behavior for pollen collection is not performed

by any other animal [70]. However, further research is required to determine whether

some flies also use vibration behavior to collect pollen.

Most bees visit flowers during the daylight; only five of nine families of bees search

for flowers in dim light [159]. Nocturnal bees have different factors that affects their flower

trips, including light intensity and temperature. Temperatures and light levels are lower

at night than during the day, and this can affect, in particular, the behavior of nocturnal

bees [29].

Figure 1. Factors that influence bee visitation.

5. Challenges Faced in Bee Pollination

Bees are surrounded by several variables that affect their role as pollinators, such as

pathogens, nutritional shortages, climate change, and deforestation (Figure 2) [160–163].

Pathogens such as viruses and bacterial infections have a negative effect on bee health and

longevity, threatening pollination services of crops and wild plants [164]. Viral infections

affect bee immune systems, causing disease in entire colonies [165]. Colony collapse dis-

order (CCD) is a phenomenon whereby there are unexplained, rapid losses of adult work-

ing bees in managed bee colonies (e.g., honey bee colonies in the USA), resulting in only

the queen and a few nursing bees remaining [166]. This problem faces many beekeepers

[167]. In the USA, the parasites Nosema ceranae and Nosema apis also have highly patho-

genic effects, causing huge honey bee losses [168]. Conroy et al. [169] found that both nu-

tritional limitation and pathogens have a large effect on bumble bees, with a lack of pollen

and low nectar sugar levels leading to reduced pollination and, consequently, a decline in

production. In addition to the natural factors affecting bee pollination, the use of pesti-

cides, such as acetamiprid and ergosterol-inhibiting fungicides, threaten pollination ser-

vices [170]. The residues of pesticides and other synthetic products remain in the nectar

and pollen collected by bees, leading to neurotoxicity, immune deficiency, behavioral

Insects 2021, 12, 688 13 of 25

changes, and chronic ailments [171,172]. The application of neonicotinoid insecticides,

which are systemic insecticides that are transferred into the pollen and nectar of many

pollinated crops, is one of the main co-factors associated with bee losses [173,174]. Spray-

ing agrochemicals such as fungicides, insecticides, and pesticides cause contamination,

toxicity, and declines in the quality and quantity of nutrients in the pollen and nectar,

leading to poor colony health and hence threatening the survival of bees [175,176].

Recently, the Environmental Protection Agency (EPA) has been investigating the ef-

fect of pesticides on the immune system of bees [177], while the European Food Safety

Authority assessment provides information on the chronic toxicity of pesticides on bees

[178]. The effect of neem-based insecticide (botanical) and pyrethroid insecticides, del-

tamethrin and the fungicides thiophanate-methyl and chlorothalonil (synthetic) insecti-

cides on the melon (Cucumis melo L.) has been investigated. Both insecticides and pesti-

cides not only reduced the visitation intensity of bees but also lead to lower melon yield

[179]. Therefore, good nutrition has a direct effect on the immune function and an indirect

effect on energy availability [161].

Many factors also affect the growth, reproduction, and survival of bees, such as high

temperatures, and humidity, reducing not only the biodiversity of bees and other pollina-

tors but also agricultural production [160]. Most bees visit flowers during the daylight,

but some bee families search for flowers in dim light [159]. Nocturnal bees settle their

flower trips by light intensity and temperature [180].

Deforestation can also affect bee populations (Figure 2) [163]. For example, the abun-

dance of bumble bees in the tropical agricultural highlands of Guatemala increased with

the increase in forests and semi-natural vegetation in local areas, but was not influenced

by season [181]. Habitat loss and climate change also affect honey bees worldwide, caus-

ing pollinator losses [182–184].

Figure 2. Challenges faced in bee pollination.

6. Bee Pollination vs. Non-Bee Pollination

Bees are considered the most effective pollinators; however, the contribution of other

insect pollinators cannot be considered negligible, as they serve to increase and stabilize

Insects 2021, 12, 688 14 of 25

crop pollination and rely on these plants for the supply of pollen and nectar [17,149,184].

The main groups of other insect pollinators are butterflies, moths (Lepidoptera), some flies

(Diptera), and beetles (Coleoptera) [17,185].

6.1. Hoverflies vs. Bees

Hoverflies (Diptera: Syrphidae) are considered the most anthophilous family in the

order Diptera [186]. Episyrphus balteatus DeGeer is one of the most common hoverfly spe-

cies to usually be found in agricultural areas, and several recent studies have confirmed

its contribution as a pollinator of many crops around the world [187]. One crop that is

pollinated by hoverflies E. balteatus is oilseed rape, which is an important crop in temper-

ate regions. It has been shown that when E. balteatus is involved in the pollination services

of this crop, sufficient numbers of seeds per pod are produced, demonstrating the ability

of E. balteatus as a pollinator of edible crops [188]. The drone fly, Eristalis tenax L., has also

been reported as a successful pollinator of numerous managed crops, such as pak choi

(Brassica rapa subsp. chinensis) and onion in New Zealand [189], onion, spring turnip rape

(Brassica rapa L. subsp. oleifera), and carrot (Daucus carota L. subsp. sativus) in Germany

[190], sweet pepper (C. annuum) in Canada [191], and kiwifruit in Italy [192]. Conse-

quently, according to Brad and Megan, E. tenax L. is often kept in large numbers in fields

during the crop flowering period [189].

A study in Germany looked at the impact of pollination by the solitary mason bee O.

rufa and two hoverfly species (E. tenax and E. balteatus) on oilseed rape. This study showed

that the fruit yield and number of seeds per pod improved with an increase in bee abun-

dance relative to hoverfly abundance, and that five-fold higher density of hoverflies than

red mason bees were required to achieve the same fruit sets and yields. Thus, mason bees

were more effective pollinators of this crop than hoverflies [122].

6.2. Butterflies vs. Bees

Around 180,000 species of butterfly and moth (Lepidoptera) are reported and make

up to about 10% of all recognized insect species. Butterflies represent approximately 10%

of Lepidoptera [193] and tend to visit psychrophilic flowers that offer small to medium

volumes of dilute nectar. These flowers are characterized by brightly colored petals with

a mild and pleasant aroma and a flat platform that enables the butterflies to land in the

inflorescence. Large- to medium-sized butterflies act as pollinators via their wings [194].

Gloriosa minor Rendle (Colchicaceae) is a dry land floral plant in Kenya that depends on

butterflies for pollination, and consequently the production of seeds, which are a source

of colchicine [195]. Caesalpinia pulcherrima was pollinated mainly via butterflies which

carry the pollen on their wings [196].

Angadenia berteroi is an endangered species that has large, showy, yellow, and tubular

flowers with no notable fragrance. The tubular shape of these flowers gives them a com-

plex structure, so any pollinators that are attracted to this plant should have body parts

that are specifically adapted to this morphology, including mouthparts that are long

enough to find the nectar [197,198]. Both bees and butterflies visit A. berteroi, allowing a

comparison of their efficiency. The long-tongued bees’ heads are wider than the apical

portion of the pollen chamber, forcing them to touch the reproductive parts of the flower,

and these bees rarely revisit the same flowers. Long-tongued bees appear to be efficient

in gathering nectar and transporting pollen [117,199]. By contrast, the two groups of but-

terflies that visit the flowers [skippers (Hesperiidae and non-skippers) carry very small

amounts of pollen on their proboscides, do not deposit this pollen on the stigmas of the

flowers, and frequently visit the same flowers, thus appearing to act as nectar thieves. The

frequent visitation of the same flower by an insect is known to have negative effects. For

instance, flower re-visitation can lead to abortion of the fruit and ovule due to self-pollen

deposition on the stigma, explaining why the mouthparts are associated with the efficacy

of the pollination process [117].

Insects 2021, 12, 688 15 of 25

6.3. Moths vs. Bees

Moths can be categorized as having a crepuscular or nocturnal lifestyle and are rec-

ognized as one of the main pollinators of a large variety of plant species in different hab-

itats around the world [200]. The information on the role of moth pollination in natural

habitats is available where about 227 flowers have been pollinated by moths [193]. Moths

are frequent floral visitors, and there are a number of encounters between plant species

and moths. Moths pollinate approximately 40% of plant species in rural landscape envi-

ronments, such as meadows, pastures, old farms, field edges, and roadsides. Conse-

quently, the role of moths in agricultural environments is often attributed to their pollina-

tion of non-crop plants, which contributes to increasing the biodiversity in agro-ecosys-

tems, offering a widely appreciated ecological function [201,202]. Moths may also polli-

nate some unique plant species, such as some orchids. At present, however, the role of

moths in pollination is likely underestimated due to the limited number of studies on this

topic [203–205].

An evaluation of insect pollination levels on sunflower crops in the central Darling

Downs during the day and night showed that Western honey bees were the most recur-

rent visitors, with populations averaging 65.3 bees per 100 flower heads across 42 crops

through mid-morning [110]. By contrast, Helicoverpa armigera Hübner moths were ob-

served visiting the plants during the night, averaging 3.9 individuals per 100 flower heads

between 7 and 8 pm and being registered in 33 crops. Thus, moths visited the flowers for

less than 2 h per night whereas bees were active for 9 h. The small population size and

low level of activity of moths indicated that bees played a significant role in sunflower

pollination in this area [110].

6.4. Beetles vs. Bees

Beetles (Coleoptera) belong to one of the most diverse insect orders and their role in

pollination systems is increasingly being recognized. Some flowering plants depend on

pollination by certain types of beetles. For example, species in the subfamily Cetoniinae

(Scarabaeidae) are common pollinators in the tropics [206]. More than 184 species of an-

giosperms are exclusively pollinated by beetles (e.g., Magnolia in Magnoliaceae) [207,208].

Some beetles use flowers as rendezvous sites besides their usage in their food which en-

hances their role as pollinators. Unlike tropical pollinators, beetles depend on odor to find

flowers, while Hopliine beetles exclusively use visual indications and, even without nour-

ishment or smell, are attracted to bright colors [209]. Beetles are always associated with

the pollination of open bowl-shaped flowers [207]. Beetles were found to be the second

most important insect group contributing to pollination services in both Lambir (27%) and

Kakachi (17%) in Malaysia and India, respectively. Both bees and beetles together repre-

sent more than 60% of the pollination services of tree species in Lambir and 34% of those

in Kakachi [210]. Bees play the main pollinator role in Lambir (32%) followed by beetle-

pollinated species (20%) [211], but the beetle Hopliini sp. (Scarabaeidae) is one of the most

effective pollinators in the southwestern area of Cape Province and Namaqualand

[212,213]. Therefore, there is a need for further studies to clarify the ecological role of bee-

tles and their effectiveness as pollinators [214].

6.5. Thrips vs. Bees

Thrips (Thysanoptera) are pollinators of plant species, however they are still poorly

studied [215]. These tiny insects have piercing-sucking mouthparts and are usually no-

ticed on flowers, where they depend on nectar, pollen, or the cell content of plant tissues

in their food [216]. Thrips have been noticed in the flowering period of coffee species C.

arabica

L. and C. canephora L. in the southern state of Chiapas, Mexico in three flowering

seasons (2013–2015). Several species of thrips on coffee flower were noticed to be carrying

a few pollen grains on their bodies [217]. Bees have increased fruit production of coffee

by 50% more than wind in shaded coffee agro-forests, South India. The role of other insect

Insects 2021, 12, 688 16 of 25

visitors with bees including Thysanoptera in coffee was insignificant as they did not touch

the flower anther or stigma enough times in addition to performing infrequent visitation

[115].

6.6. Wasps vs. Bees

Social wasps (Hymenoptera) are among the pollinators in the Neotropical region. As

predators, they can behave as flower visitors [218,219]. Many factors attract wasps to flow-

ers such as flower color and shape. Wasps are attracted to reddish brown, dirty purple,

and dirty brown flowers. Schremmer (1962) has noticed that wasps are attracted to small

flowers with bulbous, wide entrances and sucrose-rich nectar [115,220]. Floral scent is one

of the main factors attracting wasps. For example, social wasps are the main pollinators

of Epipactis helleborine L. due to their scent [221,222]. Another study has been done on the

coconut flower in the presence of wasps and honey bees. The wasps (Polistes crinita Felt)

failed as a pollinator because of their disability in loading adequate amounts of pollen and

their behavior in deterring the honey bee. In contrast, honey bees were effective as polli-

nators to coconut [95].

7. Conclusions

Bee pollination provides a wide variety of benefits to humanity, contributing to food

processing, raw materials, medicines, fibers, social, cultural values, and the maintenance

of biodiversity and environmental protections. Bees’ pollination has direct effects on the

profitability and productivity of a substantial amount of global crop varieties, including

most vegetables, seeds, and nuts, and some high-value agricultural products, such as cof-

fee, cocoa, and rapeseed. Currently, 5–8% of all global crop production would be lost with-

out the pollination services provided by bees, necessitating changes in the human diet and

the expansion of agricultural lands to resolve shortfalls in crop production. Bees are faced

with many challenges that can distort their lives, including shifts in land use, climate

change, pesticides, genetics and cultivation management. Concerns regarding the decline

of domestic and wild bees have intensified the need to encourage the usage of the wild

pollinators on agricultural lands. As wild bee trips have increased with the development

of high-diversity bee habitats in the surrounding landscape, the restoration of high-diver-

sity bee habitats is necessary to increase free pollination levels. A secure atmosphere for

bees should be provided to produce healthy crops. The use of insecticides and pesticides

is damaging to human health because both crops and bee products become contaminated

with agrochemicals that humans must eventually ingest. Although the roles played by

non-bee pollinators cannot be ignored, bee pollination remains a precious asset that

should be protected. Bee pollination must be enhanced not only to improve environmen-

tal balance but also to maintain food security worldwide. The role played by bees is im-

portant for worldwide crops and certain medicinal plants, with significant effects on

quantity and quality. Researchers should focus their attention on studying the impacts

that bees have on crop quality, which should provide more detailed data regarding how

bees can alter the chemistry of certain crops.

Author Contributions: Conceptualization, H.R.E.-S.; validation, H.R.E.-S. and S.A.M.K.; writing—

original draft preparation, E.H.E., A.A.S. and A.A.A.E.-W.; writing—review and editing, S.A.M.K.,

A.F.A., S.G.M., M.F.A., C.Z., S.H.D.M., M.M.A.-D., M.F.H., G.K., Y.A.-N., M.B., M.A.M.D. and

H.R.E.-S.; supervision, H.R.E.-S.; funding acquisition, H.R.E.-S. All authors have read and agreed to

the published version of the manuscript.

Funding: This work was supported by the Swedish Research Council Vetenskapsrådet (VR Grant

2016–05885).

Institutional Review Board Statement: Not applicable.

Informed Consent Statement: Not applicable

Insects 2021, 12, 688 17 of 25

Data Availability Statement: No new data were created or analyzed in this study. Data sharing is

not applicable to this article.

Acknowledgments: Authors are very grateful to the Swedish Research links Grant VR 2016–05885

and the Department of Molecular Biosciences, Wenner-Grens Institute, Stockholm University, Swe-

den, for the financial support.

Conflicts of Interest: The authors declare no conflict of interest.

References

1. Gill, R.J.; Baldock, K.C.; Brown, M.J.; Cresswell, J.E.; Dicks, L.V.; Fountain, M.T.; Garratt, M.P.; Gough, L.A.; Heard, M.S.; Hol-

land, J.M.O.J. Protecting an ecosystem service: approaches to understanding and mitigating threats to wild insect pollinators.

Adv. Ecol. Res. 2016, 54, 135–206, doi:10.1016/bs.aecr.2015.10.007.

2. Breeze, T.D.; Bailey, A.P.; Balcombe, K.G.; Potts, S.G. Pollination services in the UK: How important are honeybees? Agric.

Ecosyst. Environ. 2011, 142, 137–143, doi:10.1016/j.agee.2011.03.020.

3. Hristov, P.; Neov, B.; Shumkova, R.; Palova, N. Significance of apoidea as main pollinators. Ecological and economic impact

and implications for human nutrition. Diversity 2020, 12, 280–294, doi:10.3390/d12070280.

4. Sukumaran, A.; Khanduri, V.P.; Sharma, C.M. Pollinator-mediated self-pollination and reproductive assurance in an isolated

tree of Magnolia grandiflora L. Ecol. Process. 2020, 9, 45–53, doi:10.1186/s13717-020-00254-5.

5. García-Breijo, F.; Armiñana, J. R.; Garmendia, A.; Cebrián, N.; Beltrán, R.; Merle, H. In vivo pollen tube growth and evidence of

self-pollination and prefloral anthesis in cv. Macabeo (Vitis vinifera L.). Agriculture 2020, 10, 647–659.

6. MacInnis, G.; Forrest, J.R.K. Field design can affect cross-pollination and crop yield in strawberry (Fragaria x ananassa D.). Agric.

Ecosyst. Environ. 2020, 289, 106738–106745, doi:10.1016/j.agee.2019.106738.

7. Lobo, J.A.; Quesada, M.; Stoner, K.E. Effects of pollination by bats on the mating system of Ceiba pentandra (Bombacaceae) pop-

ulations in two tropical life zones in Costa Rica. Am. J. Bot. 2005, 92, 370–376, doi:10.3732/ajb.92.2.370.

8. Zeng, X.; Fischer, G.A. Wind pollination over 70 years reduces the negative genetic effects of severe forest fragmentation in the

tropical oak Quercus bambusifolia. Heredity (Edinb). 2020, 124, 156–169, doi:10.1038/s41437-019-0258-3.

9. van der Kooi, C.J.; Ollerton, J. The origins of flowering plants and pollinators. Science (80-. ). 2020, 368, 1306–1308, doi:10.1126/sci-

ence.aay3662.

10. Gallai, N.; Salles, J.M.; Settele, J.; Vaissière, B.E. Economic valuation of the vulnerability of world agriculture confronted with

pollinator decline. Ecol. Econ. 2009, 68, 810–821, doi:10.1016/j.ecolecon.2008.06.014.

11. Meena, N.K.; Lal, G.; Meena, R.S.; Meena, B.M.; Meena, R.D. Pollinator’s diversity and abundance on cumin (Cuminum cyminum

L.) and their impact on yield enhancement at semi-arid regions. J. Entomol. Zool. Stud. 2018, 6, 1017–1021.

12. Abd El-Wahab, T.E.; Ebadah, I.M.A.; Mahmoud, Y.A. Insect pollinators of anise plants (Pimpinella anisum L.) and the important

role of honey bees (Apis mellifera L.) on their yield productivity. Arch. Phytopathol. Plant Prot. 2012, 45, 677–685,

doi:10.1080/03235408.2011.591161.

13. Chambó, E.D.; Garcia, R.C.; de Oliveira, N.T.E.; Duarte-Júnior, J.B. Honey bee visitation to sunflower: Effects on pollination and

plant genotype. Sci. Agric. 2011, 68, 647–651, doi:10.1590/S0103-90162011000600007.

14. Patil, P.N.; Pastagia, J.J. Effect of bee pollination on yield of coriander, Coriandrum sativum Linnaeus. Int. J. Plant Prot. 2016, 9,

79–83.

15. Klein, A.M.; Vaissière, B.E.; Cane, J.H.; Steffan-Dewenter, I.; Cunningham, S.A.; Kremen, C.; Tscharntke, T. Importance of pol-

linators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 2007, 274, 303–313, doi:10.1098/rspb.2006.3721.

16. Calderone, N.W. Insect pollinated crops, insect pollinators and US agriculture: Trend analysis of aggregate data for the period

1992-2009. PLoS ONE 2012, 7, e37235, doi:10.1371/journal.pone.0037235.

17. Rader, R.; Bartomeus, I.; Garibaldi, L.A.; Garratt, M.P.D.; Howlett, B.G.; Winfree, R.; Cunningham, S.A.; Mayfield, M.M.; Arthur,

A.D.; Andersson, G.K.S.; et al. Non-bee insects are important contributors to global crop pollination. Proc. Natl. Acad. Sci. USA

2016, 113, 146–151, doi:10.1073/pnas.1517092112.

18. Stanley, D.A.; Msweli, S.M.; Johnson, S.D. Native honeybees as flower visitors and pollinators in wild plant communities in a

biodiversity hotspot. Ecosphere 2020, 11, e02957, doi:10.1002/ecs2.2957.

19. Rao, S.; Stephen, W.P. Bumble bee pollinators in red clover seed production. Crop Sci. 2009, 49, 2207–2214, doi:10.2135/crop-

sci2009.01.0003.

20. Bänsch, S.; Tscharntke, T.; Gabriel, D.; Westphal, C. Crop pollination services: Complementary resource use by social vs solitary

bees facing crops with contrasting flower supply. J. Appl. Ecol. 2021, 58, 476–485, doi:10.1111/1365-2664.13777.

21. Greenleaf, S.S.; Kremen, C. Wild bees enhance honey bees’ pollination of hybrid sunflower. Proc. Natl. Acad. Sci. USA 2006, 103,

13890–13895, doi:10.1073/pnas.0600929103.

22. Giannini, T.C.; Cordeiro, G.D.; Freitas, B.M.; Saraiva, A.M.; Imperatriz-Fonseca, V.L. The dependence of crops for pollinators

and the economic value of pollination in Brazil. J. Econ. Entomol. 2015, 108, 849–857, doi:10.1093/jee/tov093.

23. Potts, S.G.; Imperatriz-Fonseca, V.; Ngo, H.T.; Aizen, M.A.; Biesmeijer, J.C.; Breeze, T.D.; Dicks, L. V.; Garibaldi, L.A.; Hill, R.;

Settele, J.; et al. Safeguarding pollinators and their values to human well-being. Nature 2016, 540, 220–229, doi:10.1038/na-

ture20588.

Insects 2021, 12, 688 18 of 25

24. Lautenbach, S.; Seppelt, R.; Liebscher, J.; Dormann, C.F. Spatial and temporal trends of global pollination benefit. PLoS One

2012, 7, e35954, doi:10.1371/journal.pone.0035954.

25. Aizen, M.A.; Garibaldi, L.A.; Cunningham, S.A.; Klein, A.M. How much does agriculture depend on pollinators? Lessons from

long-term trends in crop production. Ann. Bot. 2009, 103, 1579–1588, doi:10.1093/aob/mcp076.

26. Montoya, D.; Gaba, S.; de Mazancourt, C.; Bretagnolle, V.; Loreau, M. Reconciling biodiversity conservation, food production

and farmers’ demand in agricultural landscapes. Ecol. Modell. 2020, 416, 108889-108909., doi:10.1016/j.ecolmodel.2019.108889.

27. Geeraert, L.; Aerts, R.; Berecha, G.; Daba, G.; De Fruyt, N.; D’hollander, J.; Helsen, K.; Stynen, H.; Honnay, O. Effects of land-

scape composition on bee communities and coffee pollination in Coffea arabica production forests in southwestern Ethiopia.

Agric. Ecosyst. Environ. 2020, 288, 106706–106717, doi:10.1016/j.agee.2019.106706.

28. Luo, D.; Silva, D.P.; De Marco Júnior, P.; Pimenta, M.; Caldas, M.M. Model approaches to estimate spatial distribution of bee

species richness and soybean production in the Brazilian Cerrado during 2000 to 2015. Sci. Total Environ. 2020, 737, 139674,

doi:10.1016/j.scitotenv.2020.139674.

29. Sáez, A.; Aizen, M.A.; Medici, S.; Viel, M.; Villalobos, E.; Negri, P. Bees increase crop yield in an alleged pollinator-independent

almond variety. Sci. Rep. 2020, 10, 3177–3183, doi:10.1038/s41598-020-59995-0.

30. Losey, J.E.; Vaughan, M. The economic value of ecological services provided by insects. Bioscience 2006, 56, 311–323,

doi:10.1641/0006-3568(2006)56[311:tevoes]2.0.co;2.

31. Esquivel, I.L.; Coulson, R.N.; Brewer, M.J. A native bee, melissodes tepaneca (Hymenoptera: Apidae), benefits cotton produc-

tion. Insects 2020, 11, 487–497, doi:10.3390/insects11080487.

32. Stein, K.; Coulibaly, D.; Stenchly, K.; Goetze, D.; Porembski, S.; Lindner, A.; Konaté, S.; Linsenmair, E.K. Bee pollination in-

creases yield quantity and quality of cash crops in Burkina Faso, West Africa. Sci. Rep. 2017, 7, 17691–17700, doi:10.1038/s41598-

017-17970-2.

33. Kasina, J.M.; Mburu, J.; Kraemer, M.; Holm-Mueller, K. Economic benefit of crop pollination by bees: A case of kakamega small-

holder farming in Western Kenya. J. Econ. Entomol. 2009, 102, 467–473, doi:10.1603/029.102.0201.

34. Hipólito, J.; Sousa, B. dos S.B.; Borges, R.C.; Brito, R.M. de; Jaffé, R.; Dias, S.; Imperatriz Fonseca, V.L.; Giannini, T.C. Valuing

nature’s contribution to people: The pollination services provided by two protected areas in Brazil. Glob. Ecol. Conserv. 2019, 20,

e00782, doi:10.1016/j.gecco.2019.e00782.

35. Orges, R.C.B.; Rito, R.M.B.; Onseca, V.L.I.M.; Iannini, T.C.G. The value of crop production and pollination services in the Eastern

Amazon. Neotrop. Entomol. 2020, 49, 545–556.

36. Reilly, J.R.; Artz, D.R.; Biddinger, D.; Bobiwash, K.; Boyle, N.K.; Brittain, C.; Brokaw, J.; Campbell, J.W.; Daniels, J.; Elle, E.; et

al. Crop production in the USA is frequently limited by a lack of pollinators. Proc. R. Soc. B Biol. Sci. 2020, 287, 20200922–

20200930, doi:10.1098/rspb.2020.0922.

37. Hall, M.A.; Jones, J.; Rocchetti, M.; Wright, D.; Rader, R. Bee visitation and fruit quality in berries under protected cropping

vary along the length of polytunnels. J. Econ. Entomol. 2020, 113, 1337–1346, doi:10.1093/jee/toaa037.

38. Valido, A.; Rodríguez-Rodríguez, M.C.; Jordano, P. Honeybees disrupt the structure and functionality of plant-pollinator net-

works. Sci. Rep. 2019, 9, 4711–4721.

39. Garantonakis, N.; Varikou, K.; Birouraki, A.; Edwards, M.; Kalliakaki, V.; Andrinopoulos, F. Comparing the pollination services

of honey bees and wild bees in a watermelon field. Sci. Hortic. (Amsterdam) 2016, 204, 138–144, doi:10.1016/j.scienta.2016.04.006.

40. Hung, K.-L.J.; Kingston, J.M.; Albrecht, M.; Holway, D.A.; Kohn, J.R. The worldwide importance of honey bees as pollinators

in natural habitats. Proc. R. Soc. B Biol. Sci. 2018, 285, 20172140–20172147.

41. Streinzer, M.; Brockmann, A.; Nagaraja, N.; Spaethe, J. Sex and caste-specific variation in compound eye norphology of five

honeybee species. PLoS ONE 2013, 8, e57702, doi:10.1371/journal.pone.0057702.

42. Shin, D.; Choi, W.T.; Lin, H.; Qu, Z.; Breedveld, V.; Meredith, J.C. Humidity-tolerant rate-dependent capillary viscous adhesion

of bee-collected pollen fluids. Nat. Commun. 2019, 10, 1–9, doi:10.1038/s41467-019-09372-x.

43. Ghosh, S.; Jeon, H.; Jung, C. Foraging behaviour and preference of pollen sources by honey bee (Apis mellifera) relative to protein

contents. J. Ecol. Environ. 2020, 44, 4–10, doi:10.1186/s41610-020-0149-9.

44. Seo, H.J.; Song, J.; Yoon, H.J.; Lee, K.Y. Effects of nectar contents on the foraging activity of honeybee (Apis mellifera) on Asian

pear (Pyrus pyrifolia Nakai). Sci. Hortic. (Amsterdam) 2019, 245, 185–192, doi:10.1016/j.scienta.2018.10.009.

45. Morse, R.A. and Calderone, N.W. The value of honey bees as pollinators of U.S. crops in 2000. Bee Cult. 2000, 128, 1–15,

doi:10.1021/bi00697a007.

46. Naumann, K.; Winston, M.L.; Slessor, K.N.; Smirle, M.J. Synthetic honey bee (Hymenoptera: Apidae) queen mandibular gland

pheromone applications affect pear and sweet cherry pollination. J. Econ. Entomol. 1994, 87, 1595–1599, doi:10.1093/jee/87.6.1595.

47. Rajagopal, D.; Eswarappa, G..; Raju, A.J.S. Pollination potentiality of honeybees in increasing productivity of guava in Karna-

taka. In Today and Tomorrow’s Printers & Publishers, New Delhi, India; 2005; pp. 131–141 ISBN 8173715173.

48. Meléndez-Ramírez, V.; Parra-Tabla, V.; Kevan, P.G.; Ramírez-Morillo, I.; Harries, H.; Fernández-Barrera, M.; Zizumbo-Villareal,

D. Mixed mating strategies and pollination by insects and wind in coconut palm (Cocos nucifera L. (Arecaceae)): Importance in

production and selection. Agric. For. Entomol. 2004, 6, 155–163, doi:10.1111/j.1461-9563.2004.00216.x.

49. Ewies, M.A.; EL-Sahhar, K.F. Observations on the behaviour of honeybees on onion and their effects on seed yield. J. Apic. Res.

1977, 16, 194–196, doi:10.1080/00218839.1977.11099886.

Insects 2021, 12, 688 19 of 25

50. Bartomeus, I.; Potts, S.G.; Steffan-Dewenter, I.; Vaissière, B.E.; Woyciechowski, M.; Krewenka, K.M.; Tscheulin, T.; Roberts,

S.P.M.; Szentgyörgyi, H.; Westphal, C.; et al. Contribution of insect pollinators to crop yield and quality varies with agricultural

intensification. PeerJ 2014, 2014, e328–e347, doi:10.7717/peerj.328.

51. Abd El-Wahab, T.E. and Ebadah, I.M.A. Impact of honeybee and other insect pollinators on the seed setting and yield produc-

tion of black cumin Nigella sativa L. J. Basic. Appl. Sci. Res 2011, 1, 622–626.

52. Saboor, N.; Muhammad, A.; Muhammad, A.R; Younisand, A. Role of pollinators in recommended and densely grown black

cumin (Nigella sativa L.) yield at Dera Ismail Khan. J. Entomol. Zool. Stud. 2018, 6, 983–986.

53. Bendifallah, L.; Louadi, K.; Doumandji, S. Bee fauna potential visitors of coriander flowers Coriandrum sativum L. (Apiaceae) in

the Mitidja area (Algeria). J. Apic. Sci. 2013, 57, 59–70, doi:10.2478/jas-2013-0017.

54. Geslin, B.; Aizen, M.A.; Garcia, N.; Pereira, A.; Vaissière, B.E. The impact of honey bee colony quality on crop yield and farmers

’ profit in apples and pears. Agric. Ecosyst. Environ. 2017, 248, 153–161, doi:10.1016/j.agee.2017.07.035.

55. Chautá-mellizo, A.; Campbell, S.A.; Argenis, M.; Thaler, J.S.; Poveda, K. Effects of natural and artificial pollination on fruit and

offspring quality. Basic Appl. Ecol. 2012, 13, 524–532, doi:10.1016/j.baae.2012.08.013.

56. Isaacs, R.; Kirk, A.K. Pollination services provided to small and large highbush blueberry fields by wild and managed bees. J.

Appl. Ecol. 2010, 47, 841–849, doi:10.1111/j.1365-2664.2010.01823.x.

57. Crowther, L.P.; Wright, D.J.; Richardson, D.S.; Carvell, C.; Bourke, A.F.G. Spatial ecology of a range-expanding bumble bee

pollinator. Ecol. Evol. 2019, 9, 986–997, doi:10.1002/ece3.4722.

58. Velthuis, H.H.W.; Van Doorn, A. A century of advances in bumblebee domestication and the economic and environmental

aspects of its commercialization for pollination. Apidologie 2006, 37, 421–451.

59. Peat, J.; Darvill, B.; Ellis, J.; Goulson, D. Effects of climate on intra- and interspecific size variation in bumble-bees. Funct. Ecol.

2005, 19, 145–151, doi:10.1111/j.0269-8463.2005.00946.x.

60. Fijen, T.P.M.; Scheper, J.A.; Boom, T.M.; Janssen, N.; Raemakers, I.; Kleijn, D. Insect pollination is at least as important for mar-

ketable crop yield as plant quality in a seed crop. Ecol. Lett. 2018, 21, 1704–1713, doi:10.1111/ele.13150.

61. Nayak, R.K.; Rana, K.; Sharma, H.K.; Rana, V.S.; Thakur, M. Influence of bumble bee pollination on quantitative and qualitative

parameters of kiwifruit. Indian J. Hortic. 2019, 76, 294–299.

62. Shipp, J.L.; Whitfield, G.H.; Papadopoulos, A.P. Effectiveness of the bumble bee, Bombus impatiens Cr.(Hymenoptera: Apidae),

as a pollinator of greenhouse sweet pepper. Sci. Hortic. (Amsterdam) 1994, 57, 29–39.

63. Roldán Serrano, A.; Guerra-Sanz, J.M. Quality fruit improvement in sweet pepper culture by bumblebee pollination. Sci. Hortic.

(Amsterdam) 2006, 110, 160–166, doi:10.1016/j.scienta.2006.06.024.

64. Desjardins, È.C.; De Oliveira, D. Commercial bumble bee Bombus impatiens (Hymenoptera: Apidae) as a pollinator in lowbush

blueberry (Ericale: Ericaceae) fields. J. Econ. Entomol. 2006, 99, 443–449, doi:10.1093/jee/99.2.443.

65. Yankit, P.; Rana, K.; Kumar Sharma, H.; Thakur, M.; Thakur, R.K. Effect of bumble bee pollination on quality and yield of

Tomato (Solanum lycopersicum Mill.) grown under protected conditions. Int. J. Curr. Microbiol. Appl. Sci. 2018, 7, 257–263,

doi:10.20546/ijcmas.2018.701.028.

66. Normandeau Bonneau, M.; Samson-Robert, O.; Fournier, V.; Chouinard, G. Commercial bumble bee (Bombus impatiens) hives

under exclusion netting systems for apple pollination in orchards. Renew. Agric. Food Syst. 2020, 1–11,

doi:10.1017/S1742170520000095.

67. Quezada-Euán, J.J.G. Stingless Bees of Mexico. In Stingless Bees of Mexico: The Biology, Management and Conservation of an Ancient

Heritage; Springer: New York, NY, USA; 2018; pp. 1–37, ISBN 9783319777849.

68. Ramírez, V.M.; Ayala, R.; González, H.D. Crop pollination by stingless bees. In Pot-Pollen in Stingless Bee Melittology; Springer:

Cham, Switzerland, 2018; pp. 139–153.

69. Eickwort, G.C.; Ginsberg, H.S. Foraging and mating behavior in Apoidea. Annu. Rev. Entomol. 1980, 25, 421–446.

70. De Luca, P.A.; Vallejo-Marín, M. What’s the “buzz” about? The ecology and evolutionary significance of buzz-pollination. Curr.

Opin. Plant Biol. 2013, 16, 429–435, doi:10.1016/j.pbi.2013.05.002.

71. Del Sarto, M.C.L.; Peruquetti, R.C.; Campos, L.A.O. Evaluation of the neotropical stingless bee Melipona quadrifasciata (Hyme-

noptera: Apidae) as pollinator of greenhouse tomatoes. J. Econ. Entomol. 2005, 98, 260–266, doi:10.1093/jee/98.2.260.

72. Solange, A.B.S.; Ana, C.R.; Luci, R.B. Pollination of Cucumber Cucumis sativus L. (Cucurbitales: Cucurbitaceae), by the stingless

bees Scaptotrigona aff. depili Moure and Nannotrigona testaceicornis Lepeletier (Hymenoptera: Meliponini) in greenhouses. Ne-

otrop. Entomol. 2008, 37, 506–512.

73. Azmi, W.A.; Ghazi, R.; Sultan, U.; Abidin, Z.; Chuah, T.; Mara, U.T. Effects of stingless bee (Heterotrigona itama) pollination on

greenhouse cucumber (Cucumis sativus). Malaysian Appl. Biol. 2017, 46, 51–55.

74. Azmi, W.A.; Sembok, W.Z.W.; Yusuf, N.; Hatta, M.F.M.; Salleh, A.F.; Hamzah, M.A.H.; Ramli, S.N. Effects of pollination by the

indo-Malaya stingless bee (Hymenoptera: Apidae) on the quality of greenhouse- produced rockmelon. J. Econ. Entomol. 2019,

112, 20–24, doi:10.1093/jee/toy290.

75. Roselino, A.C.; Santos, S.B.; Hrncir, M.; Bego, L.R. Differences between the quality of strawberries (Fragaria x ananassa) polli-

nated by the stingless bees Scaptotrigona aff. depilis and Nannotrigona testaceicornis. Genet. Mol. Res. 2009, 8, 539–545.

76. Ilva, P.N.U.; Rncir, M.H.; Inês, C.; Ilva, S. Stingless bees, Melipona fasciculata, as efficient pollinators of eggplant (Solanum

melongena) in greenhouses. Apidology 2013, 44, 537–546, doi:10.1007/s13592-013-0204-y.

77. Leys, R.; Cooper, S.J.B.; Schwarz, M.P. Molecular phylogeny of the large carpenter bees, genus Xylocopa (Hymenoptera: Api-

dae), based on mitochondrial DNA sequences. Mol. Phylogenet. Evol. 2000, 17, 407–418, doi:10.1006/mpev.2000.0851.

Insects 2021, 12, 688 20 of 25

78. Somanathan, H.; Saryan, P.; Balamurali, G.S. Foraging strategies and physiological adaptations in large carpenter bees. J. Comp.

Physiol. A Neuroethol. Sensory, Neural, Behav. Physiol. 2019, 205, 387–398, doi:10.1007/s00359-019-01323-7.

79. Keasar, T. Large carpenter bees as agricultural pollinators. Psyche A J. Entomol. 2010, 2010, 1–7.

80. Richards, M.H. Built environments influence carpenter bee sociality and vice versa. Insectes Soc. 2020, 67, 201–202,

doi:10.1007/s00040-020-00767-4.

81. Raju, A.J.S.; Rao, S.P. Nesting habits, floral resources and foraging ecology of large carpenter bees (Xylocopa latipes and Xylocopa

pubescens) in India. Curr. Sci. 2006, 1210–1217.

82. Halder, S.; Ghosh, S.; Khan, R.; Khan, A.A.; Perween, T.; Hasan, M.A. Role of pollination in fruit crops: A review. Pharma Innov.

J. 2019, 8, 695–705.

83. Jr, W.B.B.; Trinidad, K.A.D.; Presas, J.A. Hand pollination and natural pollination by carpenter bees (Xylocopa spp.) in Passiflora

edulis Sims. f. flavicarpa Deg. (yellow passion fruit). J. Apic. Res. 2020, doi:10.1080/00218839.2020.1842580 To,

doi:10.1080/00218839.2020.1842580.

84. Silveira, M. V; Abot, A.R.; Nascimento, J.N.; Rodrigues, E.T. Is manual pollination of yellow passion fruit completely dispensa-

ble? Sci. Hortic. (Amsterdam) 2012, 146, 99–103.

85. Hogendoorn, K.; Steen, Z.; Schwarz, M.P. Native Australian carpenter bees as a potential alternative to introducing bumble

bees for tomato pollination in greenhouses. J. Apic. Res. 2000, 39, 67–74, doi:10.1080/00218839.2000.11101023.

86. Adi, S.; Avi, S.; Tamar, K. The carpenter bee Xylocopa pubescens as an agricultural pollinator in greenhouses. Apidologie 2007,

38, 508–517.

87. Batra SW. Solitary bees. Sci. Am. 1984, 250, 120-127.

88. Biesmeijer, J.C.; Roberts, S.P.M.; Reemer, M.; Ohlemüller, R.; Edwards, M.; Peeters, T.; Schaffers, A.P.; Potts, S.G.; Kleukers, R.;

Thomas, C.D. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science (80-.). 2006,

313, 351–354.

89. Kleijn, D.; Winfree, R.; Bartomeus, I.; Carvalheiro, L.G.; Henry, M.; Isaacs, R.; Klein, A.M.; Kremen, C.; M’Gonigle, L.K.; Rader,

R.; et al. Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat. Commun. 2015,

6, 1–9, doi:10.1038/ncomms8414.

90. Garratt, M.P.D.; Breeze, T.D.; Boreux, V.; Fountain, M.T.; McKerchar, M.; Webber, S.M.; Coston, D.J.; Jenner, N.; Dean, R.; West-

bury, D.B.; et al. Apple pollination: Demand depends on variety and supply depends on pollinator identity. PLoS ONE 2016,

11, e0153889, doi:10.1371/journal.pone.0153889.

91. Khan, M.R.; Khan, M.R.. The role of honey bees Apis mellifera L. (Hymenoptera: Apidae) in pollination of apple. Pakistan J. Biol.

Sci. 2004, 7, 359–362.

92. Wu, P.; Tscharntke, T.; Westphal, C.; Wang, M.; Olhnuud, A.; Xu, H.; Yu, Z.; van der Werf, W.; Liu, Y. Bee abundance and soil

nitrogen availability interactively modulate apple quality and quantity in intensive agricultural landscapes of China. Agric.

Ecosyst. Environ. 2021, 305, 107168–107176, doi:10.1016/j.agee.2020.107168.

93. Viana, B.F.; da Encarnacao Coutinho, J.G.; Garibaldi, L.A.; Braganca Castagnino, G.L.; Gramacho, K.P.; Oliveira Silva, F. Sting-

less bees further improve apple pollination and production. J. Pollinat. Ecol. 2014, 14, 261–269, doi:10.26786/1920-7603(2014)26.

94. Mallinger, R.E.; Gratton, C. Species richness of wild bees, but not the use of managed honeybees, increases fruit set of a polli-

nator-dependent crop. J. Appl. Ecol. 2015, 52, 323–330, doi:10.1111/1365-2664.12377.

95. Free, J.B.; Raw, A.; Williams, I.H. Pollination of coconut (Cocos nucifera L.) in Jamaica by honeybees and wasps. Appl. Anim.

Ethol. 1975, 1, 213–223.

96. Walters, S.A. Honey bee pollination requirements for triploid watermelon. HortScience 2005, 40, 1268–1270,

doi:10.21273/hortsci.40.5.1268.

97. Boyle, N.K.; Pitts-Singer, T.L. Assessing blue orchard bee (Osmia lignaria) propagation and pollination services in the presence

of honey bees (Apis mellifera) in Utah tart cherries. PeerJ 2019, 7, e7639, doi:10.7717/peerj.7639.

98. Holzschuh, A.; Dudenhöffer, J.H.; Tscharntke, T. Landscapes with wild bee habitats enhance pollination, fruit set and yield of

sweet cherry. Biol. Conserv. 2012, 153, 101–107, doi:10.1016/j.biocon.2012.04.032.

99. Bosch, J.; Osorio-Canadas, S.; Sgolastra, F.; Vicens, N. Use of a managed solitary bee to pollinate almonds: Population sustain-

ability and increased fruit set. Insects 2021, 12, 1–11, doi:10.3390/insects12010056.

100. Peña, J.F.; Carabalí, A. Effect of honey bee (Apis mellifera L.) density on pollination and fruit set of avocado (Persea Americana

Mill.) cv. Hass. J. Apic. Sci. 2018, 62, 5–14, doi:10.2478/JAS-2018-0001.

101. Popak, A.E.; Markwith, S.H.; Strange, J. Economic valuation of bee pollination services for passion fruit (Malpighiales: passiflo-

raceae) cultivation on smallholding Farms in São Paulo, Brazil, using the avoided cost method. J. Econ. Entomol. 2019, 112, 2049–

2054, doi:10.1093/jee/toz169.

102. Malerbo-Souza, D.T.; Nogueira-Couto, R.H.; Couto, L.A. Honey bee attractants and pollination in sweet orange, Citrus sinensis

(L.) Osbeck, var. Pera-Rio. J. Venom. Anim. Toxins Incl. Trop. Dis. 2004, 10, 144–153, doi:10.1590/s1678-91992004000200004.

103. Deuri, A.; Rahman, A.; Gogoi, J.; Borah, P.; Bathari, M. Pollinator diversity and effect of Apis cerana F. pollination on yield of

mango (Mangifera indica L.). J. Entomol. Zool. Stud. 2018, 6, 957–961.

104. Klatt, B.K.; Holzschuh, A.; Westphal, C.; Clough, Y.; Smit, I.; Pawelzik, E.; Tscharntke, T. Bee pollination improves crop quality,

shelf life and commercial value. Proc. Biol. Sci. 2014, 281, 20132440–20132447, doi:10.1098/rspb.2013.2440.

Insects 2021, 12, 688 21 of 25

105. Herrmann, J.D.; Beye, H.; de la Broise, C.; Hartlep, H.; Diekötter, T. Positive effects of the pollinators Osmia cornuta (Megachi-

lidae) and Lucilia sericata (Calliphoridae) on strawberry quality. Arthropod. Plant. Interact. 2019, 13, 71–77, doi:10.1007/s11829-

018-9636-7.

106. Howpage, D.; Spooner-Hart, R.N.; Vithanage, V. Influence of honey bee (Apis mellifera) on kiwifruit pollination and fruit quality

under Australian conditions. New Zeal. J. Crop Hortic. Sci. 2001, 29, 51–59, doi:10.1080/01140671.2001.9514160.

107. Greenleaf, S.S.; Kremen, C. Wild bee species increase tomato production and respond differently to surrounding land use in

Northern California. Biol. Conserv. 2006, 133, 81–87, doi:10.1016/j.biocon.2006.05.025.

108. Neto, S.; Lima, F.G.; Gonçalves, B.B.; Lima Bergamini, L.; Araújo, B.; Bergamini, R.; Antônio, M.; Elias, S.; Franceschinelli, E.V.

Native bees pollinate tomato flowers and increase fruit production. J. Pollinat. Ecol. 2013, 11, 41–45.

109. Munawar, M.S.; Sarwar, G.; Raja, S.; Waghchoure, E.S.; Iftikhar, F.; Mahmood, R. Pollination by honeybee (Apis mellifera) in-

creases seed setting and yield in black seed (Nigella sativa). Int. J. Agric. Biol. 2009, 11, 611–615.

110. Radford, B.J.; Nielsen, R.G.H.; Rhodes, J.W. Agents of pollination in sunflower crops on the central darling downs, queensland.

Aust. J. Exp. Agric. 1979, 19, 565–569.

111. Pires, V.C.; Silveira, F.A.; Sujii, E.R.; Torezani, K.R.S.; Rodrigues, W.A.; Albuquerque, F.A.; Rodrigues, S.M.M.; Salomao, A.N.;

Soares Pires, C.S. Importance of bee pollination for cotton production in conventional and organic farms in Brazil. J. Pollinat.

Ecol. 2014, 13, 151–160, doi:10.26786/1920-7603(2014)20.

112. Nicodemo, D.; Couto, R.H.N.; Malheiros, E.B.; de Jong, D. Honey bee as an effective pollinating agent of pumpkin. Sci. Agric.

2009, 66, 476–480, doi:10.1590/s0103-90162009000400007.

113. Blettler, D.C.; Fagúndez, G.A.; Caviglia, O.P. Contribution of honeybees to soybean yield. Apidologie 2018, 49, 101–111,

doi:10.1007/s13592-017-0532-4.

114. Milfont, M. de O.; Rocha, E.E.M.; Lima, A.O.N.; Freitas, B.M. Higher soybean production using honeybee and wild pollinators,

a sustainable alternative to pesticides and autopollination. Environ. Chem. Lett. 2013, 11, 335–341.

115. Krishnan, S.; Kushalappa, C.G.; Shaanker, R.U.; Ghazoul, J. Status of pollinators and their efficiency in coffee fruit set in a

fragmented landscape mosaic in South India. Basic Appl. Ecol. 2012, 13, 277–285, doi:10.1016/j.baae.2012.03.007.

116. Asiwe, J.A.N. Insect mediated outcrossing and geneflow in cowpea (Vigna unguiculata (L.) Walp): Implication for seed produc-

tion and provision of containment structures for genetically transformed cowpea. African J. Biotechnol. 2009, 8, 226–230,

doi:10.4314/ajb.v8i2.59773.

117. Barrios, B.; Pena, S.R.; Salas, A.; Koptur, S. Butterflies visit more frequently, but bees are better pollinators: The importance of

mouthpart dimensions in effective pollen removal and deposition. AoB Plants 2016, 8, doi:10.1093/aobpla/plw001.

118. Mandal, E.; Amin, M.R.; Rahman, H.; Akanda, A.M. Abundance and foraging behavior of native insect pollinators and their

effect on mustard (Brassica juncea L.). Bangladesh J. Zool 2018, 46, 117–123, doi:10.1111/j.1365-2311.2010.01247.x.

119. Stanley, J.; Sah, K.; Subbanna, A.R.N.S. How efficient is the Asian honey bee, Apis cerana in pollinating mustard, Brassica cam-

pestris var. toria? Pollination behavior, pollinator efficiency, pollinator requirements and impact of pollination. J. Apic. Res. 2017,

56, 439–451, doi:10.1080/00218839.2017.1329796.

120. Klein, A.M.; Steffan-Dewenter, I.; Tscharntke, T. Fruit set of highland coffee increases with the diversity of pollinating bees.

Proc. R. Soc. B Biol. Sci. 2003, 270, 955–961, doi:10.1098/rspb.2002.2306.

121. Muto, N.A.; Leite, R.O. de S.; Pereira, D.S.; Rogez, H.L.G.; Venturieri, G.C. Impact of the introduction of stingless bee colonies

(Scaptotrigona aff. postica) on the productivity of acai (Euterpe oleracea). Rev. Verde Agroecol. Desenvolv. Sustentável 2020, 15, 265–

273, doi:10.18378/rvads.v15i3.8404.

122. Jauker, F.; Bondarenko, B.; Becker, H.C.; Steffan-Dewenter, I. Pollination efficiency of wild bees and hoverflies provided to

oilseed rape. Agric. For. Entomol. 2012, 14, 81–87, doi:10.1111/j.1461-9563.2011.00541.x.

123. Perrot, T.; Gaba, S.; Roncoroni, M.; Gautier, J.L.; Bretagnolle, V. Bees increase oilseed rape yield under real field conditions.

Agric. Ecosyst. Environ. 2018, 266, 39–48, doi:10.1016/j.agee.2018.07.020.

124. Bloch, D.; Werdenberg, N.; Erhardt, A. Pollination crisis in the butterfly-pollinated wild carnation Dianthus carthusianorum? New

Phytol. 2006, 169, 699–706, doi:10.1111/j.1469-8137.2006.01653.x.

125. Pashte, V.V.; Kulkarni, S.R. Role of pollinators in qualitative fruit crop production: A review. Trends Biosci. 2015, 8, 3743–3749.

126. Papiorek, S.; Junker, R.R.; Alves-dos-Santos, I.; Melo, G.A.R.; Amaral-Neto, L.P.; Sazima, M.; Wolowski, M.; Freitas, L.; Lunau,

K. Bees, birds and yellow flowers: Pollinator-dependent convergent evolution of UV patterns. Plant Biol. 2016, 18, 46–55.

127. Bauer, A.A.; Clayton, M.K.; Brunet, J. Floral traits influencing plant attractiveness to three bee species: Consequences for plant

reproductive success. Am. J. Bot. 2017, 104, 772–781, doi:10.3732/ajb.1600405.

128. Hennessy, G.; Harris, C.; Eaton, C.; Wright, P.; Jackson, E.; Goulson, D.; Ratnieks, F.F.L.W. Gone with the wind: effects of wind

on honey bee visit rate and foraging behaviour. Anim. Behav. 2020, 161, 23–31.

129. Whitney, H.M.; Chittka, L.; Bruce, T.J.A.; Glover, B.J. Conical epidermal cells allow bees to grip flowers and increase foraging

efficiency. Curr. Biol. 2009, 19, 948–953.

130. Rachersberger, M.; Cordeiro, G.D.; Schäffler, I.; Dötterl, S. Honeybee pollinators use visual and floral scent cues to find apple

(Malus domestica) flowers. J. Agric. Food Chem. 2019, 67, 13221–13227, doi:10.1021/acs.jafc.9b06446.

131. Varassin, I.G.; Trigo, J.R.; Sazima, M. The role of nectar production, flower pigments and odour in the pollination of four species

of Passiflora (Passifloraceae) in south-eastern Brazil. Bot. J. Linn. Soc. 2001, 136, 139–152.

Insects 2021, 12, 688 22 of 25

132. Gresty, C.E.A.; Clare, E.; Devey, D.S.; Cowan, R.S.; Csiba, L.; Malakasi, P.; Lewis, O.T.; Willis, K.J. Flower preferences and pollen

transport networks for cavity-nesting solitary bees: Implications for the design of agri-environment schemes. Ecol. Evol. 2018, 8,

7574–7587, doi:10.1002/ece3.4234.

133. Prado, S.G.; Collazo, J.A.; Marand, M.H.; Irwin, R.E. The influence of floral resources and microclimate on pollinator visitation

in an agro-ecosystem. Agric. Ecosyst. Environ. 2021, 307, 107196–107204, doi:10.1016/j.agee.2020.107196.

134. Bradshaw, H.D.; Schemske, D.W. Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers.

Nature 2003, 426, 176–178.

135. Handelman, C.; Kohn, J.R. Hummingbird color preference within a natural hybrid population of Mimulus aurantiacus

(Phrymaceae). Plant Species Biol. 2014, 29, 65–72, doi:10.1111/j.1442-1984.2012.00393.x.

136. Giurfa, M.; Núñez, J.; Chittka, L.; Menzel, R. Colour preferences of flower-naive honeybees. J. Comp. Physiol. A 1995, 177, 247–

259, doi:10.1007/BF00192415.

137. Hill, P.S.M.; Wells, P.H.; Wells, H. Spontaneous flower constancy and learning in honey bees as a function of colour. Anim.

Behav. 1997, 54, 615–627, doi:10.1006/anbe.1996.0467.

138. Chen, Z.; Liu, C.Q.; Sun, H.; Niu, Y. The ultraviolet colour component enhances the attractiveness of red flowers of a bee-

pollinated plant. J. Plant Ecol. 2020, 13, 354–360, doi:10.1093/jpe/rtaa023.

139. Alcorn, K.; Whitney, H.; Glover, B. Flower movement increases pollinator preference for flowers with better grip. Funct. Ecol.

2012, 26, 941–947, doi:10.1111/j.1365-2435.2012.02009.x.

140. Whitney, H.M.; Poetes, R.; Steiner, U.; Chittka, L.; Glover, B.J. Determining the contribution of epidermal cell shape to petal

wettability using isogenic antirrhinum lines. PLoS ONE 2011, 6, e17576, doi:10.1371/journal.pone.0017576.

141. Giuliani, C.; Giovanetti, M.; Lupi, D.; Mesiano, M.P.; Barilli, R.; Ascrizzi, R.; Flamini, G.; Fico, G. Tools to tie: Flower character-

istics, voc emission profile, and glandular trichomes of two mexican salvia species to attract bees. Plants 2020, 9, 1645–1661,

doi:10.3390/plants9121645.

142. Solís-Montero, L.; Cáceres-García, S.; Alavez-Rosas, D.; García-Crisóstomo, J.F.; Vega-Polanco, M.; Grajales-Conesa, J.; Cruz-

López, L. Pollinator preferences for floral volatiles emitted by dimorphic anthers of a buzz-pollinated herb. J. Chem. Ecol. 2018,

44, 1058–1067, doi:10.1007/s10886-018-1014-5.

143. Makino, T.T.; Ohashi, K.; Sakai, S. How do floral display size and the density of surrounding flowers influence the likelihood

of bumble bee revisitation to a plant? Funct. Ecol. 2007, 21, 87–95, doi:10.1111/j.1365-2435.2006.01211.x.

144. Shrestha, M.; Garcia, J.E.; Burd, M.; Dyer, A.G. Australian native flower colours: Does nectar reward drive bee pollinator flower

preferences? PLoS ONE 2020, 15, e0226469, doi:10.1371/journal.pone.0226469.

145. Perera, R. A. S. N.; Karunaratne, W.A.I.P. Floral visits of the wild bee, lithurgus atratus, impact yield and seed germinability of

okra, abelmoschus esculentus, in sri lanka. Pollinat. Ecol. 2019, 25, 1–6.

146. Mallinger, R.E.; Prasifka, J.R. Bee visitation rates to cultivated sunflowers increase with the amount and accessibility of nectar

sugars. J. Appl. Entomol. 2017, 141, 561–573, doi:10.1111/jen.12375.

147. Rowe, L.; Gibson, D.; Bahlai, C.A.; Gibbs, J.; Landis, D.A.; Isaacs, R. Flower traits associated with the visitation patterns of bees.

Oecologia 2020, 193, 511–522, doi:10.1007/s00442-020-04674-0.

148. Robertson, A.W.; Mountjoy, C.; Faulkner, B.E.; Roberts, M. V.; Macnair, M.R. Bumble bee selection of Mimulus guttatus flowers:

The effects of pollen quality and reward depletion. Ecology 1999, 80, 2594–2606, doi:10.1890/0012-

9658(1999)080[2594:bbsomg]2.0.co;2.

149. Mallinger, R.E.; Franco, J.G.; Prischmann-Voldseth, D.A.; Prasifka, J.R. Annual cover crops for managed and wild bees: Optimal

plant mixtures depend on pollinator enhancement goals. Agric. Ecosyst. Environ. 2019, 273, 107–116,

doi:10.1016/j.agee.2018.12.006.

150. Urbanowicz, C.; Muñiz, P.A.; McArt, S.H. Honey bees and wild pollinators differ in their preference for and use of introduced

floral resources. Ecol. Evol. 2020, 10, 6741–6751, doi:10.1002/ece3.6417.

151. Ropars, L.; Dajoz, I.; Fontaine, C.; Muratet, A.; Geslin, B. Wild pollinator activity negatively related to honey bee colony densities

in urban context. PLoS ONE 2019, 14, e0222316, doi:10.1371/journal.pone.0222316.

152. Pritchard, D.J.; Vallejo-Marín, M. Floral vibrations by buzz-pollinating bees achieve higher frequency, velocity and acceleration

than flight and defence vibrations. J. Exp. Biol. 2020, 223, doi:10.1242/jeb.220541.

153. Pritchard, D.J.; Vallejo-marín, M. Quick guide Buzz pollination ll. Curr. Biol. 2020, 30, R858–R860, doi:10.1016/j.cub.2020.05.087.

154. Luca, P.A. De; Cox, D.A.; Vallejo-marín, M. Comparison of pollination and defensive buzzes in bumblebees indicates species-

specific and context-dependent vibrations. Naturwissenschaften 2014, 101, 331–338, doi:10.1007/s00114-014-1161-7.

155. Vallejo-Marín, M. Buzz pollination: Studying bee vibrations on flowers. New Phytol. 2019, 224, 1068–1074,

doi:10.1111/nph.15666.

156. Russell, A.L.; Leonard, A.S.; Gillette, H.D.; Papaj, D.R. Concealed floral rewards and the role of experience in floral sonication

by bees. Anim. Behav. 2016, 120, 83–91, doi:10.1016/j.anbehav.2016.07.024.

157. Corbet, S.A.; Huang, S.-Q. Buzz pollination in eight bumblebee-pollinated Pedicularis species: Does it involve vibration-induced

triboelectric charging of pollen grains? Ann. Bot. 2014, 114, 1665–1674.

158. Cardinal, S.; Buchmann, S.L.; Russell, A.L. The evolution of floral sonication, a pollen foraging behavior used by bees (Anthoph-

ila). Evolution (N. Y). 2018, 72, 590–600, doi:10.1111/evo.13446.

159. Wcislo, W.T.; Tierney, S.M. Behavioural environments and niche construction: The evolution of dim-light foraging in bees. Biol.

Rev. 2009, 84, 19–37, doi:10.1111/j.1469-185X.2008.00059.x.

Insects 2021, 12, 688 23 of 25

160. Ma, W.; Li, X.; Shen, J.; Du, Y.; Xu, K.; Jiang, Y. Transcriptomic analysis reveals Apis mellifera adaptations to high temperature

and high humidity. Ecotoxicol. Environ. Saf. 2019, 184, 109599, doi:10.1016/j.ecoenv.2019.109599.

161. Dolezal, A.G.; Toth, A.L. Feedbacks between nutrition and disease in honey bee health. Curr. Opin. Insect Sci. 2018, 26, 114–119,

doi:10.1016/j.cois.2018.02.006.

162. Huang, Z.Y.; Giray, T. Factors affecting pollinators and pollination. Psyche 2012, 2012, doi:10.1155/2012/302409.

163. Christopher Brown, J.; Albrecht, C. The effect of tropical deforestation on stingless bees of the genus Melipona (Insecta: Hyme-

noptera: Apidae: Meliponini) in central Rondonia, Brazil. J. Biogeogr. 2001, 28, 623–634, doi:10.1046/j.1365-2699.2001.00583.x.

164. Yang, D.; Xu, X.; Zhao, H.; Yang, S.; Wang, X.; Zhao, D.; Diao, Q.; Hou, C. Diverse factors affecting efficiency of RNAi in honey

bee viruses. Front. Genet. 2018, 9, 384–392, doi:10.3389/fgene.2018.00384.

165. O’Neal, S.T.; Swale, D.R.; Anderson, T.D. ATP-sensitive inwardly rectifying potassium channel regulation of viral infections in

honey bees. Sci. Rep. 2017, 7, 8668–8676.

166. van Engelsdorp, D.; Evans, J.D.; Saegerman, C.; Mullin, C.; Haubruge, E.; Nguyen, B.K.; Frazier, M.; Frazier, J.; Cox-Foster, D.;

Chen, Y.; et al. Colony collapse disorder: A descriptive study. PLoS ONE 2009, 4, e6481, doi:10.1371/journal.pone.0006481.

167. van Dooremalen, C.; van Langevelde, F. Can colony size of honeybees (Apis mellifera) be used as predictor for colony losses due

to varroa destructor during winter? Agriculture1 2021, 11, 529–539, doi:10.3390/agriculture11060529.

168. Snow, J.W.; Ceylan Koydemir, H.; Karinca, D.K.; Liang, K.; Tseng, D.; Ozcan, A. Rapid imaging, detection, and quantification

of Nosema ceranae spores in honey bees using mobile phone-based fluorescence microscopy. Lab Chip 2019, 19, 789–797,

doi:10.1039/c8lc01342j.

169. Conroy, T.J.; Palmer-Young, E.C.; Irwin, R.E.; Adler, L.S. Food limitation affects parasite load and survival of Bombus impatiens

(Hymenoptera: Apidae) infected with Crithidia (Trypanosomatida: Trypanosomatidae). Environ. Entomol. 2016, 45, 1212–1219,

doi:10.1093/ee/nvw099.

170. Han, W.; Yang, Y.; Gao, J.; Zhao, D.; Ren, C.; Wang, S.; Zhao, S.; Zhong, Y. Chronic toxicity and biochemical response of Apis

cerana cerana (Hymenoptera: Apidae) exposed to acetamiprid and propiconazole alone or combined. Ecotoxicology 2019, 28, 399–

411, doi:10.1007/s10646-019-02030-4.

171. Christen, V.; Kunz, P.Y.; Fent, K. Endocrine disruption and chronic effects of plant protection products in bees: Can we better

protect our pollinators? Environ. Pollut. 2018, 243, 1588–1601, doi:10.1016/j.envpol.2018.09.117.

172. Arce, A.N.; Ramos Rodrigues, A.; Yu, J.; Colgan, T.J.; Wurm, Y.; Gill, R.J. Foraging bumblebees acquire a preference for neon-

icotinoid-treated food with prolonged exposure. Proceedings. Biol. Sci. 2018, 285, 8–11, doi:10.1098/rspb.2018.0655.

173. Woodcock, B.A.; Isaac, N.J.B.; Bullock, J.M.; Roy, D.B.; Garthwaite, D.G.; Crowe, A.; Pywell, R.F. Impacts of neonicotinoid use

on long-term population changes in wild bees in England. Nat. Commun. 2016, 7, doi:10.1038/ncomms12459.

174. Jiang, J.; Ma, D.; Zou, N.; Yu, X.; Zhang, Z.; Liu, F.; Mu, W. Concentrations of imidacloprid and thiamethoxam in pollen, nectar and

leaves from seed-dressed cotton crops and their potential risk to honeybees (Apis mellifera L.); Elsevier Ltd.: Amsterdam, The Nether-

lands, 2018; Vol. 201; ISBN 8605388242.

175. Tosi, S.; Nieh, J.C.; Sgolastra, F.; Cabbri, R.; Medrzycki, P. Neonicotinoid pesticides and nutritional stress synergistically reduce

survival in honey bees. Proc. R. Soc. B Biol. Sci. 2017, 284, 20171711–20171719.

176. Tomé, H.V.V.; Ramos, G.S.; Araújo, M.F.; Santana, W.C.; Santos, G.R.; Guedes, R.N.C.; Maciel, C.D.; Newland, P.L.; Oliveira,

E.E. Agrochemical synergism imposes higher risk to neotropical bees than to honeybees. R. Soc. Open Sci. 2017, 4, 160866,

doi:10.1098/rsos.160866.

177. Vanegas, M. The silent beehive: How the decline of honey bee populations shifted the environmental protection agency’s pes-

ticide policy towards pollinators. Ecol. Law Q. 2017, 44, 311–342.

178. Rortais, A.; Arnold, G.; Dorne, J. Lou; More, S.J.; Sperandio, G.; Streissl, F.; Szentes, C.; Verdonck, F. Risk assessment of pesti-

cides and other stressors in bees: Principles, data gaps and perspectives from the European Food Safety Authority. Sci. Total

Environ. 2017, 587–588, 524–537, doi:10.1016/j.scitotenv.2016.09.127.

179. Tschoeke, P.H.; Oliveira, E.E.; Dalcin, M.S.; Silveira-Tschoeke, M.C.A.C.; Sarmento, R.A.; Santos, G.R. Botanical and synthetic

pesticides alter the flower visitation rates of pollinator bees in Neotropical melon fields. Environ. Pollut. 2019, 251, 591–599,

doi:10.1016/j.envpol.2019.04.133.

180. Liporoni, R.; Cordeiro, G.D.; Prado, P.I.; Schlindwein, C.; Warrant, E.J.; Alves-dos-Santos, I. Light intensity regulates flower

visitation in Neotropical nocturnal bees. Sci. Rep. 2020, 10, 1–11, doi:10.1038/s41598-020-72047-x.

181. Kenefic, N.E.; González, P.L.; Theodorou, P.; Cardona, E. Disentangling the effects of local resources, landscape heterogeneity

and climatic seasonality on bee diversity and plant - pollinator networks in tropical highlands. Oecologia 2020, 1–12,

doi:10.1007/s00442-020-04715-8.

182. Grassl, J.; Holt, S.; Cremen, N.; Peso, M.; Hahne, D.; Baer, B. Synergistic effects of pathogen and pesticide exposure on honey

bee (Apis mellifera) survival and immunity. J. Invertebr. Pathol. 2018, 159, 78–86, doi:10.1016/j.jip.2018.10.005.

183. Dalsgaard, B. Land-use and climate impacts on plant-pollinator interactions and pollination services. Diversity 2020, 12, 168–

170, doi:10.3390/D12050168.

184. Jacques, A.; Laurent, M.; Consortium, E.; Ribière-Chabert, M.; Saussac, M.; Bougeard, S.; Budge, G.E.; Hendrikx, P.; Chauzat,

M.-P. A pan-European epidemiological study reveals honey bee colony survival depends on beekeeper education and disease

control. PLoS ONE 2017, 12, e0172591.

185. Cook, D.F.; Voss, S.C.; Finch, J.T.D.; Rader, R.C.; Cook, J.M.; Spurr, C.J. The role of flies as pollinators of horticultural crops: An

Australian case study with worldwide relevance. Insects 2020, 11, 23–31, doi:10.3390/insects11060341.

Insects 2021, 12, 688 24 of 25

186. Larson, B.M.H.; Kevan, P.G.; Inouye, D.W. Flies and flowers: Taxonomic diversity of anthophiles and pollinators. Can. Entomol.

2001, 133, 439–465, doi:10.4039/Ent133439-4.

187. Hodgkiss, D.; Brown, M.J.F.; Fountain, M.T. Syrphine hoverflies are effective pollinators of commercial strawberry. J. Pollinat.

Ecol. 2018, 22, 55–66, doi:10.26786/1920-7603(2018)five.

188. Jauker, F.; Wolters, V. Hover flies are efficient pollinators of oilseed rape. Oecologia 2008, 156, 819–823, doi:10.1007/s00442-008-

1034-x.

189. Howlett, B.G.; Gee, M. The potential management of the drone fly (Eristalis tenax) as a crop pollinator in New Zealand. New

Zeal. Plant Prot. 2019, 72, 221–230, doi:10.30843/nzpp.2019.72.304.

190. Schittenhelm, S.; Gladis, T.; Rao, V.R. Efficiency of various insects in germplasm regeneration of carrot, onion and turnip rape

accessions. Plant Breed. 1997, 116, 369–375, doi:10.1111/j.1439-0523.1997.tb01014.x.

191. Jarlan, A.; De Oliveira, D.; Gingras, J. Pollination of sweet pepper (Capsicum annuum L.) in green-house by the syrphid fly

Eristalis tenax (L.). Acta Hortic. 1997, 437, 335–339.

192. Barbattini, R.; Greatti, M.; Zandigiacomo, P.; Costa, G.; Testolin, R.; Vizzotto, G. Insect pollinators of kiwifruit and their role in

crop pollination. In Proceedings of the Atti XVII Congresso Nazionale Italiano di Entomologia, Udine, Italy, 13–18 June 1994;

pp. 13–18.

193. Hahn, M.; Brühl, C.A. The secret pollinators: An overview of moth pollination with a focus on Europe and North America.

Arthropod. Plant. Interact. 2016, 10, 21–28, doi:10.1007/s11829-016-9414-3.

194. Santos, R. da S.; Milfont, M. de O.; Silva, M.M.; Carneiro, L.T.; Castro, C.C. Butterflies provide pollination services to macadamia

in northeastern Brazil. Sci. Hortic. (Amsterdam) 2020, 259, 108818–108825, doi:10.1016/j.scienta.2019.108818.

195. Martins, D.J. Butterfly pollination of the dryland wildflower gloriosa minor. J. East African Nat. Hist. 2014, 103, 25–30,

doi:10.2982/028.103.0103.

196. Cruden, R.W.; Hermann-parker, S.M. Butterfly pollination of Caesalpinia pulcherrima, with observations on a psychophilous

syndrome. Br. Ecol. Soc. 1979, 67, 155–168.

197. Pinto, C.E.; Oliveira, R.; Schlindwein, C. Do consecutive flower visits within a crown diminish fruit set in mass-flowering Han-

cornia speciosa (Apocynaceae)? Plant Biol. 2008, 10, 408–412.

198. Barrios, B.; Koptur, S. Floral biology and breeding system of Angadenia berteroi (Apocynaceae): Why do flowers of the pineland

golden trumpet produce few fruits? Int. J. Plant Sci. 2011, 172, 378–385, doi:10.1086/658153.

199. Gann, G.D.; Woodmansee, S.W.; Bradley, K.A. Conserving rare plants in locally-protected urban forest fragments: A case study

from Miami-Dade County, Florida. Urban For. Urban Greening. 2020, 20, 1–11.

200. Macgregor, C.J.; Pocock, M.J.O.; Fox, R.; Evans, D.M. Pollination by nocturnal Lepidoptera, and the effects of light pollution: A

review. Ecol. Entomol. 2015, 40, 187–198, doi:10.1111/een.12174.

201. Ricketts, T.H.; Regetz, J.; Steffan-Dewenter, I.; Cunningham, S.A.; Kremen, C.; Bogdanski, A.; Gemmill-Herren, B.; Greenleaf,

S.S.; Klein, A.M.; Mayfield, M.M.; et al. Landscape effects on crop pollination services: Are there general patterns? Ecol. Lett.

2008, 11, 499–515, doi:10.1111/j.1461-0248.2008.01157.x.

202. Power, A.G. Ecosystem services and agriculture: Tradeoffs and synergies. Philos. Trans. R. Soc. B Biol. Sci. 2010, 365, 2959–2971,

doi:10.1098/rstb.2010.0143.

203. Alarcón, R.; Davidowitz, G.; Bronstein, J.L. Nectar usage in a southern Arizona hawkmoth community. Ecol. Entomol. 2008, 33,

503–509, doi:10.1111/j.1365-2311.2008.00996.x.

204. Devoto, M.; Bailey, S.; Memmott, J. The “night shift”: Nocturnal pollen-transport networks in a boreal pine forest. Ecol. Entomol.

2011, 36, 25–35, doi:10.1111/j.1365-2311.2010.01247.x.

205. Sime, K.R.; Baldwin, I.T. Predominantly self-fertilizing native tobacco. BMC Ecol. 2003, 3, 6–14.

206. Armstrong, J.E.; Irvine, A.K. Floral biology of Myristica insipida (Myristicaceae), a distinctive beetle pollination syndrome. Am.

J. Bot. 1989, 76, 86–94, doi:10.2307/2444777.

207. Bernhardt, P. Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. Pl Syst. Evol. 2000, 222, 293–320,

doi:10.1007/BF00984108.

208. Dieringer, G.; R, L.C.; Lara, M.; Loya, L.; Reyes, P.; Journal, I.; Dieringer, G.; R, L.C.; Lara, M.; Loya, L.; et al. Beetle pollination

and floral thermogenicity in Magnolia tamaulipana (Magnoliaceae). Int. J. Plant Sci. 1999, 160, 64–71.

209. Mayer, C.; Soka, G.; Picker, M. The importance of monkey beetle (Scarabaeidae: Hopliini) pollination for Aizoaceae and Aster-

aceae in grazed and ungrazed areas at Paulshoek, Succulent Karoo, South Africa. J. Insect Conserv. 2006, 10, 323–333,

doi:10.1007/s10841-006-9006-0.

210. Devy, M.S.; Davidar, P. Pollination systems of trees in Karachi, a mid-elevation wet evergreen forest in Western Ghats, India.

Am. J. Bot. 2003, 90, 650–657, doi:10.3732/ajb.90.4.650.

211. Momose, K.; Yumoto, T.; Nagamitsu, T.; Kato, M.; Nagamasu, H.; Sakai, S.; Harrison, R.D.; Itioka, T.; Hamid, A.A.; Inoue, T.

Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community

in a lowland dipterocarp forest. Am. J. Bot. 1998, 85, 1477–1501, doi:10.2307/2446404.

212. Colville, J.; Picker, M.D.; Cowling, R.M. Species turnover of monkey beetles (Scarabaeidae: Hopliini) along environmental and

disturbance gradients in the Namaqualand region of the succulent Karoo, South Africa. Biodivers. Conserv. 2002, 11, 243–264,

doi:10.1023/A:1014520226989.

213. Van Kleunen, M.; Nänni, I.; Donaldson, J.S.; Manning, J.C. The role of beetle marks and flower colour on visitation by monkey

beetles (Hopliini) in the greater c\ ape Floral Region, South Africa. Ann. Bot. 2007, 100, 1483–1489, doi:10.1093/aob/mcm256.

Insects 2021, 12, 688 25 of 25

214. Sayers, T.D.J.; Steinbauer, M.J.; Miller, R.E. Visitor or vector? The extent of rove beetle (Coleoptera: Staphylinidae) pollination

and floral interactions. Arthropod. Plant. Interact. 2019, 13, 685–701, doi:10.1007/s11829-019-09698-9.

215. Suetsugu, K. Social wasps, crickets and cockroaches contribute to pollination of the holoparasitic plant Mitrastemon yamamotoi

(Mitrastemonaceae) in southern Japan. Plant Biol. 2019, 21, 176–182.

216. Ananthakrishnan, T.N. Thrips and pollination biology. Ananthakrishnan, T. N. 1982, 51, 168–172.

217. Infante, F.; Ortíz, J.A.; Solis-Montero, L.; Mound, L.A.; Vega, F.E. Thrips (Thysanoptera) of coffee flowers. Ann. Entomol. Soc.

Am. 2017, 110, 329–336.

218. Resende, J.J.; Santos, G.M. de M.; Bichara Filho, C.C.; Gimenes, M. Atividade diária de busca de recursos pela vespa social

Polybia occidentalis occidentalis (Olivier, 1791)(Hymenoptera, Vespidae). Rev. Bras. Zoociências 2001, 3, 105–115.

219. Beggs, J. The ecological consequences of social wasps (Vespula spp.) invading an ecosystem that has an abundant carbohydrate

resource. Biol. Conserv. 2001, 99, 17–28.

220. Schremmer, F. Wespen und Hornissen (Wittenberg Lutherstadt, Germany: A. Ziemsen Verlag). 1962.

221. Brodmann, J.; Twele, R.; Francke, W.; Hölzler, G.; Zhang, Q.H.; Ayasse, M. Orchids mimic green-leaf volatiles to attract prey-

hunting wasps for pollination. Curr. Biol. 2008, 18, 740–744, doi:10.1016/j.cub.2008.04.040.

222. Jakubska-Busse, A.; Przado, D.; Steininger, M.; Aniolł-Kwiatkowska, J.; Kadej, M. Why do pollinators become “sluggish”?

Nectar chemical constituents from Epipactis helleborine (L.) crantz (Orchidaceae). Appl. Ecol. Environ. Res. 2005, 3, 29–38,

doi:10.15666/aeer/0302_029038.

Increasing Welfare of Honey Bees: Sweet Spot for Violence Prevention

Chapter

Full-text available

Apr 2025

Anne H. Outwater

This chapter describes the current plight of honey bees, focusing on Apis mellifera, who are exploited for food and medicine, pollination, and as sentinels, and to decrease violence; they also serve as cultural inspiration and are an important interface between humans and non-humans. In spite of their importance and willingness to work with human beings, honey harvesting, beekeeping, and bee farming are often violent and destructive operations. Many, if not most, honey bees die by human hands wielding fire, pesticides, diseases, and poor care. In addition, many Apis mellifera spp. are moved into ecosystems to which they are not native, and through their essential act of collecting pollen and nectar, disrupt those ecosystems. Collecting bee products is done through honey-hunting, natural beekeeping, and industrialized bee farming. Bee farming is highly associated with pesticides, disease, and displacing local pollinators. To work less violently and more peacefully with Apis mellifera spp., humans need to de-emphasize industrialized bee farming and emphasize natural beekeeping with native bees. In natural beekeeping, bee health is achieved by rejuvenating local ecosystems with foraging plants and allows periodic swarming. Beekeepers should be supported with simple tools and training to employ harvesting practices that decrease aggressive defense responses of bees. This will result in less violent, more peaceful interactions between humans and honey bees, as well as help stabilize ecosystems.

Fungicide consumption exacerbates the negative effects of a common gut parasite in bumble bee microcolonies

Article

Full-text available

Apr 2025

Bumble bees face numerous environmental stressors, including gut-parasite infection and exposure to agricultural fungicides, which can negatively impact colony health. This study evaluates the interactive effects of these stressors on bumble bee (Bombus impatiens) microcolonies, focusing on colony development, worker survival and parasite infection dynamics. Our aim in evaluating these interactions was to determine if bees would experience synergistic negative health outcomes compared to single- stressor exposures. We reared 40 queenless bumble bee microcolonies, and treated them with either fungicide-contaminated pollen, inoculation with a gut parasite, both, or neither. Contrary to original expectations, we did not observe significant synergistic interactions between the two stressors; however, we found that consumption of fungicide was associated with higher likelihood of gut-parasite infection, and delayed recovery from infection. Fungicide consumption was also connected to smaller workers, and smaller male offspring. We also found that gut-parasite infection was correlated with decreased pollen consumption overall, decreased worker survival and fewer developed pupae. This study provides insights into the impacts of co-occurring stressors affecting bumble bees and emphasizes the importance of sublethal effects on pollinator health.

De novo genome assemblies of the dwarf honey bee subgenus Micrapis: Apis andreniformis and Apis florea

Preprint

Full-text available

Apr 2025

The Micrapis subgenus, which includes the black dwarf honey bee (Apis andreniformis) and the red dwarf honey bee (Apis florea), remains underrepresented in genomic studies despite its ecological significance. Here, we present high-quality de novo genome assemblies for both species, generated using a hybrid sequencing approach combining Oxford Nanopore Technologies (ONT) long reads with Illumina short reads. The final assemblies are highly contiguous, with contig N50 values of 5.0 Mb (A. andreniformis) and 4.3 Mb (A. florea), representing a major improvement over the previously published A. florea genome. Genome completeness assessments indicate high quality, with BUSCO scores exceeding 98.5% and k-mer analyses supporting base-level accuracy. Repeat annotation revealed a relatively low repetitive sequence content (~6%), consistent with other Apis species. Using RNA sequencing data, we annotated 12,232 genes for A. andreniformis and 12,597 genes for A. florea, with >97% completeness in predicted proteomes. These genome assemblies provide a valuable resource for comparative and functional genomic studies, offering new insights into the genetic basis of dwarf honey bee adaptations.

A method for detecting transgenic rapeseed using pollen collected by Apis mellifera L

Article

Full-text available

Apr 2025
TRANSGENIC RES

With the continuous expansion of the planting area of genetically modified (GM) crops, the demand for efficient and comprehensive monitoring systems is becoming increasingly urgent. To establish a method suitable for large-scale monitoring of genetically modified rapeseed planting, beehives were strategically deployed at specific locations around genetically modified rapeseed fields, and the TaqMan quantitative PCR (qPCR) method was used to detect and analyze the genetically modified components in the rapeseed pollen collected by bees. The results demonstrated that the average Ct values for the CaMV35S promoter, Bar gene, NPTII gene, and HPT gene in the pollen of each hive were 27.91, 29.58, 31.49, and 31.97, respectively. The average ΔCt values for these four genes in hive pollen from 100 to 200 m were − 0.35, 1.66, 2.58, and 5.06, respectively, which were significantly lower than those from 300 to 1100 m (2.85, 4.01, 6.66, and 5.63). The results of this study have demonstrated the feasibility of using pollen collected by bees for large-scale detection of genetically modified rapeseed plants. This early warning model for GM crop spread based on bee pollination provides an efficient and practical solution for monitoring and managing genetically modified crops.

RNA metagenomics revealed insights into the viromes of honey bees (Apis mellifera) and Varroa mites (Varroa destructor) in Taiwan

Article

Apr 2025

Botanical origin and volatile organic compounds contents of bee bread from four Brazilian regions

Article

Apr 2025

Comparison of the toxicity and potential ecological risks of various pesticides for nurses of honey bee (Apis mellifera. L)

Article

Apr 2025

Taiwan Green Propolis Nanoparticles Induce Antiproliferation and Apoptosis in Oral Cancer Cells

Article

Apr 2025

Introduction: Taiwan green propolis (TGP) is rich in prenylflavonoids and exhibits antioxidant, antibacterial, antiviral, and antitumour properties. It induces apoptosis in various cancer cells, making it a highly promising natural medicine. Although the health benefits and food applications of TGP are widely recognised, no study has explored its effects on Taiwan oral cancer cells (OECM1). This study investigated whether TGP induces apoptosis in OECM1 cells. Methods: High-performance liquid chromatography (HPLC), thin-layer chromatography, and liquid chromatography/mass spectrometry were used to identify the components in TGP and the fruit peel of Macaranga tanarius. The inhibitory activities of TGP dissolved in DMSO (TGPDMSO) and encapsulated in food-grade zein nanoparticles (TGPNP) against OECM1 cells were compared using MTT assays. The morphological changes, cell cycle analysis, and protein expression profiles of OECM1 cells after the TGP treatments were performed using microscopy, flow cytometry, and Western blot, respectively. Results: An MTT assay of TGPDMSO-treated OECM1 cells suggested an IC50 of 12.6 µg/mL, demonstrating that TGPDMSO exhibits significant cytotoxicity. Subsequent MTT assays revealed TGPNP’s cytotoxicity against OECM1 with an IC50 of 11.6 µg/mL. Flow cytometry revealed that TGPNP induced a cell arrest in S phase and DNA fragmentation. Western blotting analyses manifested an increase in Bax and cl-Casp9 and a decrease in Bcl2 and PARP. Conclusion: This study demonstrated that both TGPDMSO and TGPNP treatments induced apoptosis in OECM1 cells with a comparable IC50. Notably, utilising edible zein as a nanoparticle carrier for TGP mitigates the cytotoxicity risk associated with DMSO, providing a novel and safe approach for cancer treatment.

Honey Bee Breeding and Breed: Advancements, Challenges, and Prospects

Article

Full-text available

Apr 2025

Honey bees occupy a pivotal role in safeguarding ecological balance and bolstering the global agricultural economy through their indispensable pollination services. As the foremost commercial pollinator and producer of bee products, the western honey bees, Apis mellifera, have been extensively domesticated and managed worldwide. To harness their potential and enhance production traits, selective breeding practices are commonly implemented under human management. Nevertheless, despite the significance of these efforts, the foundational theories and concepts that underpin honey bee breeding remain fragmented. In this paper, we discuss the biological taxonomy of A. mellifera and the pertinent issues therein, emphasizing the necessity to recognize it as a domesticated animal and elucidate the concepts associated with livestock breeding. Drawing upon recent advances in the studies of honey bees and other domesticated species, we review the progress and challenges encountered in utilizing traditional breeding methods, which rely on phenotypic selection and natural mating, as well as marker‐assisted selections integrating modern biotechnological tools at the molecular level. Moreover, the utilization of gene‐editing tools in honey bee breeding is prospected, and the importance of reconciling bee breeding practices with conservation strategies is highlighted. Future research endeavors are anticipated to decipher the intricate genetic architecture underlying honey bee traits and develop precise genetic markers while weighing the ecological consequences of these breeding interventions. Through interdisciplinary collaboration and relentless innovation, robust technological support can be established to restore and protect honey bee populations, thereby ensuring the sustained vitality and contribution of this precious natural resource to our planet.

Genga Cramswel Oliver-Thesis NOV 2023

Thesis

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Apr 2025

Can Colony Size of Honeybees (Apis mellifera) Be Used as Predictor for Colony Losses Due to Varroa destructor during Winter?

Article

Full-text available

Jun 2021

For more than three decades, honeybee colonies (Apis mellifera) have experienced high losses during winter and these losses are still continuing. It is crucial that beekeepers monitor their colonies closely and anticipate losses early enough to apply mitigating actions. We tested whether colony size can be used as early predictor for potential colony losses, in particular due to the parasitic mite Varroa destructor. V. destructor is one of the most important causes of these losses. Such an early predictor for potential V. destructor induced losses is especially relevant as measuring V. destructor load in colonies is difficult and cumbersome. Over three years, we monitored colonies with high and low V. destructor loads from July until March of the next year. We found that differences in colony size were only visible after November, even though we lost almost all colonies every winter in the group with a high V. destructor load. In the Northern hemisphere, November is considered to be too late for beekeepers to strengthen colonies in preparation for winter. We therefore argue that early warning signs for potential colony losses due to V. destructor are urgently needed to allow beekeepers to prevent winter losses. We discuss the role of precision apiculture in monitoring the health and productivity of beehive colonies.

Use of a Managed Solitary Bee to Pollinate Almonds: Population Sustainability and Increased Fruit Set

Article

Full-text available

Jan 2021

Osmia spp. are excellent orchard pollinators but evidence that their populations can be sustained in orchard environments and their use results in increased fruit production is scarce. We released an Osmia cornuta population in an almond orchard and measured its population dynamics, as well as visitation rates and fruit set at increasing distances from the nesting stations. Honeybees were 10 times more abundant than O. cornuta. However, the best models relating fruit set and bee visitation included only O. cornuta visitation, which explained 41% and 40% of the initial and final fruit set. Distance from the nesting stations explained 27.7% and 22.1% of the variability in initial and final fruit set. Of the 198 females released, 99 (54.4%) established and produced an average of 9.15 cells. Female population growth was 1.28. By comparing our results with those of previous O. cornuta studies we identify two important populational bottlenecks (female establishment and male-biased progeny sex ratios). Our study demonstrates that even a small population of a highly effective pollinator may have a significant impact on fruit set. Our results are encouraging for the use of Osmia managed populations and for the implementation of measures to promote wild pollinators in agricultural environments.

In Vivo Pollen Tube Growth and Evidence of Self-Pollination and Prefloral Anthesis in cv. Macabeo (Vitis vinifera L.)

Article

Full-text available

Dec 2020

Cultivar Macabeo is one of the most planted white grape varieties of northern Spain. A general agreement supports many Vitis vinifera cultivars possibly being self-fertile, although this seems to be a variety-dependent characteristic. No previous information about the mating system of cv. Macabeo was found. This study aimed to analyze its mating system and to compare the in vivo fertilization process with and without artificial cross-pollination. Two treatments were performed: emasculation and cross-pollination. The seed number was counted, and pollen tube growth was observed by microscopy. The results showed that cv. Macabeo is self-fertile and selfing probably occurs before the flower opens. Pollen was found over the stigma of flowers before capfall and ovule fertilization was observed even in emasculated flowers, which suggests that germination and pollen tube growth happened in a very early flower development stage. Cross-pollination increased the presence of the pollen tubes growing inside flowers but was not necessary for fruit set. Ovule fertilization was very fast as 24 h (h) were enough for pollen tubes to reach the end of stylar canals.

Tools to Tie: Flower Characteristics, VOC Emission Profile, and Glandular Trichomes of Two Mexican Salvia Species to Attract Bees

Article

Full-text available

Dec 2020

A plant can combine physical and chemical tools to interact with other organisms. Some are designed for pollinator attraction (i.e., colors and volatile organic compounds-VOCs); others can act to discourage herbivores (i.e., non-glandular trichomes). Few studies fully address available tools in a single species; notwithstanding, this information can be pivotal in understanding new interactions out of the home range. We characterized flower traits, emission profiles of constitutive compounds from flowers and leaves, micro-morphology of the glandular trichomes, and listed flower visitors of two Mexican bird-pollinated Salvia species (S. blepharophylla and S. greggii), growing in an Italian botanical garden. Flowers were highly variable in their morphometric characteristics. In both species, four trichome morphotypes with similar histochemistry and distribution were documented for leaves and flowers except the calyx abaxial side. The vegetative emission profiles were qualitatively more complex than the floral ones; however, common compounds occurring in high relative percentages were β-caryophyllene and germacrene D. Floral bouquets were dominated by limonene and β-pinene in S. greggii and by 1,8-cineole in S. blepharophylla. Two potential (non-bird) pollinators were especially abundant: small bees belonging to the genus Lasioglossum and large bees belonging to the species Xylocopa violacea. Our study highlights the plasticity of these plants, as well as tools that can be conveniently used to establish novel interactions.

The influence of floral resources and microclimate on pollinator visitation in an agro-ecosystem ☆

Article

Full-text available

Nov 2020
AGR ECOSYST ENVIRON

As agriculture expands to meet the needs of a growing global population, natural ecosystems are threatened by deforestation and habitat fragmentation. Tropical agroforestry systems offer a sustainable alternative to traditional agriculture by providing food for production while also supporting biodiversity and ecosystem services. Previous studies have shown that these systems may even improve crop pollination, but the mechanisms of how these improvements occur are still poorly understood. Using coffee as a focal crop, we explored how microcli-matic conditions affected nectar traits (sugar and caffeine concentration) important for pollinator visitation. We also studied how microclimate, floral traits, floral availability at the coffee plant level, availability of floral resources provided by other plant species in the agroecosystem ("neighborhood floral availability"), and the presence of other bees affected the amount of time bees spent foraging on coffee flowers and the proportion of coffee pollen carried on their bodies. We explored these factors using the two dominant coffee species farmed on Puerto Rico, Coffea canephora and C. arabica, under sun and shade management. We found that high nectar sugar concentration and temperature were important predictors of short floral visits (<15s), while increased numbers of bees and open coffee flowers were important predictors of longer floral visits (16-180 seconds). High nectar caffeine concentration was an important predictor of longer visits on C. arabica flowers while the opposite was observed for C. canephora flowers. For both species, high coffee floral availability was the main predicting factor for the proportion of coffee pollen on the bees' bodies. Surprisingly, neither neighborhood floral availability nor the type of coffee plantation (agroforest/shade or sun) were important predictors of bee visitation. These results suggest non-coffee flowering plants in coffee plantations were neither competitors nor facilitators of coffee plants for pollinators. Additionally, most of the bees surveyed were carrying ≥80 % pollen from one species (C. arabica or C. canephora), likely resulting in little heterospecific pollen deposition between Coffea and non-Coffea flowers. Shade trees in coffee plantations do not detract from pollinator visitation to coffee flowers, suggesting that the provision of multiple ecological and wildlife conservation benefits by shade trees is not in conflict with a grower's ability to maximize the benefits of insect pollination on fruit production.

Crop pollination services: Complementary resource use by social vs solitary bees facing crops with contrasting flower supply

Article

Full-text available

Nov 2020
J APPL ECOL

Many farmers are facing high economic risks if pollinator declines continue or temporal and spatial variation in wild bee communities cause reduced pollination services. Co‐flowering crops might compete for pollinators, while they also might facilitate the delivery of pollination services. This rarely studied topic is of particular interest with respect to the foraging decisions of bees from different functional groups and when more sparsely and mass‐flowering crops are in bloom at the same time. The abundance of honey bees, bumble bees and solitary bees in strawberry fields was quantified with transect walks along a gradient of oilseed rape (OSR) availability (product of OSR land cover and temporally changing OSR flower cover). We established a pollination experiment with pollination treatments (open‐, wind‐ and self‐pollination) to study the effects of insect pollination on strawberry fruit weight and quality. Changes in OSR availability exhibited contrasting effects on social versus solitary bees in strawberry fields. Bumble bees and honey bees were less abundant in strawberry fields when OSR availability was high, whereas solitary bees were facilitated. With more strawberry flowers, we found more bees in general. When flowers were open‐pollinated, they resulted in heavier fruits with better commercial grades compared to wind‐ and self‐pollinated flowers. A higher bee abundance enhanced the strawberry fruit weight and quality but depended on flower order and variety. Synthesis and applications. Sparsely flowering crops may compete with mass‐flowering crops for social bee pollinators, while solitary pollinators in the field might be evenly facilitated. To ensure best fruit weight and quality, it can be beneficial to support bee abundance in the field. While some social and solitary bee species can be managed for pollination services, wild bees, in particular solitary species, should be conserved and promoted for stable crop pollination services in dynamic agricultural landscapes.

Pollinator's diversity and abundance on cumin (Cuminum cyminum L.) and their impact on yield enhancement at semi-arid regions

Article

Full-text available

Jan 2018

The present investigation was conducted to study pollinator's diversity and abundance on cumin (Cuminum cyminum L.) and their impact on yield enhancement under semi-arid regions during 2015-16 and 2016-17 at research farm of ICAR-NRC on Seed Spices, Ajmer (Rajasthan), India. Cumin flowers were visited by 20 species of insects belonging to 11 families from 6 orders. Apoidea (62.4%) and Diptera (27.5%) were the two major groups comprising 89.9% of the total visitors. Apis florea was the most dominant species (31.2%) followed by A. mellifera (16.9%), A. dorsata (13.4%), Episyrphus balteatus (13.0%) and Musca sp. l (9.6%). A. mellifera and A. dorsata started foraging early at 8.00 h and A. florea at 9.00, peaked from 12.00 to 14.00 hr and declined drastically thereafter. Non-Apis pollinators were visited cumin flowers early morning by 6.00 hr with meagre in population and present throughout the day with two peaks between 11.00 to 13.00 hr, while E. balteatus reached to its peak at 15.00 hr. Most of floral visitors ceased their population and few were negligible at 18.00 hr. Population dynamics of most abundant pollinators were recorded during fourth week of February. A minimum yield of 364.50 kg/ha was recorded in caged plots without insect pollinators (control). Yields in open and bee pollinated plots were 515.30 and 510.41 kg/ha, with an increase of 41.37 and 40.03% over without insect pollinated plots, respectively but at par with each other. Maximum yield was in plots treated with bee attractant-Jaggery solution 10% (520.83 kg/ha) which was 42.88% higher over control and 1.07 and 2.04% higher over open pollinated and bee pollinated plots. Bee pollination also increased quality of cumin seed over control (WIP).

Hand pollination and natural pollination by carpenter bees (Xylocopa spp.) in Passiflora edulis Sims. f. flavicarpa Deg. (yellow passion fruit)

Article

Nov 2020
J APICULT RES

We investigated the fruit set and quality of yellow passion fruit subjected to hand and natural pollination by carpenter bees (Xylocopa spp.) in the Philippines. We also recorded the foraging behavior of the bees. A quadrat measuring 6 m x 7 m was marked in a yellow passion fruit plantation for the investigation. Two groups of 20 flowers that had been either hand pollinated or visited by the bees were followed to determine fruit set and quality. The hand pollinated flowers had significantly greater fruit set (15/20 versus 7/20), fruit weight, transverse diameter, longitudinal diameter, peel weight, number of seeds, and juice yield. Flowers that were self-pollinated by hand produced no fruit. Bee flower visit times and patterns were also investigated. The carpenter bees started visiting the passion fruit flowers from 7:00 AM to 5:00 PM, with peak visitation at 1:00 PM. The greatest mean duration of flower visits was observed at 11:00 AM (304 s), which coincided with the observed peak hour of flower opening. We observed random distances in the flight patterns of the carpenter bees, which was independent of flower distances (Kolmogorov-Smirnov test; µ=3.34 < σ²=7.91 vs. µ=2.40 > σ²=1.20). We conclude that passion fruit farmers can utilize supplemental hand pollination to increase yield when the main pollinators such as Xylocopa spp. are not available in sufficient numbers.

BUMBLE BEE SELECTION OF MIMULUS GUTTATUS FLOWERS: THE EFFECTS OF POLLEN QUALITY AND REWARD DEPLETION

Article

Dec 1999

Bee abundance and soil nitrogen availability interactively modulate apple quality and quantity in intensive agricultural landscapes of China

Article

Jan 2021
AGR ECOSYST ENVIRON

Bees provide important pollination services for crops, but pollination limitation is a common problem in agricultural landscapes worldwide. To promote ecological intensification in fruit production, more knowledge is needed concerning the interacting effects of insect pollination services and soil fertility on crop quality and quantity. We investigated the effects of three pollination treatments (open, self and hand pollination) on apple quantity and quality parameters. We also analyzed the effects of bee abundance (wild bees and managed honeybees (Apis mellifera)) and soil nitrogen on fruit quantity and quality, and the responses of bee abundance and species richness to landscape metrics. Apple fruit set and yield of open pollinated flowers increased by 57% and 25 t/ha (compared to bagged controls), respectively. Hand pollination further enhanced yields by 7 t/ha (compared to open pollination; i.e. to 39 t/ha), indicating pollination limitation in the orchards. Seed number was highest in open pollinated fruits, and increased with bee abundance if soil nitrogen was low, but decreased with bee abundance at high nitrogen levels, possibly due to higher flower density resulting in pollinator dilution effects. Higher seed numbers reduced the proportion of deformed apples and thus increased fruit quality. The percent of surrounding semi-natural habitats positively affected species richness of wild bees in apple orchards. We conclude that yield and quality of apples may benefit from ecological intensification comprising the augmentation of wild bees by semi-natural habitat and lowering of fertilizer inputs.