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The Journal of Horticultural Science and Biotechnology
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Tomato (Solanum lycopersicum) pollinators and
their effect on fruit set and quality
Hermann Cyr Toni , Bruno Agossou Djossa , Mathieu Anatole Tele Ayenan &
Oscar Teka
To cite this article: Hermann Cyr Toni , Bruno Agossou Djossa , Mathieu Anatole Tele
Ayenan & Oscar Teka (2020): Tomato (Solanum�lycopersicum) pollinators and their effect
on fruit set and quality, The Journal of Horticultural Science and Biotechnology, DOI:
10.1080/14620316.2020.1773937
To link to this article: https://doi.org/10.1080/14620316.2020.1773937
Published online: 07 Jul 2020.
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REVIEW
Tomato (Solanum lycopersicum) pollinators and their eect on fruit set and
quality
Hermann Cyr Toni
a
, Bruno Agossou Djossa
a,b
, Mathieu Anatole Tele Ayenan
c
and Oscar Teka
a
a
Laboratoire d’Ecologie Appliquée, Faculté des Sciences Agronomiques, Université d’Abomey-Calavi, Bénin;
b
Laboratoire de Foresterie et
de Conservation des Bioressources (LaFCBio), Ecole de Foresterie Tropicale, Université Nationale d’Agriculture, Benin;
c
College of Basic and
Applied Sciences, West Africa Centre for Crop Improvement, University of Ghana, Accra, Ghana
ABSTRACT
Tomato owers are self-fertile, but require pollinators’ intervention to increase fruit setting. In
this review paper, we present and discuss the current state of knowledge on tomato pollina-
tors. Information on tomato pollinators was extracted from 49 scientic publications, 6 doctoral
thesis documents, 4 books, 3 technical sheets, a compilation of conference abstracts and 3
internet publications. We identied from the various publications 77 insects that pollinate
tomato owers. These pollinators were all Hymenoptera and belong to the families, Apidae
(61%), Halictidae (35%), Megachilidae (1%), Colletidae (1%), and Andrenidae (2%). Bombus bees
were the most represented genus with 16 identied species. These pollinators contribute to
the improvement of the fruit set percentage and fruit characteristics. Worldwide, colonies of
bumblebees, Bombus terrestris, Bombus impatiens, Bombus occidentalis, Bombus ignitus and
Bombus lucorum as well as honeybee, Apis mellifera are managed for tomato pollination.
However, the exploitation of managed pollinators is poorly developed in Africa. Similarly,
very little research has been conducted on tomato pollinators in Africa and Europe. Further
investigations are needed, especially in Africa, to identify insects that are eective in tomato
pollination, and to develop management strategies for their ecient exploitation in tomato
production.
ARTICLE HISTORY
Accepted 18 May 2020
KEYWORDS
Pollination; tomato; quality;
ecosystem service
Introduction
Tomato (Solanum lycopersicum L.) is an annual plant
belonging to the family Solanaceae. This crop originated
in Andes regions of South America, extending from
central Ecuador, across Peru to northern Chile (van
Dam et al., 2005; Denham, 2014), from where it has
been introduced in other regions of the world.
Nowadays, several varieties of tomatoes of various shapes
and colours are cultivated worldwide (Denham, 2014).
Tomato is used in many dishes and is one of the main
vegetables consumed in the world. Tomato fruits play an
important nutritional role since they contain many
nutrients such as essential amino acids, vitamin C, vita-
min A, lycopene and β-carotene (USDA, 2019). Its pro-
duction is also an important source of income for
farmers (Ogunniyi & Oladejo, 2011). World tomato
production amounted to 182,256,458 tons in 2018
(FAOSTAT, 2020). During the last 10 years, the largest
tomato-producing countries were China, India and the
United States of America (FAOSTAT, 2020).
Cultivated tomato is self-pollinated. However, the
pollination process is improved by wind and insects
(Free, 1993; Hanna, 1999). The importance of pollination
in tomato production has been long recognised. Earlier
research on tomato pollination dates back to the 1890s
(Bailey, 1891). In order to improve fruit yields, several
studies have been conducted on tomato pollination dur-
ing the last two decades. These included the inventory of
natural pollinators (Teppner, 2005; Deprá et al., 2014;
Silva-Neto et al., 2017), the use of managed pollinators
for pollination under greenhouse (Hikawa & Miyanaga,
2009; Morandin et al., 2001a, 2001b) and pollinators’
efficiency (Morandin et al., 2001a; Del Sarto et al., 2005;
Bispo Dos Santos et al., 2009). Information published in
various documents is synthesised in this article in order
to provide the state of knowledge on the diversity of
tomato pollinators and their contribution to the
improvement of tomato yield and fruit characteristics.
We also identified research avenues to gain a better
understanding of the interactions of tomato-pollinators
for efficient exploitation of pollinators.
Methodology
This review article is a synthesis of information avail-
able on pollination of cultivated tomato (Solanum lyco-
persicum L.). Information was collected from different
sources including 49 scientific articles, 6 doctoral thesis
documents, 4 books, 3 technical files and a compilation
of conference abstracts. Three internet publications
CONTACT Hermann Cyr Toni tonihermann9@gmail.com Laboratoire d’Ecologie Appliquée, Faculté des Sciences Agronomiques, Université
d’Abomey-Calavi, Bénin
THE JOURNAL OF HORTICULTURAL SCIENCE AND BIOTECHNOLOGY
https://doi.org/10.1080/14620316.2020.1773937
© 2020 The Journal of Horticultural Science & Biotechnology Trust
were also consulted. Keywords used for the research
were tomato, Lycopersicon esculentum, Solanum lyco-
persicum, pollination, pollinators, fruit characteristics,
managed pollinators, fruit set and yield. The publica-
tions were retrieved from various search engines
including Google, Google Scholar, ResearchGate,
Bioline International, Scopus, and Web of Science.
After a screening of titles and abstracts of the publica-
tions, only those that explicitly addressed pollinators’
effects on tomatoes or diversity of pollinators in tomato
farms were kept for further data extraction and analysis.
Information on insects that pollinate tomato flowers,
their families and order were extracted from each pub-
lication. Countries and continents where studies were
conducted, the effects of pollinators on the different
characteristics of tomato fruits as well as the fruiting
rate were also extracted from the papers. From papers
that address the effects of pollinators on fruit character-
istics, an estimation of the increase of the improved
variables (weight, diameter, fruits set, height, etc.) was
calculated as follows (Tchuenguem et al., 2014):
Frx¼ ½ðFrZFrYÞ=FrZ 100
where Fr
Z
and Fr
Y
are the mean value of variables of
flowers subjected to treatment Z (pollinated flowers)
and treatment Y (protected flowers). Percentages
obtained were rounded to the nearest whole number.
Values of some variables were estimated from figures
in some papers. These cases were marked by the sym-
bol ‘≈’.
Results and discussion
Tomato owers and pollination
Tomato flowers are 1.5 to 2 cm in diameter and
actinomorphic (van Dam et al., 2005). Flowers arise
terminally, opposite to leaves or between the leaves.
Tomato flowers are composed of organs organised in
whorls. The first whorl corresponds to the calyx,
which is generally composed of five to six sepals of
green colour. The second whorl, the corolla consists of
bright yellow petals welded at the base. The corolla has
the same number of petals as the sepals. Androecea
constitute the third whorl and has five or six stamens,
with lateral dehiscence. Stamens are fused together to
form the staminal cone which bears the anthers of
bright yellow colour. The pistil is composed of 2 to 9
fused carpels enclosing the ovary. Depending on the
cultivar, the style may be inside the stamen cone
(brevistyle flower), at the same level with the stamen
or slightly above the stamen cone (longistyle flower)
(Petit, 2003; Ranc, 2010). Environmental conditions
such as sunlight, high temperature, and the low car-
bohydrate content associated with the high nitrogen
content in plant cells could promote the formation of
a long style (Ranc, 2010; Karlsson, 2017). Tomato
flowers are nectarless and the presence of other plant
species which produce nectar in the vicinity of tomato
becomes an additional attraction to pollinators
(Gaglianone et al., 2015).
Cultivated tomato flowers are hermaphrodite and
self-compatible (Cauich et al., 2004). They self-
pollinate and flowers set fruits without pollen vectors
(Deprá et al., 2014). This is due to the release of some
pollen grains at anther dehiscence and flower shaking
by wind (Picken, 1984). However, the quantity of
pollen grains released by flowers without the aid of
pollinators may not be enough to ensure a good polli-
nation of the species (Hanna, 1999; Macias-
Macias et al., 2009). They then require the interven-
tion of pollinators for better production, especially
when tomatoes are grown in greenhouses (Free,
1993; Deprá et al., 2014). The pollination of the tomato
flowers is mainly ensured by vibration (buzz pollina-
tion) which favours the release of the pollen
(Buchmann, 1983). Morandin et al. (2001b) showed
that higher bruising level of tomato flowers by bum-
blebee B. impatiens) increases the number of pollen
grains on the stigma which resulted in better fruit set.
Tomato flowers have a moderate dependence (10% to
40%) on pollinators (Klein et al., 2007). In fact, the
lack of pollinators could lead to reduction of tomato
yield from 10% to 40%. Since tomato requires flower
shaking for a good pollination, it has probably devel-
oped strategies to attract insects providing this service
because several main pollinators of tomato vibrate
during flower visits (sonicating bees). Pollination of
tomato flowers occurs mainly between 10 am and 4
pm, a period during which the stigma is very receptive
(Levy et al., 1978; Del Sarto et al., (2005). Tomatoes
grown in open fields are naturally pollinated by polli-
nators and wind. However, for tomatoes produced in
greenhouses, tunnels, and other protected environ-
ments, or in case of pollination deficit, pollination is
performed by managed insects, by using vibrators or
hormones (Al-
Attal et al., 2003; Velthuis & Van Doorn, 2006;
Vergara & Fonseca-Buendía, 2012).
Insect pollinators of tomato
Several insects forage on tomato flowers. Two main
factors are generally taken into account in the classifi-
cation of insects as pollinators of tomato (Deprá et al.,
2014). The first is the harvest of pollen grains by
insects during flower visits. Insects collect pollen
grains with hind legs, mandibles, or the both in some
cases (Teppner, 2005). The second factor is the vibra-
tion of flowers by insects that promote the release of
pollen grains. This last criterium is not consistent. In
fact, some insects lacking the ability to vibrate tomato
flowers are classified as tomato pollinators (Santos et
2H. C. TONI ET AL.
al., 2014; Vinícius-
Silva et al., 2017). The synthesis of documents allowed
us to identify 77 pollinators of tomato (Table 1). They
are all insects. Nevertheless, this number could be
revised upwards or downwards because of certain
genera for which the species has not been identified
(eg. Pseudaugochlora spp., Dialictus spp.,
Augochloropsis spp.), especially when they were
reported in several studies.
All reported pollinators belong to the Hymenoptera
order and to five families, Apidae, Halictidae,
Megachilidae, Colletidae and Andrenidae (Figure 1).
The Apidae family is the most represented with 47
species, followed by Halictidae with 27 species. The
families, Megachilidae, Colletidae, and Andrenidae,
are each represented by one species. The genus
Bombus was the most represented genus of all polli-
nating insects with 16 well-identified species. The pre-
sence of natural habitats and the availability of floral
resources are important determinants of pollinator
diversity and abundance in tomato fields (Westphal
et al., 2003; Greenleaf & Kremen, 2006).
The majority of insects were considered tomato
pollinators because they vibrate their flight muscles
during flower visits. However, some insects including
Apis mellifera, Trigona spinipes and Paratrigona line-
ata were considered pollinators because of their fora-
ging behaviour, which could favour cross-pollination
(Santos et al., 2014; Vinícius-Silva et al., 2017). Indeed,
they dip their head in the anther cone to collect the
pollen which sticks to their head. These pollen grains
could be deposited on the stigma of other flowers since
these bees come into contact with the stigma during
pollen collection.
Most of the previous research about tomato polli-
nators were focused on inventory of pollinators
(Teppner, 2005; Deprá et al., 2014; Vinícius-Silva
et al., 2017) and the comparison of the efficiency of
native pollinators and exotic managed pollinators such
as A. mellifera, B. impatiens, and B. occidentalis (Palma
et al., 2008; Bispo Dos Santos et al., 2009; Torres-Ruiz
& Jones, 2012). The majority of these studies were
conducted in Americas (Brazil, Chile, Mexico,
United States of America, Canada, etc.) and Oceania,
particularly in Australia (Figure 2). This could be
explained by intensive research to improve the pro-
ductivity of tomato in these countries by exploiting the
potential of pollinators.
Plus, the identification of indigenous pollinators of
tomato in each region could enable the development
of breeding strategies to improve their pollinating
abilities and efficiency. Doing so, some countries
could limit the importation of exotic pollinators that
may have adverse effects on local biodiversity
(Goulson, 2003). On the other hand, there is little
work and data available on tomato pollination, espe-
cially on plant–pollinator relationships in Africa
(Rodger et al., 2004). In Algeria, no pollinating bee
was found during observations of tomato flowers on
two sites surrounded by natural habitats inhabiting
melliferous plants (Benachour, 2008). In Benin,
Xylocopa sp. and A. mellifera, considered as pollinators
of tomato in other countries, were identified during an
inventory of tomato field entomofauna (Chougourou
et al., 2012; Santos et al., 2014). Kasina (2007) identi-
fied Xylocopa calens and Halictus spp. as pollinators of
tomato in Kenya. The bumblebee Bombus terrestris,
whose natural range covers North Africa, is also used
to pollinate tomatoes in this part of the continent
(Velthuis & Van Doorn, 2006). The little knowledge
of pollinators in Africa may be somewhat due to the
low availability of insect systematists on the continent
(Gemmill et al., 2019) and tomato production system,
which is predominantly in open fields.
Eect of pollinators on the fruit set percentage
and fruit characteristics
Pollinators improve several fruit characteristics and
consequently fruit quality. Several studies have
assessed the effect of pollinators on tomato fruit char-
acteristics and fruit set percentage (Table 2).
Seventy-five percent (12 out of 16) of the studies
addressing the effect of pollinators on fruit setting
reported that pollinators improved tomato fruit set
percentage (Macias-Macias et al., 2009; Silva-Neto
et al., 2013; Deprá et al., 2014). Improvements of 7%
to 70% were reported. However, Estay et al. (2001) and
Nunes-Silva et al. (2013) reported no effect of pollina-
tors on tomato fruit quality and fruit setting. These
findings suggest that the effect of pollinators on fruit
setting is context-dependent. For instance, in an envir-
onment where the wind is strong enough to promote
pollination, the effects of pollinators on fruit setting
may be less perceptible.
Pollinators also positively affect the following fruit
characteristics: fruit weight, number of seeds per fruit,
diameter or transversal circumference, vertical height,
sugar content, and roundness. The number of seeds
seems to be more sensitive to pollinator visits because
it had been increased in all studied cases (20) followed
by fruit height or vertical circumferences (3 out of 3
studied cases). These parameters were improved by 9%
to 70% for the seed number and 3% to 15% for the fruit
height or vertical circumference. An interesting
improvement rate due to pollinator visits was also
reported for tomato weight (16 out of 20 studied
cases, i.e. 80%) (e.g.: Morandin et al., 2001b; Amala &
Shivalingaswamy, 2017). However, Deprá et al. (2014)
and Santos et al. (2014) found no effect of pollinator on
tomato fruit weight. Pollinators contribute to pollen
grains transfer to stigma (Dogterom et al., 1998). As
a result, pollinators have been consistently reported to
improve the number of seeds per fruit, which may be
THE JOURNAL OF HORTICULTURAL SCIENCE AND BIOTECHNOLOGY 3
Table 1. Insect pollinators of tomato.
Family Species References
Apidae Amegilla holmesi Bell et al. (2006)
Amegilla zonata Amala & Shivalingaswamy (2017)
Amegilla chlorocyanea Hogendoorn et al., (2006), Hogendoorn et al., (2007)
Anthophora urbana Greenleaf & Kremen (2006), Garibaldi et al. (2013)
Apis mellifera Higo et al. (2004), Bispo Dos Santos et al. (2009), Macias-Macias et al. (2009), Santos et al. (2014)
Bombus pauloensis Vinícius-Silva et al. (2017)
Bombus atratus Aldana et al. (2007)
Bombus bimaculatus Kevan et al. (1991)
Bombus californicus Xerces Society for Invertebrate Conservation (2019)
Bombus dahlbomii Ruz (2005), Estay et al. (2001)
Bombus ephippiatus Vergara & Fonseca-Buendía (2012), Torres-Ruiz and Jones (2012)
Bombus impatiens Morandin et al. (2001b, 2011a), Higo et al. (2004), Palma et al. (2008), Torres-Ruiz & Jones (2012), Nunes-Silva et al. (2013)
Bombus lapidarius Teppner (2005)
Bombus lucorum Velthuis & Van Doorn (2006), Wu et al. (2008)
Bombus morio Silva-Neto et al. (2013, 2017), Deprá et al. (2014), Santos et al. (2014), Vinícius-Silva et al. (2017)
Bombus occidentalis Whittington & Winston (2004); Velthuis & Van Doorn (2006)
Bombus pascuorum Teppner (2005)
Bombus ruderatus Velthuis & Van Doorn (2006)
Bombus spp. Chougourou et al. (2012), Garibaldi et al. (2013)
Bombus sylvarum Teppner (2005)
Bombus terrestris Pressman et al. (1999), Dasgan & Ozdogan (2004), Teppner (2005), Velthuis & Van Doorn (2006), Hikawa & Miyanaga (2009)
Bombus vosnesenskii Dogterom et al. (1998), Greenleaf & Kremen (2006)
Centris aenea Santos et al. (2014), Silva-Neto et al. (2017)
Centris fuscata Silva-Neto et al. (2017)
Centris spp. Deprá et al. (2014), Silva-Neto et al. (2017)
Centris tarsata Silva-Neto et al. (2013, 2017)
Centris varia Silva-Neto et al. (2017)
Epicharis flava Silva-Neto et al. (2017)
Epicharis sp. Silva-Neto et al. (2013, 2017)
Euglossa spp. Deprá et al. (2014)
Eulaema nigrita Silva-Neto et al. (2013, 2017), Deprá et al. (2014), Santos et al. (2014)
Exomalopsis analis Silva-Neto et al. (2013, 2017), Santos et al. (2014), Vinícius-Silva et al. (2017)
Exomalopsis fulvofasciata Vinícius-Silva et al. (2017), Silva-Neto et al. (2017)
Exomalopsis minor Silva-Neto et al. (2017)
Exomalopsis spp. Macias-Macias et al. (2009), Deprá et al. (2014)
Exomalopsis sp1. Silva-Neto et al. (2017)
Exomalopsis sp2. Silva-Neto et al. (2017)
Melipona quadrifasciata Del Sarto et al. (2005), Bispo Dos Santos et al. (2009), Hikawa & Miyanaga (2009), Deprá et al. (2014)
Melipona quinquefasciata Santos et al. (2014), Silva-Neto et al. (2017)
Nannotrigona perilampoides Cauich et al. (2004), Palma et al. (2008)
Paratrigona lineata Santos et al. (2014)
Thygater (Thygater) analis Vinícius-Silva et al. (2017)
Trigona spinipes Vinícius-Silva et al. (2017)
Xylocopa calens Kasina (2007)
Xylocopa frontalis Silva-Neto et al. (2017)
Xylocopa lestis Hogendoorn et al. (2000)
Xylocopa spp. Chougourou et al. (2012), Deprá et al. (2014)
(Continued)
4H. C. TONI ET AL.
Table 1. (Continued).
Family Species References
Halictidae Augochlora pura Garibaldi et al. (2013)
Augochlora spp. Silva-Neto et al. (2017)
Augochlorella aurata Garibaldi et al. (2013)
Augochloropsis callichroa Vinícius-Silva et al. (2017), Silva-Neto et al. (2017)
Augochloropsis cupreola Santos et al. (2014)
Augochloropsis electra Vinícius-Silva et al. (2017)
Augochloropsis smithiana Vinícius-Silva et al. (2017), Silva-Neto et al. (2017)
Augochloropsis sp2. Silva-Neto et al. (2017)
Augochloropsis sp3. Silva-Neto et al. (2017)
Augochloropsis sp4. Silva-Neto et al. (2017)
Augochloropsis sp5. Silva-Neto et al. (2017)
Augochloropsis sp6.Silva-Neto et al. (2017)
Augochloropsis spp. Macias-Macias et al. (2009), Deprá et al. (2014), Vinícius-Silva et al. (2017)
Dialictus sp1. Silva-Neto et al. (2017)
Dialictus spp. Garibaldi et al. (2013)
Halictus spp. Kasina (2007)
Hoplonomia westwoodi Amala & Shivalingaswamy (2017)
Lasioglossum morio Teppner (2005)
Lasioglossum politum Teppner (2005)
Lasioglossum spp. Garibaldi et al. (2013)
Lasioglossum zonulum Teppner (2005)
Pseudaugochlora erythrogaster Vinícius-Silva et al. (2017)
Pseudaugochlora graminea Santos et al. (2014), Vinícius-Silva et al. (2017), Silva-Neto et al. (2017)
Pseudaugochlora indistincta Silva-Neto et al. (2017)
Pseudaugochlora sp1. Silva-Neto et al. (2017)
Pseudaugochlora sp2. Silva-Neto et al. (2017)
Pseudaugochlora spp. Deprá et al. (2014)
Megachilidae Megachile willughbiella Teppner (2005)
Colletidae Hylaeus gibbus Teppner (2005)
Andrenidae Oxaea flavescens Deprá et al. (2014), Santos et al. (2014), Silva-Neto et al. (2017), Vinícius-Silva et al. (2017)
THE JOURNAL OF HORTICULTURAL SCIENCE AND BIOTECHNOLOGY 5
important for seed multiplication in the seed industry.
The improvement of the fruit characteristics by polli-
nators should increase the commercial value of tomato
fruits (Klatt et al., 2014). Moreover, the combined posi-
tive effect of pollinators on fruit characteristics and fruit
set percentage increased tomato yield (Cauich et al.,
2004; Amala & Shivalingaswamy, 2017). As a result,
pollinators contribute to improve incomes of tomato
growers. Concerning the maturing time, no significant
difference was observed between the pollinated and
protected fruits (Morandin et al., 2001b) while
Vergara & Fonseca-Buendía (2012) reported a longer
maturing time for pollinated fruits (delay of about
9 days).
Pollinators’ effects on tomato fruit set percentage
and fruit characteristics vary among varieties. When
considering the same pollinator B. impatiens), it
improved the fruiting rate of the Tricia variety
(Torres-Ruiz & Jones, 2012) while it had no effect on
the variety Clarance (Nunes-Silva et al., 2013). These
differences may be due to differences in several factors
such as experimental designs, tomato varieties (flower
morphology and especially the position of the stigma)
used for experiments, the landscape around experi-
mental sites and therefore the composition of pollina-
tor community. For example, studies in which
pollinating bees were kept in a greenhouse may result
in best pollination success than studies conducted
open field, because pollinators could visit more attrac-
tive plants (Whittington et al., 2004). The environ-
mental conditions during the experiments may also
influence the visitation and foraging behaviour of the
pollinators (Tuell & Isaacs, 2010). Besides, tomato
varieties differed in the quantity of volatiles produced
and then have different attractiveness to pollinators
(Morse, 2009) as clearly demonstrated for strawberry
varieties (Klatt et al., 2013). Differences may also occur
in tomato flower morphology (brevistyle or longistyle
flowers) depending on the variety/cultivar, which
could affect the pollination success of this crop
(Ranc, 2010). Pollinators are likely to have a positive
effect on varieties with longistyle flowers which are
more prone to outcrossing because their pollen grains
cannot easily land on the stigma without assistance.
Taken together, these findings suggest that the effects
of pollinators on tomato fruit attributes are context-
dependent, and results from an experiment or
a geographic area can barely be extrapolated. Thus, it
becomes critical to assess the effect of native pollinator
communities on the agronomic performance and quality
attributes of tomato in Africa, where a huge information
gap still exists. Gaining such knowledge will provide a key
basis for better managing tomato growing environments
to increase the exploitation of pollinators’ potential to
improve tomato productivity and quality.
Figure 1. Tomato pollinator families.
Figure 2. Continents in which tomato pollinators have been inventoried.
6H. C. TONI ET AL.
Table 2. Effect of pollinators on tomato fruit characteristics and fruit set.
Pollinators Fruit set Weight
Seed
numb. Vol.
Diam/
Tr.Cir. Roud.
Height/
Ve.Cir. Sugar
Mat
Dur. Methodology and studied varieties
Studied area and
country References
Amegilla zonata ≈60% 61% 68% 55% No Cloth protected flowers vs. insect pollinated flowers.
Variety: Abhinav
Open field
(India)
Amala &
Shivalingaswamy
(2017)
Hoplonomia westwoodi ≈43% 47% 60% 41% No
Amegilla holmesi No 11% 39% 6% 25% Bag protected flowers vs. A. holmesi pollinated flowers.
Variety: Label
Glasshouse
(Australia)
Bell et al. (2006)
Melipona quadrifasciata 14–16% ≈32–50%
≈
60–70% ≈21–37% ≈10–15% Greenhouse without pollinators vs. greenhouse with colonies of
M. quadrifasciata and A. mellifera. Variety: NA
Greenhouse
(Brazil)
Bispo Dos Santos et al.
(2009)
Apis mellifera No ≈31% ≈38–54% ≈12% ≈6%
Bombus impatiens 63–70% 36–40% 48–68% 15% No No No Flowers with no bruising vs. flowers submitted to 4 degrees of bruising.
Variety: Trust
Greenhouse
(Canada)
Morandin et al. (2001b)
Nannotrigona perilampoides 37% No 40% Greenhouse without pollinators vs. greenhouse with colonies of N.
perilampoides. Variety: Maya
Greenhouse
(Mexico)
Cauich et al. (2004)
Augochloropsis spp.
Bombus morio
Centris spp.
Euglossa spp.
Eulaema nigrita
Exomalopsis spp.
Melipona quadrifasciata
Oxaea flavescens
Pseudaugochlora spp.
Xylocopa spp.
7–8% No 15% No No Bag protected flowers vs. insect pollinated flowers.
Varieties: Ivanhoé Agrocinco and Dominador Agristar
Open field
(Brazil)
Deprá et al. (2014)
Exomalopsis sp. ≈31% 32% 60% Bag protected flowers vs. insect pollinated flowers
Variety: Saladette
Open field
(Mexico)
Macias-Macias et al.
(2009)
Augochloropsis sp. ≈33% 35% 61%
Apis mellifera ≈20% 18% 42%
Bombus morio
Centris tarsata
Epicharis sp.
Eulaema nigrita
Exomalopsis analis
39% 33% 68% 9% Bag protected flowers vs. insect pollinated flowers.
Variety: Italian
Open field
(Brazil)
Silva-Neto et al. (2013)
Bombus impatiens No ≈32–46% ≈45–61% Bag protected flowers vs. flowers pollinated by B. impatiens.
Variety: Clarance
Greenhouse Nunes-Silva et al. (2013)
(Continued)
THE JOURNAL OF HORTICULTURAL SCIENCE AND BIOTECHNOLOGY 7
Table 2. (Continued).
Pollinators Fruit set Weight
Seed
numb. Vol.
Diam/
Tr.Cir. Roud.
Height/
Ve.Cir. Sugar
Mat
Dur. Methodology and studied varieties
Studied area and
country References
Apis mellifera
Augochloropsis callichroa
Augochloropsis electra
Augochloropsis smithiana
Augochloropsis sp.
Bombus morio
Bombus pauloensis
Exomalopsis analis
Exomalopsis fulvofasciata
Pseudaugochlora
erythrogaster
Pseudaugochlora
graminea
Thygater analis
Trigona spinipes
Oxaea flavescens
40% 73% 62% Bag protected flowers vs. insect pollinated flowers.
Variety: Salad type
Open field
(Brazil)
Vinícius-Silva et al.
(2017)
Exomalopsis analis ≈47% No 29% No No Bag protected flowers vs. flowers pollinated by E. analis.
Variety: Forty
Open field
(Brazil)
Santos et al. (2014)
Bombus ephippiatus 8% 31% No 5% 16% Bag protected flowers vs. flowers pollinated by B. ephippiatus.
Variety: Mallory
Greenhouse
(Mexico)
Vergara & Fonseca-
Buendía (2012)
Bombus impatiens 52% 60% 26% Bag protected flowers vs. flowers pollinated by B. impatiens and
B. ephippiatus. Variety: Tricia
Greenhouse
(Mexico)
Torres-Ruiz & Jones
(2012)
Bombus ephippiatus 49% 62% 25%
Bombus dahlbomii No No 9% No Greenhouse without pollinators vs. greenhouse with colonies of
B. dahlbomii. Variety: FA 144
Greenhouse
(Chile)
Estay et al. (2001)
Xylocopa calens
Halictus spp.
15% 42% 7% 3% Bag protected flowers vs. insect pollinated flowers.
Variety:NA
Open field
(Kenya)
Kasina (2007)
Legend: Seed numb.: seed number; Vol.: volume; Diam.: diameter; Tr.Cir.: Transversal circumference; Ve.Cir.: Vertical circumference; Round.: Roundness; Mat Dur.: Maturity Duration, vs.: versus; ≈ is used to show value estimated on the basis
of figures.
8H. C. TONI ET AL.
In addition, assessing the effects of pollinators on
crop production in general and tomato performance
and quality, in particular, would provide evidences for
raising awareness on the importance of pollinators
and the needs to adopt practices that preserve them
in the ecosystem. In some regions of the world, espe-
cially in Europe and United States of America,
a decline in domestic pollinators population along
with the potential reduction in their eco-systemic ser-
vice have been reported (Potts et al., 2010) while the
dynamic in pollinator populations is still poorly docu-
mented in Africa.
Ecacy, eectiveness and eciency of tomato
pollinators
Pollination efficacy expresses the ‘contribution of each
pollinator to the plant reproductive success after
a pollination event’ while pollination effectiveness is
the ‘total contribution by a certain pollinator to male
and female components of reproductive success’
(Freitas, 2013). The same author defined pollinator
efficiency as ‘the pollinator efficacy in relation to floral
resource consumption and pollen wastage’. It is
assessed using the Spear’s pollination efficiency index
(Macias-Macias et al., 2009). Several studies investi-
gated the efficacy, effectiveness, and efficiency of pol-
linators that are adapted to local ecological conditions.
These studies generally compared the efficiency, effec-
tiveness and efficacy of native with exotic pollinators.
The comparative study of the efficiency of two native
bees from Mexico (Exomalopsis sp. and Augochloropsis
sp.) and the honey bee, A. mellifera, showed that native
bees were more efficient with a better fruit set percen-
tage, heavier fruits and a larger number of seeds per
fruit (Macias-Macias et al., 2009). Higo et al., (2004)
also came to a similar conclusion by assessing the
additional effect of the honey bee in the pollination
of tomatoes compared to B. impatiens. Bispo Dos
Santos et al. (2009) demonstrated that the native
honey bee Melipona quadrifasciata was more effective
than A. mellifera in Brazil. Even though
M. quadrifasciata was more efficient than the honey
bee, Del Sarto et al. (2005) noticed that it is not
a pollinator of choice for tomato because its foraging
period (08:00 to 11:00) does not coincide with the
receptivity period of tomato flower stigma (10:30 to
15:30). The characteristics of fruits pollinated by
M. quadrifasciata do not differ from those pollinated
by a handheld electric vibrator, but the insect
destroyed less flowers than the electric vibrator.
Palma et al. (2008) compared the managed bumblebee,
B. impatiens and Nannotrigona perilampoides,
a Mexican native bee in Conkal, Yucatán (Mexico).
The heavier fruits and the higher seed number were
obtained from flowers pollinated by B. impatiens.
Whittington & Winston (2004) also found that
B. impatiens (exotic species) was more effective than
B. occidentalis, because it visits flowers more fre-
quently and the colony grows larger. The effectiveness
of this species is favoured by its rapid collection of
pollen, the visit of a large number of flower-
sand a higher visitation frequency per flower and
time unit due to its more active foraging behaviour.
These characteristics could be considered as ideal for
tomato pollinators. One to two visits of B. impatiens
are sufficient to ensure a good pollination of tomato
flowers (Morandin et al., 2001b; Nunes-Silva et al.,
2013). However, Torres-Ruiz & Jones (2012) found
no significant difference between characteristics
(number of seeds per fruit, weight and diameter) of
fruits pollinated by B. impatiens and B. ephippiatus
(native pollinator) in State of Querétaro (Mexico),
because these pollinators had the same pollination
rate. This finding substantiates that of Asada & Ono
(1996). These results demonstrate that some native
pollinators could validly substitute exotic pollinators,
reducing ecological risks that might arise from com-
petition between exotic and native pollinators. Besides
competition, management of native pollinators may
be more cost-effective.
Some studies have also compared the efficacy of
different native pollinators. The comparison of
Amegilla zonata and Hoplonomia westwoodi, two
native bees in India, showed that tomato plants polli-
nated with the first yielded heavier and larger fruits
(Amala & Shivalingaswamy, 2017).
Globally, the managed bumblebee B. impatiens was
more effective than other pollinators except
B. ephippiatus. The effectiveness of this species, its avail-
ability and the mastering of its rearing could justify its
great use for pollination of tomatoes in North America
(Velthuis & Van Doorn, 2006). The honey bee
(A. mellifera) also improved some characteristics of
tomato fruits, but other pollinators have been reported
to be more effective. This situation probably explains the
low use of this species for tomato pollination, although it
is widely used for pollination of other crops (Klein et al.,
2007; Toni et al., 2018). However, Sabara & Winston
(2003) observed that the species could be a good pollina-
tor for greenhouse tomato during the winter, since it
significantly improved the production during this period.
Overall, insect pollinators (B. ephippiatus,
B. impatiens, N. perilampoides) are more effective
than hand pollination of tomato (Palma et al., 2008;
Vergara & Fonseca-Buendía, 2012). Besides, handheld
vibrators damage more flowers than insect pollinators.
These results confirm that insect pollinators could
effectively replace the hand pollination of tomatoes
under greenhouse and allow producers to reduce pro-
duction cost. Despite the efficiency of each pollinator
species, presence of more diverse pollinator commu-
nities improved better tomato yield (Higo et al., 2004;
Macias-Macias et al., 2009; Garibaldi et al., 2013). It is
THE JOURNAL OF HORTICULTURAL SCIENCE AND BIOTECHNOLOGY 9
therefore important to conserve natural habitats
around farmlands in order to continue to benefit
their services.
Bee colony management for tomato pollination
Several insects contribute to crop pollination when
harvesting floral resources. But the development of
intensive agriculture has decreased populations of
wild pollinators (Batra, 1995; Potts et al., 2003). This
situation has resulted in a pollination deficit in several
crops worldwide leading to yield reduction (Garibaldi
et al., 2011; Partap & Ya, 2012; Garibaldi et al., 2016).
To cope with pollination deficit in tomato and deliver
good pollination for greenhouse tomatoes, hormones
and handheld vibrators are commonly used (Dasgan &
Ozdogan, 2004; Velthuis & Van Doorn, 2006; Bispo Dos
Santos et al., 2009). Owing to disadvantages of these
techniques (expensive, time-consuming for hand pollina-
tion, destruction of several flowers), tomato growers
adopted the use of the bumblebee, Bombus terrestris in
1987 in Belgium (Velthuis & Van Doorn, 2006). The use
of this bee for tomato pollination has then been spread to
other countries and continents (Ruz, 2002; Velthuis &
Van Doorn, 2006). Companies specialised in the produc-
tion of B. terrestris colonies have been developed and
export colonies to other countries such as Chile, Japan,
Korea, Morocco, France, China and New Zealand
(Choukr-Allah, 1999; Ruz, 2002; Wu et al., 2008).
A subspecies of B. terrestris, B. t. canariensis has been
also used since 1994 to pollinate tomatoes in the Canary
Islands (Velthuis & Van Doorn, 2006; Koppert, 2017). In
the light of the success of B. terrestris, a species native to
Europe, coastal North Africa and West and Central Asia
(Winter et al., 2006), other species of the genus Bombus
were successfully tested and then introduced to ensure
pollination of tomato in some parts of the world. This
strategy aims to limit risks associated with the introduc-
tion of exotic species such as competition for resources,
crossbreeding with native species and the importation of
new pathologies. Thus, B. impatiens and B. occidentalis
have been identified to pollinate tomatoes in North
America, particularly in the United States, Canada and
Mexico (Morandin et al., 2001a; Palma et al., 2008). In
Asia, studies on the efficiency and breeding potential of
bumblebees such as B. hypocrita, B. ignitus, B. ardens,
B. diversus, B. lucorum (Asada & Ono, 1996, 2000; Peng et
al., 2003) resulted in the selection of B. ignitus, which is
already used for tomato pollination in Japan and China.
B. lucorum is also used to pollinate tomatoes in China
(Velthuis & Van Doorn, 2006; Wu et al., 2008). The use of
these different species of the genus Bombus ranks tomato
as the main beneficiary of pollination services provided
by managed bumblebee colonies around the world. In
fact, over 95% of colonies produced are used to pollinate
tomatoes (Velthuis & Van Doorn, 2006). Despite the
great success of tomato pollination with bumblebees,
these insects sometimes leave greenhouses to forage on
other plants without pollinating adequately tomato
(Morse, 2009).
In addition to bumblebees, the honey bee, A. mellifera
is also used to pollinate tomato. The use of this species
has been reported in some countries such as the United
Kingdom (Carreck et al., 1997) and South Africa (Brand,
2014). Sabara & Winston (2003) demonstrated that this
practice could be economically viable for both bee-
keepers and tomato growers.
It appears that managed pollination of tomato is
poorly documented and poorly used in Africa. This prac-
tice has been reported in South Africa with A. mellifera,
and in North Africa (Morocco, Egypt) with B. terrestris
where the species were commercially used (Velthuis &
Van Doorn, 2006). This situation could be due to the low
intensification of agriculture in the continent (Vandame
& Palacio, 2010; Van Der Valk et al., 2013), which still
favours crop pollination by wild pollinators. Indeed, it
was shown that wild pollinators improved fruit charac-
teristics and tomato yield by 25% in Kenya in Africa
(Kasina, 2007). The low production of tomatoes under
greenhouse, i.e. tomato is most produced in the open
fields and the poor awareness of farmers about pollina-
tion services on the continent (Bosselmann & Hansted,
2015) could also explain the low use of managed bees for
tomato pollination. Several bee species effectively polli-
nate tomatoes worldwide, but the unavailability of
a rearing protocol still hampers their use for managed
pollination. This calls for the development of rearing and
management strategies for highly effective bee species in
order to fully exploit their potential in tomato
production.
Disclosure statement
We declare that there is no conflict of interest.
ORCID
Mathieu Anatole Tele Ayenan http://orcid.org/0000-
0001-5774-9029
References
Al-Attal, Y.Z., Kasrawi, M.A., & Nazer, I.K. (2003).
Influence of pollination technique on greenhouse tomato
production. Agricultural and Marine Sciences, 8, 21–26.
Aldana, J., Cure, J.R., Almanza, M.T., Vecil, D., &
Rodríguez, D. (2007). Efecto de Bombus atratus
Hymenoptera: Apidae) sobre la productividad de tomate
(Lycopersicon esculentum) invernadero en la Sabana de
Bogotá, Colombia. Agronomía Colombiana, 25, 62–72.
Amala, U., & Shivalingaswamy, T.M. (2017). Role of native
buzz pollinator bees in enhancing fruit and seed set in
10 H. C. TONI ET AL.
tomatoes under open field conditions. Journal of
Entomology and Zoology Studies, 5, 1742–1744.
Asada, S., & Ono, M. (1996). Tomato pollination with Japanese
native bumblebees (Bombus spp.). Applied Entomology and
Zoology, 31, 581–586. doi:10.1303/aez.31.581
Asada, S., & Ono, M. (2000). Difference in colony develop-
ment of two Japanese bumblebees, Bombus hypocrita and
Bombus ignitus (Hymenoptera: Apidae). Applied
Entomology and Zoology, 35, 597–603. doi:10.1303/
aez.2000.597
Bailey, L.H. (1891). Experiments in the forcing of tomatoes
N. Y. (Cornell). Agricultural Experiment Station Bulletin,
28, 45.
Batra, S.W.T. (1995). Bees and pollination in our changing
environment. Apidologie, 26, 361–370. doi:10.1051/
apido:19950501
Bell, M.C., Spooner-Hart, R.N., & Haigh, A.M. (2006).
Pollination of greenhouse tomatoes by the Australian
bluebanded bee Amegilla (Zonamegilla) holmesi
(Hymenoptera: Apidae). Journal of Economic
Entomology, 99, 437–442. doi:10.1093/jee/99.2.437
Benachour, K. (2008). Diversité et activité pollinisatrice des
abeilles (Hymenoptera: Apoidea) sur les plantes cultivées
(Thèse de doctorat). Algérie: Faculté des Sciences de la
Nature et de la Vie- Université Mentouri de Constantine,
151.
Bispo Dos Santos, A., Roselino, A.C., Hrncir, M., & Bego, L.
R. (2009). Pollination of tomatoes by the stingless bee
Melipona quadrifasciata and the honey bee Apis mellifera
(Hymenoptera, Apidae). Genetics and Molecular
Research, 8, 751–757. doi:10.4238/vol8-2kerr015
Bosselmann, A.S., & Hansted, L. (2015, September 16–19).
Payments for pollination services – An unexplored oppor-
tunity for African beekeepers. Abstract book of the 44th
APIMONDIA International Apicultural Congress held at
Daejeon, Korea.
Brand, M. (2014). Pollination ecosystem services to onion
hybrid seed crops in South Africa (PhD thesis). South
Africa: Faculty of AgriSciences - Stellenbosch
University, 164.
Buchmann, S.L. (1983). Buzz pollination in angiosperms. In
C.E. Jones & R.J. Little (Eds.), Handbook of experimental
pollination biology (pp. 73–113). New York: Van
Nostrand-Rheinhold.
Carreck, N., Williams, I., & Little, D. (1997). The movement
of honey bee colonies for crop pollination and honey
production by beekeepers in Great Britain. Bee World,
78, 67–77. doi:10.1080/0005772X.1997.11099337
Cauich, O., Quezada-Euán, J.J.C., Macias-Macias, J.O.,
Reyes-Orecel, V., Medina-Peralta, S., & Parra-Tabla, V.
(2004). Behaviour and pollination efficiency of
Nannotrigona perilampoides (Hymenoptera: Meliponini)
on greenhouse tomatoes (Lycopersicon esculentum) in
sub-tropical Mexico. Journal of Economic Entomology,
97, 475–481. doi:10.1603/0022-0493-97.2.475
Chougourou, D., Agbaka, A., Adjakpa, J., Ehinnou
Koutchika, R., Kponhinto, U., & Adjalian, E. (2012).
Inventaire préliminaire de l’entomofaune des champs de
tomates (Lycopersicon esculentum Mill) dans la
Commune de Djakotomey au Bénin. International
Journal of Biological and Chemical Sciences, 6, 1798–1803.
Choukr-Allah, R. (1999). Protected culture in Morocco. In
R. Choukr-Allah (Ed.), Cultures protégées dans la région
Méditerranéenne (pp. 9–15). Agadir (Maroc): IAV
Hassan II. (Cahiers Options Méditerranéennes 31).
Colloque sur les Cultures Protégées dans la Région
Méditerranéenne, 1996/10/06-09. Agadir, Maroc.
Retrieved from http://ressources.ciheam.org/om/pdf/
c31/CI020827.pdf
Dasgan, H.Y., & Ozdogan, A. (2004). Effectiveness of bum-
blebee pollination in anti-frost heated tomato green-
houses in the Mediterranean Basin. Turkish Journal of
Agriculture and Forestry, 28, 73–82.
Del Sarto, M.C.L., Peruquetti, R.C., & Campos, L.A.O.
(2005). Evaluation of the neotropical bee Melipona quad-
rifasciata (Hymenoptera: Apidae) as pollinator of green-
house tomatoes. Journal of Economic Entomology, 98,
260–266. doi:10.1093/jee/98.2.260
Denham, T. (2014). Tomatoes: Origins and development.
In: C. Smith (Ed.), Encyclopedia of global archaeology (pp.
7316–7319). New York, NY: Springer. doi:10.1007/978-
1-4419-0465-2
Deprá, M.S., Delaqua, G.C.G., Freitas, L., & Gaglianone, M.
C. (2014). Pollination deficit in open-field tomato crops
(Solanum lycopersicum L., Solanaceae) in Rio de Janeiro
state, southeast Brazil. Journal of Pollination Ecology, 12,
1–8. doi:10.26786/1920-7603(2014)7
Dogterom, M.H., Matteoni, J.A., & Plowright, R.C. (1998).
Pollination of greenhouse tomatoes by the North American
Bombus vosnesenskii (Hymenoptera: Apidae). Journal of
Economic Entomology, 91, 71–75. doi:10.1093/jee/91.1.71
Estay, P., Wagner, A., & Escaff, M. (2001). Evaluation of
Bombus dahlbomii (Guer.) as a pollinating agent for
tomato (Lycopersicon esculentum (Mill.)) flowers under
greenhouse conditions. Agricultura Técnica, 61, 113–119.
doi:10.4067/S0365-28072001000200001
FAOSTAT. (2020, May 1). Statistical division of the food and
agriculture organization of the United Nations. Retrieved
from http://www.fao.org/faostat/en/#compare
Free, J.B. (1993). Insect pollination of crops. London:
Academic Press.
Freitas, L. (2013). Concepts of pollinator performance: Is
a simple approach necessary to achieve a standardized
terminology? Brazilian Journal of Botany, 36, 3–8.
doi:10.1007/s40415-013-0005-6
Gaglianone, M.C., Campos, M.J.O., Franceschinelli, E.,
Deprá, M.S., Slva, P.N., Montagnana, P.C., . . .
Campos, L.A.O. (2015). Plano de manejo para os polini-
zadores do tomateiro (pp. 48). Rio de Janeiro: Funbio.
Garibaldi, L., Carvalheiro, L.G., Vaissière, B.E., Gemmill-
Herren, B., Hipólito, J., Freitas, B.M., . . . Åström, J.
(2016). Mutually beneficial pollinator diversity and crop
yield outcomes in small and large farms. Science, 35,
388–391. doi:10.1126/science.aac7287
Garibaldi, L.A., Aizen, M.A., Klein, A.M., Cunningham, S.
A., & Harder, L.D. (2011). Global growth and stability of
agricultural yield decrease with pollinator dependence.
Proceedings of the National Academy of Sciences of the
United States of America, 108, 5909–5914.
Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.
A., Bommarco, R., Cunningham, S.A., & Klein, A.M.
(2013). Wild pollinators enhance fruit set of crops regard-
less of honey bee abundance. Science, 339, 1608–1611.
doi:10.1126/science.1230200
Gemmill, B., Kinuthia, W., & Eardley, C. (2019). Overview of
pollination in agrobiodiversity planning: Principles and
best practices. Retrieved from https://www.cbd.int/doc/
nbsap/agriculture/pollination.pdf
Goulson, D. (2003). Effects of introduced bees on native
ecosystems. Annual Review of Ecology, Evolution, and
Systematics, 34, 1–26. doi:10.1146/annurev.
ecolsys.34.011802.132355
Greenleaf, S.S., & Kremen, C. (2006). Wild bee species
increase tomato production and respond differently to
THE JOURNAL OF HORTICULTURAL SCIENCE AND BIOTECHNOLOGY 11
surrounding land use in Northern California. Biological
Conservation, 133, 81–87. doi:10.1016/j.
biocon.2006.05.025
Hanna, H.Y. (1999). Assisting natural wind pollination of
field tomatoes with an air blower enhances yield.
Hortscience, 34, 846–847. doi:10.21273/
HORTSCI.34.5.846
Higo, H.A., Rice, N.D., Winston, M.L., & Lewis, B. (2004).
Honey bee (Hymenoptera: Apidae) distribution and
potential for supplementary pollination in commercial
tomato greenhouses during winter. Journal of Economic
Entomology, 97, 163–170. doi:10.1093/jee/97.2.163
Hikawa, M., & Miyanaga, R. (2009). Effects of pollination by
Melipona quadrifasciata (Hymenoptera: Apidae) on
tomatoes in protected culture. Applied Entomology and
Zoology, 44, 301–307. doi:10.1303/aez.2009.301
Hogendoorn, K., Coventry, S., & Keller, M. (2007). Foraging
behaviour of a blue banded bee, Amegilla chlorocyanea in
greenhouses: Implications for use as tomato pollinators.
Apidologie, 38, 86–92. doi:10.1051/apido:2006060
Hogendoorn, K., Sedgley, M., Gross, C.L., & Keller, M.
(2006). Increased tomato yield through pollination by
native Australian blue-banded bees (Amegilla chlorocya-
nea Cockerell). Journal of Economic Entomology, 99,
828–833. doi:10.1093/jee/99.3.828
Hogendoorn, K., Steen, Z., & Schwarz, M.P. (2000). Native
Australian carpenter bees as a potential alternative to
introducing bumble bees for tomato pollination in
greenhouses. Journal of Apicultural Research, 39, 67–74.
doi:10.1080/00218839.2000.11101023
Karlsson, M. (2017). Pollination and fruit development in
tomatoes. Alaska, USA: University of Alaska Fairbanks
Cooperative Extension Service, United States Department
of Agriculture.
Kasina, J.M. (2007). Bee pollinators and economic impor-
tance of pollination in crop production: Case of
Kakamega, western Kenya (PhD dissertation). Germany:
University of Bonn, 150.
Kevan, P.G., Straver, W.A., Offer, M., & Laverty, T.M.
(1991). Pollination of greenhouse tomatoes by bumble-
bees in Ontario. Proceedings of the Entomological Society
of Ontario, 122, 15–19.
Klatt, B.K., Burmeister, C., Westphal, C., Tscharntke, T., &
von Fragstein, M. (2013). Flower volatiles, crop varieties
and bee responses. PloS One, 8, e72724. doi:10.1371/jour-
nal.pone.0072724
Klatt, B.K., Holzschuh, A., Westphal, C., Clough, Y., Smit, I.,
Pawelzik, E., & Tscharntke, T. (2014). Bee pollination
improves crop quality, shelf life and commercial value.
Proceedings of the Royal Society B, 281, 20132440.
doi:10.1098/rspb.2013.2440
Klein, A.M., Vaissiere, B., Cane, J.H., Steffan-Dewenter, I.,
Cunningham, S.A., Kremen, C., & Tscharntke, T. (2007).
Importance of crop pollinators in changing landscapes
for world crops. Proceedings of the Royal Society of
London: Series B. Biological Sciences, 274, 303–313.
doi:10.1098/rspb.2006.3721
Koppert. (2017). Retrieved from https://www.koppert.com/
Levy, A., Rabinowitch, H.D., & Kedar, N. (1978).
Morphological and physiological characters affecting
flower drop and fruit set of tomatoes at high
temperatures. Euphytica, 27, 211–218. doi:10.1007/
BF00039137
Macias-Macias, O., Chuc, J., Ancona-Xiu, P., Cauich, O., &
Quezada-Euan, J.J.G. (2009). Contribution of native bees
and Africanized honey bees (Hymenoptera: Apoidea) to
Solanaceae crop pollination in tropical Mexico. Journal of
Applied Entomology, 133, 456–465. doi:10.1111/j.1439-
0418.2009.01399.x
Morandin, L.A., Laverty, T.M., & Kevan, P.G. (2001a).
Bumble bee (Hymenoptera: Apidae) activity and pollina-
tion levels in commercial tomato greenhouses. Journal of
Economic Entomology, 94, 462–467. doi:10.1603/0022-
0493-94.2.462
Morandin, L.A., Laverty, T.M., & Kevan, P.G. (2001b).
Effect of bumble bee (Hymenoptera: Apidae) pollination
intensity on the quality of greenhouse tomatoes. Journal
of Economic Entomology, 94, 172–179. doi:10.1603/0022-
0493-94.1.172
Morse, A. (2009). Floral scent and pollination of greenhouse
tomatoes (Master of Science thesis). Canada: Faculty of
Graduate Studies of The University of Guelph, 139.
Nunes-Silva, P., Hnrcir, M., Shipp, L., Imperatriz-
Fonseca, V.L., & Kevan, G.P. (2013). The behaviour of
Bombus impatiens (Apidae, Bombini) on tomato
(Lycopersicon esculentum Mill., solanaceae) flowers:
Pollination and reward perception. Journal of
Pollination Ecology, 11, 33–40. doi:10.26786/1920-
7603(2013)3
Ogunniyi, L.T., & Oladejo, J.A. (2011). Technical efficiency
of tomato production in Oyo State Nigeria. Agricultural
Science Research Journal, 1, 84–91.
Palma, G., Quezada-Euán, J.J.G., Reyes-Oregel, V.,
Meléndez, V., & Moo-Valle, H. (2008). Production of
greenhouse tomatoes (Lycopersicon esculentum) using
Nannotrigona perilampoides, Bombus impatiens and
mechanical vibration (Hym.: Apoidea). Journal of
Applied Entomology, 132, 79–85. doi:10.1111/j.1439-
0418.2007.01246.x
Partap, U., & Ya, T. (2012). The human pollinators of fruit
crops in Maoxian County, Sichuan, China, a case study of
the failure of pollination services and farmers’ adaptation
strategies. Mountain Research and Development, 32,
176–186. doi:10.1659/MRD-JOURNAL-D-11-00108.1
Peng, W.J., Wu, J., Guo, Z.B., & An, J.D. (2003). A study on
mating of Bombus lucorum under artificial conditions
and the influential factors. Journal of Bee, 54, 3–4. (in
Chinese).
Petit, J. (2003). Identification et validation fonctionnelle de
gènes candidats contrôlant la composition de la cuticule
chez le fruit de tomate (Thèse de doctorat). France: Ecole
Doctorale des Sciences de la Vie et de la Santé, Université
de Bordeaux I, 168.
Picken, A.J.F. (1984). A review of pollination and fruit set in
the tomato (Lycopersicon esculentum Mill.). Journal of
Horticultural Science, 59, 1–13. doi:10.1080/
00221589.1984.11515163
Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P.,
Schweiger, O., & Kunin, W. E. (2010). Global pollina-
tor declines: trends, impacts and drivers. Trends in
ecology & evolution, 25(6), 345–353. doi:10.1016/j.
tree.2010.01.007
Pressman, E., Shaked, R., Rosenfeld, K., & Hefetz, A. (1999).
A comparative study of the efficiency of bumble bees and
an electric bee in pollinating unheated greenhouse
tomatoes. Journal of Horticultural Science and
Biotechnology, 74, 101–104. doi:10.1080/
14620316.1999.11511080
Ranc, N. (2010). Analyse du polymorphisme moléculaire de
gènes de composantes de la qualité des fruits dans les
ressources génétiques sauvages et cultivées de tomate;
recherche d’associations gènes/QTL (Thèse de doctorat).
France: Ecole Nationale Superieure Agronomique de
Montpellier – Supagro, 263.
12 H. C. TONI ET AL.
Rodger, J.G., Balkwill, K., & Gemmill, B. (2004). African
pollination studies: Where are the gaps? International
Journal of Tropical Insect Science, 24, 5–28. doi:10.1079/
IJT20045
Ruz, L. (2002). Bee pollinators introduced to Chile:
A review. In: P. Kevan & V.L. Imperatriz Fonseca
(Eds.), Pollinating Bees - The conservation link between
agriculture and nature (pp. 155–167). Brasília, Brazil:
Ministry of Environment.
Sabara, H., & Winston, M.L. (2003). Managing honeybees
(Hymenoptera: Apidae) for greenhouse tomato
pollination. Journal of Economic Entomology, 96,
547–554. doi:10.1093/jee/96.3.547
Santos, A.O.R., Bartelli, B.F., & Nogueira-Ferreira, F.H.
(2014). Potential pollinators of tomato, Lycopersicon escu-
lentum (Solanaceae), in open crops and the effect of
a solitary bee in fruit set and quality. Journal of
Economic Entomology, 107, 987–994. doi:10.1603/
EC13378
Silva-Neto, C.M., Bergamini, L.L., Elias, M.A.S., Moreira, G.
L., Morais, J.M., Bergamini, B.A.R., & Franceschinelli, E.
V. (2017). High species richness of native pollinators in
Brazilian tomato crops. Brazilian Journal of Biology, 77,
506–513. doi:10.1590/1519-6984.17515
Silva-Neto, C.M., Lima, F.G., Gonçalves, B.B., Lima, L.B.,
Bergamini, B.A.R., Elias, M.A.S., & Franceschinelli, E.V.
(2013). Native bees pollinate tomato flowers and increase
fruit production. Journal of Pollination Ecology, 11, 41–45.
Tchuenguem Fohouo, F.-N., Tope, S.N., & Bruckner, D.
(2014). Foraging and pollination behaviour of Xylocopa
olivacea (Hymenoptera: Apidae) on Phaseolus coccineus
(Fabaceae) flowers at Ngaoundéré (Cameroon).
International Journal of Tropical Insect Science, 34,
127–137. doi:10.1017/S1742758414000241
Teppner, H. (2005). Pollinators of tomato, Solanum lycopersi-
cum (Solanaceae) in Central Europe. Phyton, 45, 217–235.
Toni, C.H., Djossa, B.A., Yédomonhan, H., Zannou, E.T., &
Mensah, G.A. (2018). Western honey bee Apis mellifera
management for crop pollination. African Crop Science
Journal, 26, 26: 1–17. doi:10.4314/acsj.v26i1.1
Torres-Ruiz, A., & Jones, R.W. (2012). Comparison of the
efficiency of the bumble bees Bombus impatiens and
Bombus ephippiatus (Hymenoptera: Apidae) as pollina-
tors of tomato in greenhouses. Journal of Economic
Entomology, 105, 1871–1877. doi:10.1603/EC12171
Tuell, J.K., & Isaacs, R. (2010). Weather during bloom affects
pollination and yield of highbush blueberry. Journal of
Economic Entomology, 103, 557–562. doi:10.1603/EC09387
USDA. (2019, January). Retrieved from https://ndb.nal.
usda.gov/ndb/foods/show/11529
van Dam, B., Goffau, M., van Lidt, J., & Naika, S. (2005). La
culture de la tomate: Production, transformation et com-
mercialisation (pp. 105). Agrodok 17. Wageningen- Pays-
Bas: Agromisa/ CTA.
Van Der Valk, H., Koomen, I., Nocelli, R.C.F., Ribeiro, M.D.F.,
Freitas, B.M., Carvalho, S., . . . Mutiso, M. (2013). Aspects
determining the risk of pesticides to wild bees: Risk profiles for
focal crops on three continents (pp. 67). Rome, Italy: FAO.
Pollination services for sustainable agriculture, field
manuals.
Vandame, R., & Palacio, M.A. (2010). Preserved honey bee
health in Latin America: A fragile equilibrium due to
low-intensity agriculture and beekeeping? Apidologie,
41, 243–255. doi:10.1051/apido/2010025
Velthuis, H.H.W., & Van Doorn, A. (2006). A century of
advances in bumblebee domestication and the economic
and environmental aspects of its commercialization for
pollination. Apidologie, 37, 421–451. doi:10.1051/
apido:2006019
Vergara, C.H., & Fonseca-Buendía, P. (2012). Pollination of
greenhouse tomatoes by the Mexican bumblebee Bombus
ephippiatus (hymenoptera: Apidae). Journal of
Pollination Ecology, 7, 27–30. doi:10.26786/1920-7603-
(2012)1
Vinícius-Silva, R., Parma, D., Tostes, R., Arruda, V., &
Werneck, M. (2017). Importance of bees in pollination
of Solanum lycopersicum L. (Solanaceae) in open-field of
the Southeast of Minas Gerais State, Brazil. Hoehne, 44,
349–360. doi:10.1590/2236-8906-07/2017
Westphal, C., Steffan-Dewenter, I., & Tscharntke, T. (2003).
Mass flowering crops enhance pollinator densities at
a landscape scale. Ecology Letters, 6, 961–965.
doi:10.1046/j.1461-0248.2003.00523.x
Whittington, R., & Winston, M.L. (2004). Comparison and
examination of Bombus occidentalis and Bombus impa-
tiens (Hymenoptera: Apidae) in tomato greenhouses.
Journal of Economic Entomology, 97, 1384–1389.
doi:10.1093/jee/97.4.1384
Whittington, R., Winston, M.L., Tucker, C., &
Parachnowitsch, A.L. (2004). Plant-species identity of
pollen collected by bumblebees placed in greenhouses
for tomato pollination. Canadian Journal of Plant
Science, 84, 599–602. doi:10.4141/P02-192
Winter, K., Thorp, R., Inouye, D., Day, L., Ascher, J., &
Buchmann, S. (2006). Importation of non-native bumble
bees into North America: Potential consequences of using
Bombus terrestris and Other non-native bumble bees for
greenhouse crop pollination in Canada, Mexico, and the
United States (pp. 33). Washington, DC: North American
Pollinator Protection Campaign (NAPPC).
Wu, J., Cai, W., Peng, W., An, J., & Huang, J. (2008).
Comparison of the colony development of two native
bumblebee species Bombus ignitus and Bombus lucorum
as candidates for commercial pollination in China.
Journal of Apicultural Research and Bee World, 47,
22–26. doi:10.3896/IBRA.1.47.1.04
Xerces Society for Invertebrate Conservation. (2019). Native
Bee pollination of cherry tomatoes. Retrieved from www.
xerces.org/wp. . ./factsheet_cherry_tomato_pollination.pdf
Yoon, H.J., & Park, I.G. (2019). Current status and agricultural
utilization of insect pollinators in Korea. Retrieved from
www.niaes.affrc.go.jp/sinfo/sympo/h22/1109/paper_07.pdf
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