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The pollination biology of onion (Allium cepa L.)-A Review

Article · April 2015


DOI: 10.5958/0976-0741.2015.00001.X

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Agri. Review, 36 (1) 2015 : 1-13 AGRICULTURAL RESEARCH COMMUNICATION CENTRE
Print ISSN:0253-1696 / Online ISSN:0976-0539 www.arccjournals.com

The pollination biology of onion (Allium cepa L.)- A Review


Sunita Devi, Rachna Gulati, Kanika Tehri* and Asha Poonia
Department of Zoology,
CCS Haryana Agricultural University, Hisar-125 004, India.
Received: 18-12-2014 Accepted: 23-02-2015 DOI: 10.5958/0976-0741.2015.00001.X
ABSTRACT
Managed pollination is an essential input in enhancing the crop productivity. In recent years, there has been an increase in
the accumulation of data to indicate that seed yields of insect pollinated crops may often be lower than the expected, not
because of adverse climatic, edaphic or cultural factors, but simply because the number of certain pollinators is inadequate.
In absence of pollination in many entomophilous crops, fruit or seed set is affected adversely even if all the cultural practices
are followed meticulously. Insect pollinators set a greater proportion of early flowers of the crop and increase quality and
quantity of the seed yield. Before the use of managed pollination, it is necessary to have a basic knowledge of factors which
influence pollinator activity and preference of the pollinators for different crops. This review summarizes the pollination
biology of the important vegetable crop, Allium cepa L., commonly known as onion.
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Key words: Abundance,Floral biology, Male sterility, Mode of pollination, Onion, Pollinators, Yield.
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Allium is the genus of onions with about 1250 The height may vary from 0.9 m to 1.2m depending on the
species of perennial bulbous plants. Onions are among the genotype and other factors. Flowers in the umbel are enclosed
world’s oldest cultivated plants. They were probably known in a membranous 2-3 white coloured sheath called spathe.
in India, China, and the Middle East before recorded history. The sheath splits because of the pressure created by growing
Ancient Egyptians regarded the spherical bulb as a symbol flowers inside the umbel. There may be 50 -2000 florets in
of the universe. It is considered as native to southwestern an Inflorescence depending on the genotype, planting time,
Asia but is now grown throughout the world, chiefly in the size and storage conditions of the mother bulb. The flowers
temperate regions. Onion makes an important source of are white to bluish in colour. The perianth segments are six
vegetable and its seeds are source of condiments (Baswana, in two whorls spreading, reflexed, free and ovate. The stamens
1984). There are several species of Allium or onion that are are also six in two whorls. Anthers are bilocular and the ovary
grown exclusively for their flowers instead of their bulbous is superior. Anthers may be green or purple in colour
structures.Allium cepa L. is a liliaceous crop, which is grown depending upon genotype. The colour also changes with
in different parts of world and its cultivation is becoming the age of flower. Some florets have two ovaries with seven
popular in a state like Haryana too (Sihag, 1985). In India it stamens.Anthesis occurs in early morning (6-7 h). Anther
has been grown in 0.52million ha with the production of 6.5 dehiscence takes place between 7.00 and 17.00 h and on
million tones (FAO, 2002). The productivity of onion in India next day also with peak between 9.30 and 17.00 h. Pollen
is 12.5 t/ha, which is much lower than the productivity of fertility is highest on the days of anthesis. Stigma receptivity
USA (41.12 t/ha)(FAO, 2002). The higher productivity of is also high on the day of anthesis (Jones, 1933). The
onion in USA is due to the growing of the long day hybrids duration of anthesis is approximately four weeks on
and crop varieties.The literature pertaining to floral biology, individual umbel. The anthesis begins from outer flowers
pollinators and their abundance, foraging behaviour, and goes centrally in succession. The flower is protandrous
pollination efficiency and effect of mode of pollination on in nature and stigma becomes receptive when shedding of
onion yield is reviewed below: pollen is over. Male-sterile and male-fertile lines differed
Floral biology: The crop is strongly protandrous; self in their stigma and style characteristics and pattern of
pollination is largely absent which depends upon insects for development. At flower opening, the styles of male-sterile
cross pollination (Baswana, 1984). Inflorescence is present lines were longer and the stigmatic knob became receptive
at the top of the green plant which is hollow from the inside. relatively sooner (Ali et al., 1984).

*Corresponding author’ e-mail: knkzoology@gmail.com.


2 AGRICULTURAL REVIEWS
Diversity of insect visitors on onion umbels: Onion umbels pollen, nectar sugar concentration, quality of nectar, body
are visited by honey bees, small syrphid flies, bumble bees, size and tongue length of pollinators, floral shape, size and
halictid bees, drone flies, butterflies and insects of minor colour are known to cause orientation in honey bees to locate
importance with respect to pollination (Sajjad et al., 2008). food source of their choice. Honey bees have certain
The blossoms of onion are highly attractive to both pollen idiosyncrasies which are very useful for pollination point of
and nectar collecting insects (Free, 1993). Kordakova (1956) view and generally increase their efficiency as pollinators
and Sakharov (1956) gave major credit to the honey bee as a (Free, 1993). Honey bees are known to be “fairly faithful”
pollinator of onions in Russia. Bohart etal. (1970) reported and “constant” to plants and become “fixed” to small area of
267 species of insect visitors on onion flowers, the most crops being worked by them for collecting nectar and
important of which were honey bees, small syrphid flies, pollens.The blossoms of onion crop are highly attractive to
halictid bees and drone flies. Of these, only the honey bee pollen and nectar collecting insects. The receptivity of stigma
can be manipulated and used in large-scale onion seed within one to two days, provides better chance to the plant to
production. Apart from honey bees, Halictus farinosus get pollinated by insects (Baswana, 1984). Higher seed yield
(Parker, 1982), butterflies (Jaboñski et al.,1982;), Bombus of the crops may be obtained by the maintenance of a large
occidentalis, Megachile rotundata, Osmia lignaria, Osmia population of pollinating insects due to visit by a large number
cornifons and Nomia melanderi (Mayer and Lunden, 2001), of pollinating species to the crop (Sihag, 1985, 1986; Free,
Osmia rufa (Wilkaniec et al., 2002) and syrphid flies were 1993; Singh and Hameed, 1995).
also recorded to take part in the process of pollination Honey bees are considered as the primary agents
(Chaudhary, 2004).
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for pollination in onion crop (Walsh 1965). Rao and Lazer


The predominance of honey bees in the range of (1980) gave major credit to the honey bee as a pollinator of
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60-95 per cent was recorded by many workers (Singh and onions, however, Halictus farinosus and Osmia rufa was
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Dharamwal, 1970; Parker and Hatley, 1978; Jadhav, 1981; found to be the most abundant pollinator of onion by Parker
Kumar et al., 1985). Under sub-temperate conditions of (1982) and Wilkaniec et al. (2002), respectively. On Allium
Himachal Pradesh situated at an altitude of 1200 m above sp., the dominance of the giant bee A. dorsata as efficient
mean sea level, Apis dorsata, A. florea and syrphids pollinator was recorded by many workers (Chaudhary, 2004;
(Episyrphus balteatus, Metasyrphus conferator and M. Shafqat and Masood, 2008). Jadhav (1981) also reported that
corollae) were important visitors (Chandel et al., 2004). Saeed A. florea is the most important pollinator for onion var. N-
et al. (2008) reported the presence of four bee species and 53. A. cerana was considered as more efficient pollinator by
twelve true fly species as community of pollinators on onion, Rao and Suryanarayana (1989) on the basis of visiting more
whereas Shafqat and Masood (2008) reported two
number of florets and umbels in a unit time than A. florea
Hymenopteran bees and eight true flies of Diptera as
and Trigona iridipennis.Among the pollinators, A. dorsata
pollinators of onion crop.
was found to be a predominant visitor covering an average
Pollinator abundance and activity on onion umbels: For of 7.5 flowers per umbel per visit during peak hours of their
different crops, different pollinators are responsible to effect foraging activity (1200-1400 h) followed by A. cerana (5.4
cross pollination. Almost every order of insects has been flower/umbel/visit) ascompared to A. florea, A. mellifera and
reported to play a role in the pollination of flowering
syrphid flies (Chandel et al., 2004). In the same study,
vegetables and spice crops. McGregor (1976) and Free(1993)
Syrphids covered a minimum of 1.6 flowers/umbel/visit, yet
reported that insects like ants, aphids, bees, beetles, butterflies,
spent maximum time (8.8 seconds) on the flowers during 800-
flies, midges, mosquitoes, moths, thrips and wasps act as
1200 hours. Apis dorsata had the maximum foraging period
pollinators in cultivated crops. Among them, bees are
considered to be the most important pollinators because they (0630-1855 h) followed by A. cerana (0645-1830 h) and A.
are the only insects whose immature stages are reared mellifera had the least foraging period (0725-1820 h) on onion
exclusively on pollen and nectar (Crane, 1990). Crailsheim seed crop. In contrast to previous report where A. cerana
(1991) has reported that the adult worker honey bees feed was considered as second most abundant pollinator,
upon pollen to produce royal jelly for the queen bees, the Chaudhary and Sihag (2003) reported A. florea as the second
brood, the adult workers of different age and the drones. The most abundant species on onion after A. dorsata.According
younger bees are the nurse bees which feed upon pollen to Witter and Blochtein (2003), A. mellifera transported more
mainly to produce royal jelly from their highly developed than 70 percent of pollen and become indispensable in onion
hypopharyngeal glands. Priti and Sihag (1997) found that pollination.
Vol. 36 No. 1, 2015 3
Effect of nectar on foraging behavior: The foraging activity plant species recorded floral nectar sugar concentration
of honey bees on onion inflorescences is dependent on the ranging between 4-87 per cent (Vansell, 1934; Fahn, 1949
interactions of several factors like nectar quality, sugar and Percival, 1965). Some of the species reported by Shuel
quantity, potassium content etc. Waller (1970) believed that (1955) having remarkable high concentration of sugar are
a high level of potassium in the nectar might be an important Astragalus pachypus (59.2%), Salix sp. (60%) Robinia
clue to the reluctance of bees to visit onion flowers. Jula et pseudo-acasia (63%) Aesculus sp. (72.2%) and Vitis sp.
al. (1965) calculated that onions produced 71 percent as much (75%). Gegear and Thompson (2004) observed a strong
nectar per day as the highly attractive sainfoin. Similarly, Silva positive relationship between degree of flower constancy and
and Dean (2000) observed that in nine inbred lines of onion rate of net energy gain indicating that honey bees were more
(A. cepa), the average amount of nectar produced by umbels economic foragers. Abrol (2006) observed a significant
and the individual florets were significantly positively positive correlation between bee activity and nectar sugar
correlated with the number of bee visits. The mean number concentration.
of honey bees visiting on inflorescence every ten minutes Foraging activity: The density of insects on blossom depends
and the mean residing time of each honey bee on a seed stalk on several factors like flower shape, size, colour, availability
were significantly different among the cultivars. Hurand of floral rewards and weather conditions (Mevetty et al.,
flowers of onion had the least number of visitors and Dorche 1989). Insect pollinators have their specific ecological
flowers had the longest visiting time (Seyedebrahimi et al., threshold level, below which activity does not occur. The
2004). ecological threshold required for normal activity and its
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Nectar is recognized as the main attractant for maintenance differ inter- and intra- specifically depending
pollinators. Many workers have worked out a linear upon the level of adaptability of a species in a given
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relationship between the quantity and quality of nectar and environment (Kapil and Jain, 1980). Insect activity increases
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population of honey bees (Wykes, 1953; Mommers, 1977; sharply after sunshine, decreases gradually through the day
Corbet, 1978). Hagler et al. (1990) examined nectar and ceases before sunset (Oh and Woo, 1990). The daily flight
characteristics of six onion varieties and recorded that mean activity varies with the time of the day and meteorological
nectar amount ranged from 0.54 to 0.84µl per day. Mohr and variables, especially wind, rainfall, temperature and humidity
Jay (1990) found that mean daily nectar production and sugar (Sarviva, 1985). Bees collect pollen on cucumber in early
concentration for Brassica compestris cultivars were 0.68 µl morning and switch to nectar later in the morning. The first
and 57 per cent respectively and for B. napus cultivars were honey bee to visit a flower coats a large portion of the stigma
0.90 µl and 62 per cent respectively. The major sugar with pollen. Although there is less receptive surface on the
constituents of various nectar types are sucrose, glucose and stigma with each succeeding visit but multiple bee visits per
fructose (Wykes, 1952). Generally, pollinators with high flower (within the range of 1-20) increase fruit-set and average
energy requirements foraged on sucrose rich flowers, whereas number of seeds per fruit (Collison, 1976). In general, when
those with low energy requirements relied on glucose or bees start foraging they might collect nectar and/or pollen
fructose rich flowers (Abrol and Kapil, 1991). (Crane, 1990). Many bees that collect pollens change later in
Nectar sugar concentration is one of the most to the nectar, but once the bees start collecting nectar are
important factors affecting bee flower interaction. A positive unlikely to change to pollen collection. Flower visitors seem
correlation was found between attractiveness to bees and to prefer nectar collection even if it takes them much longer
nectar sugar concentration in citrus, suggesting that this time to get nectar. Honey bees collected nectar from both
characteristic is one of the parameters responsible for staminate (S) and pistillate (P) flowers but few bees collected
variability in attractiveness to honey bees (Wolf et al., 1999). pollens. Bees spent twice as long on ‘P’ flower as on ‘S’ flower
Generally high nectar sugar concentration was desirable for (Collison, 1973). Nemirovich-Danchenko (1964) observed
attracting the honey bees (Frisch, 1950; Meloyan 1975). that nectar secretion was greatest after 3 to 4 hours of the
Frisch (1950) reported the threshold value (5 to 40%) of sugar flower opening. Amaral et al. (1963) concluded that bees
concentration for its acceptance by the bees. Backman and show no preference for staminate over pistillate flowers. Bees
Waller (1971) observed that the bees rejected a solution with work on blossoms later in the day in springtime or in cooler
sugar concentration less than 20 per cent. It has also been climates than in summer or warmer climates.
reported that honey bees were able to discriminate a sugar McGregor (1976) showed that A. mellifera was
solution with a difference of 5 per cent concentration active between 0900-1300 h on onion umbels and collected
(Jamieson and Austin, 1956). Various workers in variety of heavy pollen loads during morning and at noon. Ewies and
4 AGRICULTURAL REVIEWS
El-Sahhar (1977) recorded 1100-1400 h as the most active florea started their activity in the morning (0700-0800h) and
period of the day for bee visitation on onion. According to remained active till evening (1800h).Yucel and Duman (2005)
Jadhav (1981), A. florea started foraging activity a little earlier recorded that A. mellifera visited 8, 13 and 4 flowers per
(0855 h) than A. dorsata (0930 h) and continued late hours minute at 0900, 1200 and 1500 h and collected 8, 10 and 6
in the evening (1700 h) as compared to A. dorsata which mg pollen from onion umbels. According to Shafqat and
stopped the day’s work at about 1625 h. Yucel and Duman Masood (2008), Eupeodes corollae (Syrphidae) exhibited the
(2005) observed that A. mellifera foraged on onion umbels most efficient foraging behaviour by visiting 17.14± 1.38
between 0815 to 1630 h and peak foraging was between 1100- flowers in 147.5± 8.14 seconds on an umbel.Saeed et al.
1200 h. (2008) recorded that honey bees began foraging on A fistulum
Foraging speed and rate: Foraging speed (time spent per flowers at about 0600 h and ceased at about 1900 h with a
flower) and foraging rate (number of flowers visited per min.) total foraging activity time of 1300 h which was slightly more
depend upon the foraging behaviour of insects and floral than the time recorded in the present study (1130 h for A.
structure of the crop concerned, particularly the corolla depth dorsata).
(Gilbert, 1980). Foraging is a trade between the amount of Loose pollen grains sticking to the body of a bee: The
nectar expected from a flower and time required to extract it honey bee becomes well dusted with pollen grains as a result
(Pyke et al., 1977). Inouye (1980) observed that more the of inserting their heads into the middle of the staminal column
nectar is available, more time will be spent per flower of a flower and curling their abdomen around anthers, thus,
however, both the parameters might be affected by the length they carry more pollen grains. Amount of loose pollen on the
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of proboscis (Inouye, 1980). The number of flowers visited body varies with the plant species and the varieties of a crop
by an insect species also depends upon the type of floral on which the insects are visiting. Furthermore, solitary bees
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reward (working for nectar and/or pollen), bloom and the have the advantage of carrying it in a drier condition, which
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density of flowers on a particular cultivar. is more likely to be rubbed of easily in to the stigmas of the
Foraging speed of the insect depends upon the flowers (Free, 1960). The amount of loose pollen grains on
foraging behaviour of the visitors and floral structure of the the body of an insect varies on different body parts. Usually,
crop (Free, 1993). Foraging speed varies among the insect it may be twice on bee’s thorax as on its abdomen. While
species. Apis cerana indica nectar foragers, visited 17.5 and working over flowers, pubescent hairs on their bodies may
25.0 flowers per minute in the morning and afternoon, entangle as many as 250000 to 300000 pollen grains
whereas, A. mellifera visited 25.8 and 33.6 flowers per minute (Skrebtsova, 1957). While visiting various flowers of the same
during the same hours (Gupta et al., 1984). Weather plant species honey bees are instrumental in disseminating
conditions have a pronounced effect on foraging speed of pollen and consequently accomplish the job of pollination
insects. Generally, adverse whether conditions increased the par excellence.
time spent per flower. Ideal conditions for bee-flying include In cucumber, honey bees exhibit no preference for
temperature greater than 21°C (70°F), humidity less than 75 staminate vs. pistillate flowers (Stephen, 1970), while
per cent, wind speed below 25 km/h (15 mph) and few or no Collison and Martin (1979) reported that the staminate
clouds (Meléndez-Ramirez et al., 2002). Foraging rate of flowers of cucumber were relatively more attractive than
foragers is influenced by the length of corolla tube apart from pistillate and this might be related to higher sugar
a complex system of factors like temperature, humidity etc. concentration found in the nectar of staminate flower. The
(Benedek, 1976). Rate of foraging by an individual bee amount of pollen carried on insect bodies and their viability
increases when the bee finds profitable flower patch (major was influenced by the onion cultivar and the visitor species
nectar source) but declines when the individual bee assess (Parker, 1982). Richard et al. (2003) reported that the
low profitability from its forages (Seeley et al., 1991). behavior of nectar foragers on staminate flowers differed
According to Ewies and El-Sahhar (1977), 2.6 bees/ according to body size. Large bees foraged for nectar mostly
min visited one umbel with 6.8 movements between the florets in the afternoon after nectar sugar concentrations reached
of an umbel. In another study, onion umbels received an high values, while smaller bees foraged for nectar throughout
average of 0.6 A. cerana bees/ min. and time spent by a bee the day.
on a flower was 3.3 seconds (Kumar et al., 1989). Rao and Sharma and Singh (2000) reported that the number
Suryanarayana (1989) observed that A. cerana, and A. florea of loose pollen grains sticking on an individual bee of two
initiated foraging at 0950-1130 h and ceased foraging at 1710- species, while foraging on sunflower head was counted to be
1815 h. Chaudhary (2004) reported that A. dorsata and A. 22900 and 20500 for A. dorsata and A. mellifera, respectively
Vol. 36 No. 1, 2015 5
at Hisar. Similarly, Kumar (2002) observed that the number (nectar robbers or side workers). This is considered to be the
of sunflower loose pollen grains sticking on the body surface most reliable method for computing pollination efficiency of
of A. dorsata was maximum (111109.40 during April 2002 insect visitors on different crops.
and 90623.45 during May 2002) followed by A. mellifera Insects visit the flower of commercial crops to seek
(74998.45 during April 2002 and 72917.70 during May nectar and/or pollen and contribute in pollination. The
2002). Hence, it was concluded that A. dorsata was most absolute necessity of insect pollination on fruit set in non-
efficient carrier of the loose pollen grains. Sharma and Singh parthenocarpic cucumber varieties as there was 100 per cent
(1999) reported that A. dorsata carried more number of carrot abortion for all pistillate flowers that received no
pollen grains (av. 5200) than A. florea (av. 4700). The number entomophilous visitation were demonstrated. Total abortion
of pollen grains sticking to the body of different bee species, of female flowers in the absence of bee visitation found in
while foraging Brassica campestris bloom was 13187, 4857 these experiments confirms the results of other studies on
and 11437 on A. dorsata, A. florea and A. mellifera, cucumber (Morris, 1968). However, relatively a few are
respectively (Sharma et al., 2000). Gill et al. (2001) stated consistently good pollinators. The different criteria to be used
that the number of loose pollen grains sticking on an for evaluating the relative efficiency of insect visitors are
individual bee of three species while foraging on phalsa abundance, foraging behaviour, loose pollen carrying
flowers were counted to be 6901.5 in case of A. dorsata capacities, multiplicities of bee visits and morphometrical
followed by 5506.3 and 4710.9 pollen grains in A. mellifera characters, i.e., body size, tongue length, pollen collecting
and A. florea, respectively. The number of loose pollen grains apparatus and hairyness. Various workers (Free, 1993)
sticking on an individual bees of two species while foraging
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considered the relative effectiveness of insect pollinators of


on onion flowers were counted to be 10187 (A. dorsata) and crops on the basis of their abundance alone. However, there
5625 (A. florea) at Hisar (Sharma et al., 2001).
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are inherent differences in the ability of various species to


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Pollination efficiency: Pollination efficiency of different affect pollination inspite of their abundance (Anderson et al.,
insect pollinators has been evaluated on the basis of number 1982). Therefore, efficiency of an insect as a pollinator has
of characteristics. Most of the workers (McGregor, 1976) also been attributed to its size, foraging behaviour and the
considered the relative effectiveness in the variability of amount of loose pollen grains adhering to its body (Free et
various species to affect pollination in spite of their abundance al., 1975). Baker et al. (1971) reported that the frequency of
(Anderson et al., 1982). Therefore, the efficiency of an insect flower visitors, the number of flower visited per unit time,
species as a pollinator has also been attributed to its size, the amount of pollen picked per visit helped to distinguish
foraging behaviour and the amount of loose pollen grains the pollinators as major and minor ones.
adhering to its body (Free et al., 1975). Brantjes and Leemans Kumar (2002) reported that Melissodes sp. was
(1976) considered that large sized insects were effective in found to be the best pollinator of cucumber blossoms. The
pollination of flowers due to their body contact with anthers Sarcophaga sp. and A. mellifera were ranked second and
and stigmas as compared to small size insects, which often third. Bumble bees (Bombus impatiens) visited flowers
missed their contact with anthers and stigmas while foraging consistently had a lower percent abortion than honey bees
for floral rewards. Therefore, different characteristics can be (A. mellifera) when compared at equal bee visit numbers
combined to determine the pollinating efficiency of insect (Stanghellini et al., 1997). Use of bees increased the
visitors/ Apis spp. on the basis of actual field observations productivity of hybrids Maiskii, TSKhA-1 and TSKhA-77
on abundance, their foraging behaviour, siliqua and seed set by 34.7, 50.0 and 21.2%, respectively (Kochetov, 2004). In
in B. campestries var. sarsonflowers, which were allowed watermelon, the anthesis in both staminate and pistillate
one visit by an Apis sp. and by using all these parameters for flowers took place in early morning (0600 h) and flowering
developing an equation. Based on size, hairiness, activity lasts for 6-9 h. Apis cerana (87%) was the principal
pattern and quantity of loose pollen grains carried by different pollinating insect at Vijayarai and was found to be more
pollinators, these are assigned pollinators’ efficiency rating. efficient pollinator than A. florea and Trigona irridipennis.
This efficiency rating is multiplied by the number of insects Apis cerana population was maximum at 0900 h; also during
concerned that are foraging on the crop (relative abundance) the period, the maximum pollen collectors were found at
to give relative pollination index for the species. For honey Andhra Pradesh (Rao and Suryanarayana, 1988).
and bumble bees, it is essential to take into account the The pollination efficiency of three honey bee species
proportion of nectar and/or pollen gatherers and the A. dorsata, A. florea and A. mellifera on phalsa flowers under
proportion that obtain forage without pollinating the flowers semi-arid subtropical conditions of Haryana showed that the
6 AGRICULTURAL REVIEWS
abundance of A. florea was maximum (4.88 bees/branch/5 Several other workers also reported that air
minute) than abundance of A. dorsata and A. mellifera was temperature significantly affected the foraging activities of
2.70 and 0.96 bees/branch/5 minute, respectively (Gill et al., honey bees as flower visiting rate was increased with
2001). The number of loose pollen grains sticking on A. increasing air temperature. Kwon and Saeed (2003) also
dorsata, A. mellifera and A. florea were 6901.5, 5506.3 and highlighted the importance of temperature on the foraging
4710.9, respectively. On the basis of pollination index, A. activity of Bombus terrestris L. Nuenz (1977) reported that
florea was found to be the most efficient pollinator (22989.2) morning activity of A. mellifera was related to nectar flow,
of this crop followed by A. dorsata and A. mellifera with a and afternoon activity with photoperiod. Gary (1975) stated
pollination index of 18634.0 and 2286.0, respectively (Gill that 13°C appeared to be the minimum threshold temperature
et al., 2001). Sharma et al. (2000) observed that A. dorsata for initiation of the field activities by the honey bees which
was the most efficient pollinator followed by A. mellifera continued at extremely high temperature of 43°C for water
and A. florea on ‘sarson’ bloom. Similarly, A. dorsata, having collection but at this temperature nectar and pollen foraging
a pollination index 162247 was found to be the most efficient was ceased. Whitcomb (1980) reported that A. florea worker
pollinator of sunflower than A. mellifera having a pollination bee did not forage at temperature below 18°C. Jain and Kapil
index of 124066 at Hisar (Sharma and Singh, 2000). In onion, (1980) reported that air temperature appeared to be a key
among different insect visitors, A. cerana indica was the most factor influencing the initiation of bee activity but cessation
dominant (68.30%) followed by T. irridipenis (46.66%) and was independent of air temperature. Alam et al. (1987)
A. florea (42.73%) (Rao and Lazer, 1980). However, Sharma observed that honey bee activity was highest when the
et al. (2001) reported that on the basis of pollination index, temperature averaged from 31.8° to 34.9C; thereafter,
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A. dorsata, having a pollination index of 12082 was found to foraging activity of honey bees declined as temperature
be the most efficient pollinator of onion crop under agro- increased and did not resume again in favourable temperature
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ecological conditions of Hisar than A. florea having in the evening. It was postulated that availability of pollen
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pollination index of 4298. A. dorsata is bigger in size and and nectar are crucial for foraging activity on a particular
has more number of body hairs than A. florea,which is smaller crop.
in size and consequently has less number of body hairs. Bee activity was found to be uniformly positively
Therefore, A. dorsata entrapped more number of onion loose and significantly correlated with the ambient temperature and
pollen grains on the body as compared to A. florea. nectar sugar concentration on all the cultivars of oilseed crops
Effect of me teorologi cal variables on foraging (Sihag and Khatkar, 1999). The correlation coefficient matrix
behavior: Each honey bee species was found to have its between bee activity and environmental factors indicated that
specific ecological threshold below which activity does foraging populations of A. dorsata, A. mellifera, A. cerana
n ot occur. Ava i l a bl e l i t er a t ur e on t h e effect of and A. florea correlated significantly and positively with air
environmental factors in influencing the foraging pattern temperature (Abrol, 2006).
of various pollinators suggests that temperature plays a In majority of the studies, foraging activity was also
key role in initiation and cessation of foraging activity. found to be significantly and positively correlated with solar
Kapil and Kumar (1974) reported 15–18 0 C as the radiation intensity (Abrol, 2006). Lerer et al. (1982) stated
minimum threshold temperature for commencement of
that though ambient temperature plays an important role in
field activities in honey bees. In a similar study, Osgood
the initiation of flight and hence in the pollination activity of
(1974) r eport ed tha t a mbi ent tempera tur e i s t he
M. rotunata, but it is the solar irradiance that appears primarily
predominant factor governing the morning flight of
responsible for controlling the pollination activity. Cessation
Megachile rotundata while cessation of activity is
of activity occurred even before the temperature dropped to
governed by light intensity. Szabo and Smith (1972)
the level required for initiation of bee activity. The correlation
reported that greatest foraging activity of M. rotundata
coefficient matrix between foraging populations of honey bees
occurred at 300C in bright sunshine and declined at higher
(A. dorsata, A. mellifera, A. cerana and A. florea) and solar
temperature in Hungary. Kapil and Brar (1971) recorded
peak activity of A. florea on toria between 21–25 0 C radiation and light intensitywas significantly and positive
(Abrol, 2006).
temperature and 50–57 per cent relative humidity during
November. In general, suitability of optimum bee activity In earlier studies, foraging activity of honey bee
varies from season to season, depending upon the species was also found to be significantly and negatively
geographical regions, time of the year, other melliferous correlated with relative humidity (Sihag and Khatkar, 1999).
crops or other species of bees. Jain and Kapil (1980) reported that the suitability of
Vol. 36 No. 1, 2015 7
atmospheric temperature coupled with relative humidity and foragers started their activity at 0845 to 0915 h on coriander
light intensity not only favoured the initiation but also led to blossom and stopped at 1600 to 1700h (Shelar and
maximum of bee activity. In the evening and relative humidity Suryanarayana, 1981).
remained favourable but cessation of bee activity occurred However, workers have highlighted the importance
due to decline in the light intensity. However, Burill and Dietz of other factors in regulating the flight activity of bees. For
(1981) found that in honey bees, foraging activity increased instance, Bellusci and Marques (2001) reported the
with increasing air temperature but was not correlated with importance of circadian activity rhythm of the foragers of a
changes in atmospheric pressure and relative humidity. eusocial bee, Scaptotrigona sp. outside the nest. In a similar
In most of the studies combination of various study, Harrison and Fewell (2002) found that environmental
meteorological parameters were found to govern the foraging and genetic influences regulate the flight metabolic rate in
pattern of pollinators. Kapil and Brar (1971) stated that a the honey bee, A. mellifera. Higher air temperatures tend to
combination of 15-18°C temperature and 80-82 percent RH increase colonial net gain rates, efficiencies and honey storage
appeared to be minimum activity peaked at a combination of rates due to lower metabolic rates during flight and in the
22-25°C temperature and 50-65 percent RH. The cessation hive. They further found that variation in flight metabolism
of activity seemed to be governed by the fast decline in light has a clear genetic basis. Different genetic strains of honey
intensity. Similar results were obtained by Cirudarescu (1971) bees often differ in flight metabolic rate, and these differences
who found that the number of insect visitors on lucerne varied in flight physiology can be correlated with foraging effort,
directly with temperature and inversely with relative humidity. suggesting a possible pathway for selection effects on flight
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Sihag (1984) gave a conclusive report that in social bees metabolism. Pereboom and Biesmeijer (2003) on the other
temperature acted as a stimulus for the commencement and hand emphasized more the importance of body size and
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cessation of pollination activity in winter whereas light did it coloration for stingless bee foragers. Devillers et al. (2004)
www.IndianJournals.com

in summer. Winter solitary bees behaved identically alike reported on modeling the flight activity of A. mellifera at the
which social bee did in winter. However, in summer solitary hive entrance.
bees, for the commencement of foraging activity, increasing Theoretical and empirical models to study foraging
temperature in the morning acted as a stimulus, whereas, behaviour: Pollinator-plant interaction has co-evolved as
cessation in the evening was affected by decreasing light reciprocal selective factors shaping the behaviour, physiology
intensity. and ecology of each other. In the course of evolution, there
Abrol (2006) studied various meteorological has been a competition between the plants for pollinators
parameters in detail in relation with foraging activity of and between the pollinators for plants (Heinrich and Raven,
pollinators. For initiation of flight activity A. dorsata required 1972). In later years, the “energetics” approach has been a
160C temperature, 74 % relative humidity, 600 lx light major focus of behavioural ecologists for studying foraging
intensity and 10 mW/cm2 solar radiation; A. mellifera required behaviour of insect visitors of flowering plants (Schmid-
160C temperature, 75 % relative humidity, 800 1x light Hempel, 1984). Heinrich and Raven (1972) emphasized the
intensity and 10 mW/cm2 solar radiation; A. cerana required role of energetics in flower foraging and in the evolution of
15.50C temperature, 76 % relative humidity, 600 1x light bee flower relationship. The food rewards from a plant species
intensity and 9 mW/cm2 solar radiation and A. florea required is the quantity of food that can be collected per unit time.
18.50C temperature, 64 % relative humidity, 1700 1x light This quantity is a function of the distance between flowers
intensity and 20 mW/cm2 solar radiation (Abrol, 2006). and the speed with which food rewards can be gathered from
Thereafter, all honey bee species continued foraging under them. Acquisition of energy rewards comes only with the
light intensity, solar radiation and temperature levels lower costs. Time and energy are spent during all foraging activities.
than conditions needed to commence foraging. However, The rate at which flowers can be manipulated makes the
cessation of foraging activity occurred even before difference between profit and loss. Flowers have different
temperatures dropped to the values required for structure that require different pattern to be learned through
commencement of field activity. trial and error for acquiring food. All this information is used
Additionally, peak of anthesis also governed the to choose between flowers of different species and to make
foraging pattern of various pollinators. The most common foraging decisions. MacArthur and Pianka (1966) developed
visitors were the honey bees (A. florea and A. dorsata) which a theoretical and empirical construct, the optimal foraging
were most active about 1100 to 1400h; the peak of anthesis theory (OFT), which lead to a better understanding of foraging
also occurred during this period (Baswana, 1984). Pollen behavior. Emlen (1966) demonstrated the need for a model
8 AGRICULTURAL REVIEWS
where food item selection of animals could be understood as In onion crop, Glukhov (1955) and Martin (1979) observed
an evolutionary construct which maximizes the net energy higher germination (97%) and emergence rate (85.5%) in
gained per unit feeding time. Optimal foraging theory open plots as compared to caged plots (85.5 and 81%). Gjorgji
(Waddington, 1982) hypothesizes animals will forage in ways and Rukie (1997) revealed that seed germination rate was
that maximized some measure of foraging efficiency. The 3.6 per cent greater in onion with honey bee activity. Hwang
“currency” (Schoener, 1971) usually thought to be maximized et al. (1998) recorded that rates of seed set were high (64.1%)
is net rate of energy intake although other possibilities exist in fly pollinated onions as compared to 62.7 and 60.8 per
(Pyke et al., 1977). Natural selection is expected to favor cent seed set in honey bee pollinated and open pollinated
efficient foraging patterns and this expectation forms the basis crop. Munavar and Muzaffar (1999) recorded 10-11 fold
of a large body of optimal foraging theory. increase in seed yield due to honey bee pollination. Yucel
Effect of mode of pollination on crop yield parameters: and Duman (2005) reported that seed yield per bulb was
Honey bees are the most important pollinators of onion crop higher in open plots (5.74 g/ flower) as compared to 1.29 g/
because the duration of pollinator visits to a flower is flower in caged plots. A. dorsata was revealed as the most
correlated positively to pollination rate, which is itself effective pollinator based on seed setting results which
correlated to the number of seeds produced, their weight and produced 506 seeds/ umbel/ 20 minute visit (Shafqat and
their seedling length.Van der Meer and van Bennekom (1968) Masood, 2008).
reported only 9 percent self-fertilization in onion crop which Effec t of honey be e pol li nation on crop yi el d
corroborated the present finding of low seed set in self parameters: Effect of honey bee pollination was studied
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pollination. In Poland, the yield of hybrid seed of plants in in comparison with other modes of pollination in various
field cages pollinated by honey bees, bumble bees (Bombus crops including onion. Hamilton (1946) found that an
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terrestris or B. ruderarius) and Megachile rotundata was onion grower produced more seed than he had in the past
www.IndianJournals.com

equivalent to 301, 295 and 47 kg/ha, respectively after he rented 8 colonies of bees. Sanduleac (1961) and
(Ruszkowski and Bilinski, 1984). In a similar study, seed set Le Baron (1962) stated that bees increase eight to ten times
(68.8%) and germination (86%) in onion seeds was better in t he producti on of on ion seed in Roma n ia , an d
open pollination as compared to self pollination (22.8, 67.5%, recommended about two colonies per acre. Jones and
respectively) (Kumar et al., 1985). They although reported Emsweller (1933) reported 157 seeds produced per bagged
higher seed set and germination in open pollination in onion head compared with 712 seeds in open pollination. The
than in caged umbels but no significant difference was increase in seed production was found to 175 (Deodikar
observed between these treatments for mean weight of 100 and Suryanarayana, 1972) to 1000 per cent (Singh and
seeds. Dharamwal, 1970) under bee pollinated area. Although
Nye et al. (1971) reported an average of 100 bees per 100
Nogueira-Couto and Calmona (1993) grew
feet of male fertile rows and a maximum of 40 per 100
cucumber plants with three different treatments, i.e., netted
feet on the male sterile rows, the number of honey bee
without honey bees, netted with honey bees and open-
visitors needed per onion plant, umbel, or linear feet of
pollinated produced. They observed that open pollinated
row has not been determined. The study conducted by
plants produced more fruits than without pollination.
Benedak and Gaal (1972) revealed that fertilization rate,
Cervancia and Bergonia (1991) found that per cent fruit set
seed yield a n d per cent a ge of ger mi n at ion wer e
of bee-pollinated and open-pollinated (uncaged) plants did
significantly better in uncaged inflorescences. Singh and
not differ significantly in Philippines, but was about twice
Dharamwal (1970) reported an increase of 72-79 per cent
that of non-pollinated plants. They further observed that fruits
in seed set in open pollinated plants over bagged plants
were heavier (0.87 kg) and more uniform than those of open-
and Jadhav (1981) recorded per cent fruit set and seed
pollinated plants (0.6 kg), while fruits from non-pollinated
number were 74.33 and 1063 in open pollination with
plants were shortest and lightest (0.36 kg). The percent fruit
set was maximum (84.29%) under bee pollination plus hand better seed germination (90.7%) as compared to 7.67 per
pollination and minimum (79.99%) under hand pollination cent fruit set and 49 seeds in bagged umbels. Ewies and
conditions. Average fruit diameter, fruit length and fruit weight El-Sahhar (1977) reported 61.8 per cent seed setting in
was maximum (3.51 cm, 13.31 cm and 135.25 g, respectively) open pollination as compared to 1.5 per cent in self
under bee pollination and bee pollination + hand pollination, pollination of onion crop. Woyke (1981) observed that
while these were observed minimum (3.49 cm, 12.19 cm and numbers and weight of onion seeds from self pollination
132.83 g, respectively) under hand pollination conditions were very low as compared with yields on open fields
(Kumar, 2004). provided with honey bee colonies.
Vol. 36 No. 1, 2015 9
The pollination by honey bee, A. cerana and by hand gave major drawback in seed production (Chandel et al., 2004).
15 and 8 per cent fruit set in bottle gourd, respectively, According to Chandel et al. (2004), induced bee pollination
whereas, isolated plants gave only 3-5 per cent fruit set in increased seed yield by 2.5 times and produced on an average
Punjab (Alam and Quadir, 1986). Kuti and Rovelo (1992) 971 seeds per umbel compared to 406 in the control. The
reported that honey bee pollination produced more fruits per seeds from induced pollination field resulted in 90 percent
plant, higher seed weight and greater seed viability than hand germination compared to 69.5 percent germination from the
pollination in melon. Under honey bee pollination, more than control.Yucel and Duman (2005) reported that seed yield per
85 per cent of flowers set fruit, compared with less than 20 bulb was higher in open plots (5.74 g/ flower) as compared
per cent for hand pollination. Brewer (1974) reported that to 1.29 g/ flower in caged plots. A. dorsata was revealed as
the weight of melons and both number and weight of mature the most effective pollinator based on seed setting results
seeds per melon were significantly higher from plots visited which produced 506 seeds/ umbel/ 20 minute visit (Shafqat
by bees than those where bees were excluded in Colorado and Masood, 2008).
(USA).Nogueira-Couto and Calmona (1993) observed that Several pollination factors are considered for
cucumber plots netted with bees yielded more fruits/m2 and agricultural production such as self-pollination, wind
heavier and higher quality fruits than other plots. The weight pollination, hand pollination, pollen dispensers, pollination
of fruits on an average was 2.73 kg per plant visited by insect through insects, birds etc. Vegetable and fruit crops depend
pollinators and 1.9 kg per plant not visited by bees indicating upon insect pollination for yield and fruit quality. Colour,
more than 30 per cent higher fruit yield by shape and odour of flowers are well-known attractants to
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pollination.Munavar and Muzaffar (1999) recorded 10-11 pollinators. Besides these physical features, the other source
fold increase in seed yield due to honey bee pollination. The of variation for differential attraction between genotypes is
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seeds from induced bee pollination showed high seed set the caloric reward viz„ nectar and pollen provided by the
www.IndianJournals.com

(Prasad et al., 2000), maximum germination (Chandel et al., flowers. Different cultivars differ in their production of pollen
2004), shoot and root length (Kalmath and Sattigi, 2004) as and bees can discriminate these varieties. Likewise, the nectar
compared to control.Onion (Allium cepa L.) does not produce provided by the flowers has been found to be a significant
quality seed if insects do not visit the flowers. In mountainous parameter that shapes the behaviour of pollinators in relation
regions of India, availability of natural pollinators has been a to their energetic needs.

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