Overview of Bee Pollination and Its Economic Value for Crop Production

Abstract

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.

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, improving global economic and dietary outcomes. This review highlights the role played by bee pollination, which influences the economy, and enlists the different types of bees and other insects associated with pollination.

Full text

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, *


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 Pascual
Received: 16 April 2021
Accepted: 23 July 2021
Published: 31 July 2021
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2021 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
1Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University,
S-10691 Stockholm, Sweden
2Department 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.)
3Agricultural Research Centre, Department of Bee Research, Plant Protection Research Institute,
Giza 12627, Egypt; aidaabd.elwahed@arc.sci.eg
4Alnahalaljwal Foundation Saudi Arabia, P.O. Box 617, Al Jumum 21926, Makkah, Saudi Arabia;
ahmed@alnahalaljwal.com.sa
5International Center for Chemical and Biological Sciences, H.E.J. Research Institute of Chemistry,
University of Karachi, Karachi 75270, Pakistan; musharraf@iccs.edu
6Department of Pharmacognosy, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia;
malajmii@ksu.edu.sa
7College of Food Science, Fujian Agriculture and Forestry University, Fuzhou 350002, China; zhchao@live.cn
8Department of Plant Protection and Biomolecular Diagnosis, Arid Lands Cultivation Research
Institute (ALCRI), City of Scientific Research and Technological Applications,
New Borg El-Arab City P.O. Box 21934, Egypt; saad.masry@adafsa.gov.ae
9Abu 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,
P.O. Box 591, SE 75124 Uppsala, Sweden
18 International Research Center for Food Nutrition and Safety, Jiangsu University, Zhenjiang 212013, China
*Correspondence: shaden.khalifa.2014@gmail.com (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
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.
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
Insects 2021,12, 688. https://doi.org/10.3390/insects12080688 https://www.mdpi.com/journal/insects

Insects 2021,12, 688 2 of 23
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, improving
global economic and dietary outcomes. This review highlights the role played by bee pollination,
which influences the economy, and enlists the different types of bees and other insects associated
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, incor-
porating both wild and managed bee species in a region could enhance cross-pollination [
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 participate
in global economic food production. Global pollination’s economic value averaged EUR
153 billion, which is worth 9.5% of the world’s agricultural production of human 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 attributable
solely to the accessibility of honey bees [16,17].
The Western honey bee (Apis mellifera L.) is the main species responsible for bee
pollination 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
bumble 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].
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.

Insects 2021,12, 688 3 of 23
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 improves
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 ecosystems,
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 (Glycine
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 ecological
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 pol-
lination 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
subterranean 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 the 36 crops
produced in the state of Pará, 20 (55%) are dependent on animal pollinators, and the overall
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 pol-
lination service value including; cocoa (USD 187.6 million), Acaípalm (USD 635.6 million),
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 estimated 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 billion [36].
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

Insects 2021,12, 688 4 of 23
honey bees, carpenter bees, stingless bees, bumble bees, long-tongued bee, feral bees, social
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
pollination 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 pollinators to
their flowers so that the pollen can adhere to bee-collected pollen grains [
42
]. Researchers
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
quality 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 esculentum
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 affecting the
total yield, which has led to the recommendation that beekeepers place bee colonies 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 p.m.
, and increased the yield above levels seen with insect exclusion, though levels were
below those obtained with open pollination [
12
]. Honey bees and six species of Andrenidae
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-quality
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

Insects 2021,12, 688 5 of 23
by 70%. Pollination by high-quality colonies also increased fruit weight by approximately
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 flowers 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) (Table 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 haemorrhoidalis
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 freshness,
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 maximum
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 estimated USD
18,007 and USD 17,174 hectare, respectively [
60
]. In some cases, wild pollinators 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].
3.3. Stingless Bees
Stingless bees (Apidae: Meliponini) are common floral visitors in tropical and subtrop-
ical 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 development of
pollination solutions that are best suited to the needs of particular crops and habitats [67].
Stingless bees are a large, diverse group of eusocial bees, making them good candidate
pollinators. They vary widely in their body size, being described as small- to medium-sized,
and have vestigial stings [
67
]. Some species tend to be large and smooth, with long hairs

Insects 2021,12, 688 6 of 23
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
mechanical 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 compared 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 seasons.
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
foundation [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), cu-
curbits, and other vegetables and fruits, as observed in the Philippines, Brazil, USA, and
Malaysia [
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
bees [
85
]. The carpenter bee Xylocopa pubescens Spinola is also used to pollinate greenhouse-
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 pollination 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

Insects 2021,12, 688 7 of 23
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 abundance 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 production than
supplementation with honeybees alone.
Brazil [93]
Honey bee (A. mellifera)Increased fruit set by 15%, seed set and content of
fruit sugar, and farmer’s profits by 70%. Argentina [54]
Bumble bees (B. impatiens)
and honey bee (A. mellifera)
The quantity and quality of fruits produced 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
(Citrullus 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%
compared 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 variety by 7%, and
seed mass by 8.4%.
Colombia [55]
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-pollination. 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 (Xylocopa 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
(Xylocopa spp.)
Production costs lowered by 58%.
Average production was 7000 kg/hectare/year. Brazil [101]
Citrus (Citrus sinensis L.) Honey bees (A. mellifera)Lead to heavier fruit with less acid content 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
occurred (more intensive red colour and lower
sugar acid ratios).
Germany [104]
Bees Quantity and quality improved.
Yield increased 20%. Germany [50]
European orchard bee
(Osmia cornuta Latr) Fruit weight was higher than the control treatment. Germany [105]

Insects 2021,12, 688 8 of 23
Table 1. Cont.
Crop (Species) Bee Pollinator Impact on Crop Yield Country Reference
Kiwifruit (Actinidia Deliciosa)
Honey bees (A. mellifera) Increased fruit set and yield. Australia [106]
Bumble bee (Bombus
haemorrhoidalis Smith)
Higher fruit breadth, longer fruits, heavier fruits,
higher healthy fruits, and higher fruit set. India [61]
Pear (Pyrus communis L.) Honey bees (A. mellifera)Fruit size increased by 7% and lead to USD 400 per
hectare net increase in income. USA [46]
Cranberries (Vaccinium
oxycoccos L.) Honey bees (A. mellifera)Production increased from 3.7 million in 1989 to
5.4 million in 1998. USA [45]
Vegetables
Cucumbers
(Cucumis sativus L.)
Honey bees (A. mellifera) 10% increase in production. USA [45]
Stingless bee
(Heterotrigona itama)Lead to larger, heavier, and longer cucumbers. Terengganu [73]
Sweet pepper (Capsicum
annuum L.)
Bumble bee
(Bombus impatiens Cr.)
Increased fruit weight, width, and volume.
Increased seed weight and reduced
harvesting time.
Canada [62]
Bumble bees
(Bombus terrestris L.)
Increased yields, fruit weight, and quality 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
lycopersicum L.)
Bumble bee (Anthophora
urbana Cresson and Bombus
vosnesenskii Radoszkowski)
Lead to higher yield and improved the
quality of fruits. USA [107]
Bees (Exomalopsis analis
Spinola,Centris tarsata Smith,
Bombus morio Swederus,
Eulaema 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 produced. 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 (Helianthus
annuus L.)
Wild bees and honey bees
(A. mellifera)
Interactions between wild and honey bees
increased the efficiency of pollination 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 Darling Downs [110]
Coriander (Coriandrum
sativum Linnaeus.) 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
(Cucurbita maxima L.) Honey bees (A. mellifera)Fruit set, fruit size, weight, and number of seeds
increased linearly with the number of visits. Brazil [112]
Soyabean (Glycine max L.) Honey bees (A. mellifera)Yield increase was associated with an increase 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.
The exclusion of pollinators caused an average
yield gap of 59%.
West Africa [32]

Insects 2021,12, 688 9 of 23
Table 1. Cont.
Crop (Species) Bee Pollinator Impact on Crop Yield Country Reference
C. canephora LApis dorsata F. Bees increased fruit production of coffee by 50%
more than wind. South India [115]
Cowpea
(Vigna unguiculata 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 communis)
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
(Voandzeia subterranean L.)
Feral bees Enhanced yield and improved the quality of crops. Kenya [33]
Coffee (Coffea arabica 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
(Brassica 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 pol-
lination 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].
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, ultravio-
let, 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 ultraviolet
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
functions, 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 usually 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 col-
lection 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].

Insects 2021,12, 688 10 of 23
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
Figure 1. Factors that influence bee visitation.
Finally, the quantity and/or quality of pollen and nectar produced may affect the
visitation 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 guttatus
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 period 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 appealing to honey bees
and bumble bees, while sunflowers and local wildflowers are more appealing 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 pollination,
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

Insects 2021,12, 688 11 of 23
from plant species that have small pores on their anthers [
155
]. During this behavior, 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 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].
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
disorder (CCD) is a phenomenon whereby there are unexplained, rapid losses of adult
working 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
pathogenic effects, causing huge honey bee losses [
168
]. Conroy et al. [
169
] found that
both nutritional 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
pesticides, such as acetamiprid and ergosterol-inhibiting fungicides, threaten pollination
services [
170
]. The residues of pesticides and other synthetic products remain in the nectar
and pollen collected by bees, leading to neurotoxicity, immune deficiency, behavioral
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
]. Spraying
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 effect
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, deltamethrin and
the fungicides thiophanate-methyl and chlorothalonil (synthetic) insecticides on the melon
(Cucumis melo L.) has been investigated. Both insecticides and pesticides 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].

Insects 2021,12, 688 12 of 23
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.
Figure 2. Challenges faced in bee pollination.
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
pollinators 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, causing
pollinator losses [182–184].
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
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
species 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 temperate
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
]. Consequently, according

Insects 2021,12, 688 13 of 23
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
abundance 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 complex
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 butterflies 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].
6.3. Moths vs. Bees
Moths can be categorized as having a crepuscular or nocturnal lifestyle and are recog-
nized as one of the main pollinators of a large variety of plant species in different habitats
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 fre-
quent floral visitors, and there are a number of encounters between plant species and moths.
Moths pollinate approximately 40% of plant species in rural landscape environments, such
as meadows, pastures, old farms, field edges, and roadsides. Consequently, the role of
moths in agricultural environments is often attributed to their pollination of non-crop
plants, which contributes to increasing the biodiversity in agro-ecosystems, offering a
widely appreciated ecological function [
201
,
202
]. Moths may also pollinate 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 recurrent
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 observed visiting

Insects 2021,12, 688 14 of 23
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
nourishment 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
represent 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 Namaqua-
land [
212
,
213
]. Therefore, there is a need for further studies to clarify the ecological role of
beetles 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 noticed
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 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
flowers 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
pollinators 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

Insects 2021,12, 688 15 of 23
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
coffee, cocoa, and rapeseed. Currently, 5–8% of all global crop production would be lost
without 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-diversity
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 environmental balance
but also to maintain food security worldwide. The role played by bees is important 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.
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, Sweden,
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.;
Holland, 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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]

Insects 2021,12, 688 16 of 23
7.
Lobo, J.A.; Quesada, M.; Stoner, K.E. Effects of pollination by bats on the mating system of Ceiba pentandra (Bombacaceae)
populations in two tropical life zones in Costa Rica. Am. J. Bot. 2005,92, 370–376. [CrossRef]
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. [CrossRef]
9. Van der Kooi, C.J.; Ollerton, J. The origins of flowering plants and pollinators. Science (80-.) 2020,368, 1306–1308. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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
pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 2007,274, 303–313. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
19. Rao, S.; Stephen, W.P. Bumble bee pollinators in red clover seed production. Crop Sci. 2009,49, 2207–2214. [CrossRef]
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. [CrossRef]
21.
Greenleaf, S.S.; Kremen, C. Wild bees enhance honey bees’ pollination of hybrid sunflower. Proc. Natl. Acad. Sci. USA
2006
,103,
13890–13895. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
24.
Lautenbach, S.; Seppelt, R.; Liebscher, J.; Dormann, C.F. Spatial and temporal trends of global pollination benefit. PLoS One
2012
,
7, e35954. [CrossRef]
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. [CrossRef]
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. [CrossRef]
27.
Geeraert, L.; Aerts, R.; Berecha, G.; Daba, G.; De Fruyt, N.; D’hollander, J.; Helsen, K.; Stynen, H.; Honnay, O. Effects of landscape
composition on bee communities and coffee pollination in Coffea arabica production forests in southwestern Ethiopia. Agric.
Ecosyst. Environ. 2020,288, 106706–106717. [CrossRef]
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.
[CrossRef]
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. [CrossRef]
30. Losey, J.E.; Vaughan, M. The economic value of ecological services provided by insects. Bioscience 2006,56, 311–323. [CrossRef]
31.
Esquivel, I.L.; Coulson, R.N.; Brewer, M.J. A native bee, melissodes tepaneca (Hymenoptera: Apidae), benefits cotton production.
Insects 2020,11, 487. [CrossRef]
32.
Stein, K.; Coulibaly, D.; Stenchly, K.; Goetze, D.; Porembski, S.; Lindner, A.; Konaté, S.; Linsenmair, E.K. Bee pollination increases
yield quantity and quality of cash crops in Burkina Faso, West Africa. Sci. Rep. 2017,7, 17691–17700. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
34.
Hipólito, J.; Sousa, B.d.S.B.; Borges, R.C.; de Brito, R.M.; 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.
[CrossRef]
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. [CrossRef]

Insects 2021,12, 688 17 of 23
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.
[CrossRef] [PubMed]
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. [CrossRef]
38.
Valido, A.; Rodríguez-Rodríguez, M.C.; Jordano, P. Honeybees disrupt the structure and functionality of plant-pollinator networks.
Sci. Rep. 2019,9, 4711–4721. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
47.
Rajagopal, D.; Eswarappa, G.; Raju, A.J.S. Pollination Potentiality of Honeybees in Increasing Productivity of Guava in Karnataka.
In Changing Trends in Pollen Spore Research; 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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
51.
Abd El-Wahab, T.E.; Ebadah, I.M.A. Impact of honeybee and other insect pollinators on the seed setting and yield production 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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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
marketable crop yield as plant quality in a seed crop. Ecol. Lett. 2018,21, 1704–1713. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]

Insects 2021,12, 688 18 of 23
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. [CrossRef]
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. [CrossRef]
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. 2020,36, 234–244. [CrossRef]
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. [CrossRef]
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. [CrossRef]
71.
Del Sarto, M.C.L.; Peruquetti, R.C.; Campos, L.A.O. Evaluation of the neotropical stingless bee Melipona quadrifasciata (Hy-
menoptera: Apidae) as pollinator of greenhouse tomatoes. J. Econ. Entomol. 2005,98, 260–266. [CrossRef]
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. Neotrop.
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. [CrossRef]
75.
Roselino, A.C.; Santos, S.B.; Hrncir, M.; Bego, L.R. Differences between the quality of strawberries (Fragaria x ananassa) pollinated
by the stingless bees Scaptotrigona aff. depilis and Nannotrigona testaceicornis.Genet. Mol. Res. 2009,8, 539–545. [CrossRef]
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. [CrossRef]
77.
Leys, R.; Cooper, S.J.B.; Schwarz, M.P. Molecular phylogeny of the large carpenter bees, genus Xylocopa (Hymenoptera: Apidae),
based on mitochondrial DNA sequences. Mol. Phylogenet. Evol. 2000,17, 407–418. [CrossRef]
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. [CrossRef] [PubMed]
79. Keasar, T. Large carpenter bees as agricultural pollinators. Psyche A J. Entomol. 2010,2010, 1–7. [CrossRef]
80. Richards, M.H. Built environments influence carpenter bee sociality and vice versa. Insectes Soc. 2020,67, 201–202. [CrossRef]
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.
Barrera, W.B., Jr.; 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. [CrossRef]
84.
Silveira, M.V.; Abot, A.R.; Nascimento, J.N.; Rodrigues, E.T. Is manual pollination of yellow passion fruit completely dispensable?
Sci. Hortic. (Amsterdam) 2012,146, 99–103. [CrossRef]
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. [CrossRef]
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, S.W. Solitary bees. Sci. Am. 1984,250, 120–127. [CrossRef]
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
2006
,313,
351–354. [CrossRef]
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.
[CrossRef]
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.;
Westbury, D.B.; et al.
Apple pollination: Demand depends on variety and supply depends on pollinator identity. PLoS ONE
2016
,
11, e0153889. [CrossRef]
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.

Insects 2021,12, 688 19 of 23
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. [CrossRef]
93.
Viana, B.F.; da Encarnacao Coutinho, J.G.; Garibaldi, L.A.; Braganca Castagnino, G.L.; Gramacho, K.P.; Oliveira Silva, F. Stingless
bees further improve apple pollination and production. J. Pollinat. Ecol. 2014,14, 261–269. [CrossRef]
94.
Mallinger, R.E.; Gratton, C. Species richness of wild bees, but not the use of managed honeybees, increases fruit set of a
pollinator-dependent crop. J. Appl. Ecol. 2015,52, 323–330. [CrossRef]
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. [CrossRef]
96. Walters, S.A. Honey bee pollination requirements for triploid watermelon. HortScience 2005,40, 1268–1270. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef]
99.
Bosch, J.; Osorio-Canadas, S.; Sgolastra, F.; Vicens, N. Use of a managed solitary bee to pollinate almonds: Population sustainability
and increased fruit set. Insects 2021,12, 56. [CrossRef]
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. [CrossRef]
101.
Popak, A.E.; Markwith, S.H.; Strange, J. Economic valuation of bee pollination services for passion fruit (Malpighiales: Passi-
floraceae) cultivation on smallholding Farms in São Paulo, Brazil, using the avoided cost method. J. Econ. Entomol.
2019
,112,
2049–2054. [CrossRef]
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. [CrossRef]
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. [CrossRef]
105.
Herrmann, J.D.; Beye, H.; de la Broise, C.; Hartlep, H.; Diekötter, T. Positive effects of the pollinators Osmia cornuta (Megachilidae)
and Lucilia sericata (Calliphoridae) on strawberry quality. Arthropod. Plant. Interact. 2019,13, 71–77. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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) increases
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
113.
Blettler, D.C.; Fagúndez, G.A.; Caviglia, O.P. Contribution of honeybees to soybean yield. Apidologie
2018
,49, 101–111. [CrossRef]
114.
De Milfont, M.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. [CrossRef]
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. [CrossRef]
116.
Asiwe, J.A.N. Insect mediated outcrossing and geneflow in cowpea (Vigna unguiculata (L.) Walp): Implication for seed production
and provision of containment structures for genetically transformed cowpea. African J. Biotechnol. 2009,8, 226–230. [CrossRef]
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. [CrossRef]
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. [CrossRef]
119.
Stanley, J.; Sah, K.; Subbanna, A.R.N.S. How efficient is the Asian honey bee, Apis cerana in pollinating mustard, Brassica campestris
var. toria? Pollination behavior, pollinator efficiency, pollinator requirements and impact of pollination. J. Apic. Res.
2017
,56,
439–451. [CrossRef]

Insects 2021,12, 688 20 of 23
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. [CrossRef]
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.
[CrossRef]
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. [CrossRef]
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. [CrossRef]
124.
Bloch, D.; Werdenberg, N.; Erhardt, A. Pollination crisis in the butterfly-pollinated wild carnation Dianthus carthusianorum?New
Phytol. 2006,169, 699–706. [CrossRef]
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. [CrossRef]
[PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
135.
Handelman, C.; Kohn, J.R. Hummingbird color preference within a natural hybrid population of Mimulus aurantiacus (Phry-
maceae). Plant Species Biol. 2014,29, 65–72. [CrossRef]
136.
Giurfa, M.; Núñez, J.; Chittka, L.; Menzel, R. Colour preferences of flower-naive honeybees. J. Comp. Physiol. A
1995
,177, 247–259.
[CrossRef]
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. [CrossRef]
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. [CrossRef]
139.
Alcorn, K.; Whitney, H.; Glover, B. Flower movement increases pollinator preference for flowers with better grip. Funct. Ecol.
2012,26, 941–947. [CrossRef]
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. [CrossRef]
141.
Giuliani, C.; Giovanetti, M.; Lupi, D.; Mesiano, M.P.; Barilli, R.; Ascrizzi, R.; Flamini, G.; Fico, G. Tools to tie: Flower characteristics,
voc emission profile, and glandular trichomes of two mexican salvia species to attract bees. Plants 2020,9, 1645. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]

Insects 2021,12, 688 21 of 23
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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, jeb220541. [CrossRef]
153. Pritchard, D.J.; Vallejo-marín, M. Quick guide Buzz pollination ll. Curr. Biol. 2020,30, R858–R860. [CrossRef]
154.
De Luca, P.A.; 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. [CrossRef]
155. Vallejo-Marín, M. Buzz pollination: Studying bee vibrations on flowers. New Phytol. 2019,224, 1068–1074. [CrossRef]
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. [CrossRef]
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. [CrossRef] [PubMed]
158.
Cardinal, S.; Buchmann, S.L.; Russell, A.L. The evolution of floral sonication, a pollen foraging behavior used by bees (Anthophila).
Evolution 2018,72, 590–600. [CrossRef]
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. [CrossRef]
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. [CrossRef]
161.
Dolezal, A.G.; Toth, A.L. Feedbacks between nutrition and disease in honey bee health. Curr. Opin. Insect Sci.
2018
,26, 114–119.
[CrossRef] [PubMed]
162. Huang, Z.Y.; Giray, T. Factors affecting pollinators and pollination. Psyche 2012,2012. [CrossRef]
163.
Christopher Brown, J.; Albrecht, C. The effect of tropical deforestation on stingless bees of the genus Melipona (Insecta:
Hymenoptera: Apidae: Meliponini) in central Rondonia, Brazil. J. Biogeogr. 2001,28, 623–634. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
[PubMed]
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.
[CrossRef]
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.
[CrossRef] [PubMed]
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. [CrossRef] [PubMed]
172.
Arce, A.N.; Ramos Rodrigues, A.; Yu, J.; Colgan, T.J.; Wurm, Y.; Gill, R.J. Foraging bumblebees acquire a preference for
neonicotinoid-treated food with prolonged exposure. Proceedings. Biol. Sci. 2018,285, 8–11. [CrossRef] [PubMed]
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, 12459. [CrossRef]
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
Netherlands, 2018; Volume 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. [CrossRef]
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. [CrossRef]

Insects 2021,12, 688 22 of 23
177.
Vanegas, M. The silent beehive: How the decline of honey bee populations shifted the environmental protection agency’s pesticide
policy towards pollinators. Ecol. Law Q. 2017,44, 311–342.
178.
Rortais, A.; Arnold, G.; Dorne, J.L.; More, S.J.; Sperandio, G.; Streissl, F.; Szentes, C.; Verdonck, F. Risk assessment of pesticides
and other stressors in bees: Principles, data gaps and perspectives from the European Food Safety Authority. Sci. Total Environ.
2017,587–588, 524–537. [CrossRef]
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.
[CrossRef]
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. [CrossRef]
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
,194, 333–344.
[CrossRef]
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. [CrossRef]
183.
Dalsgaard, B. Land-use and climate impacts on plant-pollinator interactions and pollination services. Diversity
2020
,12, 168.
[CrossRef]
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. [CrossRef]
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, 341. [CrossRef]
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. [CrossRef]
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. [CrossRef]
188. Jauker, F.; Wolters, V. Hover flies are efficient pollinators of oilseed rape. Oecologia 2008,156, 819–823. [CrossRef]
189.
Howlett, B.G.; Gee, M. The potential management of the drone fly (Eristalis tenax) as a crop pollinator in New Zealand. N. Z.
Plant Prot. 2019,72, 221–230. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
194.
Santos, R.d.S.; Milfont, M.d.O.; Silva, M.M.; Carneiro, L.T.; Castro, C.C. Butterflies provide pollination services to macadamia in
northeastern Brazil. Sci. Hortic. 2020,259, 108818–108825. [CrossRef]
195.
Martins, D.J. Butterfly pollination of the dryland wildflower gloriosa minor. J. East African Nat. Hist.
2014
,103, 25–30. [CrossRef]
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. [CrossRef]
197.
Pinto, C.E.; Oliveira, R.; Schlindwein, C. Do consecutive flower visits within a crown diminish fruit set in mass-flowering
Hancornia speciosa (Apocynaceae)? Plant Biol. 2008,10, 408–412. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
202.
Power, A.G. Ecosystem services and agriculture: Tradeoffs and synergies. Philos. Trans. R. Soc. B Biol. Sci.
2010
,365, 2959–2971.
[CrossRef]
203.
Alarcón, R.; Davidowitz, G.; Bronstein, J.L. Nectar usage in a southern Arizona hawkmoth community. Ecol. Entomol.
2008
,33,
503–509. [CrossRef]

Insects 2021,12, 688 23 of 23
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. [CrossRef]
205. Sime, K.R.; Baldwin, I.T. Predominantly self-fertilizing native tobacco. BMC Ecol. 2003,3, 6–14. [CrossRef]
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. [CrossRef]
207.
Bernhardt, P. Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. Pl Syst. Evol.
2000
,222, 293–320.
[CrossRef]
208.
Dieringer, G.; Cabrera, R.L.; Lara, M.; Loya, L.; Reyes, P.; Journal, I. Beetle pollination and floral thermogenicity in Magnolia
tamaulipana (Magnoliaceae). Int. J. Plant Sci. 1999,160, 64–71. [CrossRef]
209.
Mayer, C.; Soka, G.; Picker, M. The importance of monkey beetle (Scarabaeidae: Hopliini) pollination for Aizoaceae and Asteraceae
in grazed and ungrazed areas at Paulshoek, Succulent Karoo, South Africa. J. Insect Conserv. 2006,10, 323–333. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef]
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.
[CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
216. Ananthakrishnan, T.N. Thrips and pollination biology. Curr. Sci. 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. [CrossRef]
218.
Resende, J.J.; de M. Santos, G.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. [CrossRef]
220. Schremmer, F. Wespen und Hornissen; Ziemsen: Wittenberg Lutherstadt, Germany, 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. [CrossRef] [PubMed]
222.
Jakubska-Busse, A.; Przado, 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. [CrossRef]