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Overview of Bee Pollination and Its Economic Value for Crop Production

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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.
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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
1,
*, Esraa H. Elshafiey
2
, Aya A. Shetaia
2
, Aida A. Abd El-Wahed
3
,
Ahmed F. Algethami
4
, Syed G. Musharraf
5
, Mohamed F. AlAjmi
6
,
Chao Zhao
7
, Saad H. D. Masry
8,9
,
Mohamed M. Abdel-Daim
10
, Mohammed F. Halabi
11
, Guoyin Kai
12
, Yahya Al Naggar
13,14
, Mokhtar Bishr
15
,
Mohamed A. M. Diab
16
and Hesham R. El-Seedi
2,17,18,
*
1
Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University,
S-10691 Stockholm, Sweden
2
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.)
3
Agricultural Research Centre, Department of Bee Research, Plant Protection Research Institute,
Giza 12627, Egypt; aidaabd.elwahed@arc.sci.eg
4
Alnahalaljwal Foundation Saudi Arabia, P.O. Box 617, Al Jumum 21926, Makkah, Saudi Arabia;
ahmed@alnahalaljwal.com.sa
5
International Center for Chemical and Biological Sciences, H.E.J. Research Institute of Chemistry, University
of Karachi, Karachi 75270, Pakistan; musharraf@iccs.edu
6
Department of Pharmacognosy, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia;
malajmii@ksu.edu.sa
7
College of Food Science, Fujian Agriculture and Forestry University, Fuzhou 350002, China; zhchao@live.cn
8
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
9
Abu Dhabi Agriculture and Food Safety Authority (ADAFSA), Al Ain 52150, United Arab Emirates
10
Pharmacology Department, Faculty of Veterinary Medicine, Suez Canal University, Ismailia 41522, Egypt;
abdeldaim.m@vet.suez.edu.eg
11
Al-Rayan Research and Innovation Center, Al-Rayan Colleges, Medina 42541, Saudi Arabia;
m.halabi@amc.edu.sa
12
Laboratory of Medicinal Plant Biotechnology, College of Pharmacy, Zhejiang Chinese Medical University,
Hangzhou 310053, China; kaiguoyin@zcmu.edu.cn
13
General Zoology, Institute for Biology, Martin Luther University Halle-Wittenberg, Hoher Weg 8,
06120 Halle, Germany; yehia.elnagar@science.tanta.edu.eg
14
Zoology Department, Faculty of Science, Tanta University, Tanta 31527, Egypt
15
Arab Company for Pharmaceuticals and Medicinal Plants, (Mepaco-Medifood), El-Sharqiya 11361, Egypt;
m-bishr@mepaco-pharma.net
16
EWG Company, Menoufia, Shebin El-Kom 32512, Egypt; Mmmdiab82@gmail.com
17
Pharmacognosy Group, Biomedical Centre, Department of Pharmaceutical Biosciences, Uppsala University,
Box 591, SE 75124 Uppsala, Sweden
18
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.
Copyright: © 2021 by the authors. Li-
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 beespollination 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 (
A
.
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 (
A
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.
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... Bees have a crucial role in natural 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 [62]. Plant pollination by more than one bee species, including honey bees, carpenter bees, stingless bees, bumble bees, longtongued bee, feral bees, social bees, and solitary bees, results in a better pollination/ vegetation process [24]. ...
... Plant pollination by more than one bee species, including honey bees, carpenter bees, stingless bees, bumble bees, longtongued bee, feral bees, social bees, and solitary bees, results in a better pollination/ vegetation process [24]. An estimated 5-8% of all global crop production would be lost without the pollination services provided by bees [62]. ...
... Ironically, in Europe fears are being expressed that the local A. mellifera spp. who have been carted all over the world are becoming extinct in their native home [29,62]. Managed beehives have intermingled with the wild ones to the extent, that the wild ones have succumbed to disease and starvation. ...
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... Bumble bees (Bombus spp.) are declining in both density and richness at the global scale, threatening losses to biodiversity [1] and food security [2,3]. Bumble bee declines have been attributed to an array of stressors, including habitat loss and loss of floral resources [4,5], pesticide use [6][7][8], parasites and pathogens [7,[9][10][11] and climate change [4,12]. ...
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... Honey bees (Apis spp.) are among the most ecologically and economically significant insects on the planet (Hristov et al. 2020; Khalifa et al. 2021; Papa et al. 2022). Renowned for their role in pollination, honey production, and as models for studying social behavior, these eusocial insects are indispensable to agricultural systems and natural ecosystems (Gill 1990; Zayed and Robinson 2012; Hoover and Ovinge 2018). ...
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... Honeybees serve as the primary pollination vector for many crops and wild plant species (Khalifa et al. 2021) and play a crucial role in both long-distance and short-distance transmission. The average distance covered by honeybee flights for nectar collection is approximately 2 km, with a potential range of up to 13.5 km (Zurbuchen et al. 2010;Danner et al. 2016). ...
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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).
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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.
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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.