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Cargas polinicas de Apis mellifera para entender los patrones de forrajeo de polen usados en apicultura en una franja potencialmente agricola en Bengala, India.

Apis mellifera pollen loads to understand the pollen foraging pattern used for apicultural practice in a potentially agricultural belt in Bengal, India

Pollen is the bee's major sources of proteins, amino acids, lipids, minerals and vitamins (Marchini, Reis, & Moreti, 2006). It is essential for the growth of larvae and young adult bees (Dietz, 1975; Modro, Silva, Cynthia, Luz, & Message, 2009). Rearing one worker bee from larval to adult stage requires approximately 120-145 mg of pollen (Alfonsus, 1933; Haydak, 1935). Honeybee transports pollen to the hive in specialised structures of its legs (corbicula), in which pollen moistened with nectar and hypopharyngeal and mandibular secretions, is packaged forming pasty pellets called 'pollen loads' (Thorp, 2000). The pollen composition in the pollen loads is a reflection of the local flora preferred by the workers of the bee species surrounding hives (Diaz-Losada, Ricciardelli-d'Albore, & Saa-Otero, 1998). Therefore determination of polleniferous flora in a given area is very important for development of any apiculture industry (Sajwani, Farooq, & Bryant, 2014). In West Bengal some work on polleniferous flora was done by Pal and Karmakar (2013), More, Ghorai, & Bera, 2010. Though few works on pollen analyses of A. mellifera form outside the state as well as from other countries were reported by Suryanarayana, Rao, & Singh, 1992; Noor, Khan, & Camphor, 2009; Lopez, Vives, & Boi, 2013; Saavedra-Carhuatacto, Aguinago-Castro, Rojas-Indrogo, & Delgado-Paredes, 2014 and Freitas, Sattler, Souza, Almeida-Muradian, Sattler, & Barth, 2015.

The present study aims to investigate the botanical origin of pollen loads collected in North 24 Parganas district, West Bengal to provide a guide to the optimal utilization of floral resources by honeybees for sustainable apiculture industries.


Study site: North 24 Pargana is a district in southern West Bengal of Eastern India. The district situated between (22[degrees] 11' - 23[degrees]15' N & 88[degrees]20 '- 89[degrees]5' E) with a total area of 4 094 km2. The climatic condition is tropical and experiences hot, humid and exhausting summer (mid April-mid June) with daily temperature ranging from 20 [degrees]C to 40 [degrees]C. The next season is monsoon which continued up to August, with an average annual rainfall of 1 579 mm and with high relative humidity level (RH 90 %). The cold and dry winter approach in early December and stay up to mid February with day temperature ranges from 8 to 28 [degrees]C. Major rivers flows through the district are Ganges, Ichhamati, Jamuna and Bidyadhari. The soil of the northern part of the district is sandy, in the central middle part it is sandy and clay loam and in the southern side it is clay loam. The area harbours a diversified flora with a productive agricultural output as the river Ganges flows its long course through the district.

Collection of samples: A total of 2 434 pollen loads were collected from four apiaries viz. Amdanga (634 pollen loads), Bagdaha (586 pollen loads), Barrackpur (610 pollen loads) and Haripur (604 pollen loads) located at four different areas of North 24 Parganas district, West Bengal (Fig. 1). Pollen samples were collected for 12 months (January to December) and three to four sampling days per month. 30 to 64 loads were collected for each sampling day from one apiary. Incoming pollen foragers were captured at the entrance of the hive, and the two corbicular loads were collected. Pollen loads were preserved separately in (5 mL) white glass vials containing FAA (Formalin-Aceto-Alcohol, 5:5:90) solution.

Palynological analyses: Each pollen load was analyzed separately. The pollen loads were suspended in 50 mL of 95% ethanol and thoroughly mixed (Jones & Bryant, 2004). The final suspension was then centrifuged at 4 000 rpm for 5 min. After decanting supernatant, the sediment was subjected to acetolysis (Erdtman, 1960) with a 9:1 ratio of acetic anhydride to conc. sulphuric acid. After thoroughly mixing, the mixture containing tube was placed into a water bath (at 80[degrees]C) for 3 min. Then 5 mL of glacial acetic acid was added to each sample. The samples were rinsed twice with distilled water, centrifuging and decanting each time, and then once with 95% ethyl alcohol. After centrifuging, the pellet was taken on a small piece of glycerine jelly and transferred to the centre of a glass slide. Glycerine jelly was used as a mounting medium to prepare the samples for light microscopy (Ohe, Oddo, Piana, Morlot, & Martin, 2004). Then warmed gently to melt the jelly containing pollen sediment and covered by cover glass and sealed with paraffin wax. Identification of pollen types was done (on the basis of 500 grains counted per slide) with the help of reference slides prepared from the local flora as well as from published accounts (Nayar, 1990; Layek & Karmakar, 2016). Analysis was conducted using Leica DM1000 and photomicrographs of suitable magnifications were made with Leica DFC295 Digital camera. The contents of each pollen load were designated as being unifloral (with single pollen type [greater than or equal to] 90%), bifloral (with pollen of two types, one 80-90% and other 20-10%) and multifloral (with pollen of more than two types [greater than or equal to] 10%). Month wise percentages of the pollen types were also determined. Then we classified the obtained pollen types into three groups: very frequent (> 20%), frequent (10-20 %) and less frequent (< 10%) (Layek & Karmakar, 2018).

Data Analysis: Statistical analyses of the pollen materials were done to get the arithmetic mean and standard deviation. To assess the association between different variables we followed Kearl Pearson's correlation coefficient method.


The analyzed pollen loads were designated as unifloral, bifloral and multifloral according to their pollen composition. The overall number of unifloral loads was 1 776 (72.97%), bifloral was 462 (18.98%) and multifloral was 196 (8.05%). Among the multifloral loads, the majority had three pollen types and only eight loads were with four pollen types in composition. The highest proportion of unifloral loads was recorded during April (89.8%), followed by March (86.1%), November (85.05%), January (82.30%), December (80.18%), February (79.34%), October (71.4%), September (64.89%), May (61.96%), June (53.33%), July (50.60%) and August (49.50%). The sequences were almost reverse in cases of bifloral and multifloral loads (Table 1, Fig. 2). A total of 43 pollen types belonging to 28 plant families were identified (Table 2). Month wise analysis of loads revealed highest number of pollen types during March (13 types), followed by July (11 types), February, June and August (each of them with ten types), January, April, May and September (each with 8 types), October and December (both of each with seven types), and November with 6 pollen types (Table 2). According to frequency classes very frequent (> 20%) pollen types were Brassica nigra, Phoenix sylvestris (during January); Coriandrum sativum (in February); Borassus flabellifer (during March and April); Sesamum indicum (in May); Acacia auriculiformis, Cocos nucifera (in September); Cocos nucifera, Poa gangetica (in October) and Brassica nigra during November and December. Besides the above mentioned pollen types, other frequent pollen types were Alangium salviifolium, Citrus x aurantiifolia, Citrus maxima, Croton bonplandianum, Cyanotis axillaris, Luffa cylindrica, Neolamarckia cadamba and Trema orientalis. Plants that accounted for the higher number of pollen loads were Brassica nigra (7.59%), followed by Cocos nucifera (4.57%), Poa gangetica (3.34%), Borassus flabellifer (3.20%), Sesamum indicum (3.19 %), Coriandrum sativum (3.08%), Phoenix sylvestris (2.68%), Trema orientalis (2.37%) and Acacia auriculiformis (2.16%). Plant families that accounted for a large number of loads were Arecaceae (21%), Brassicaceae (16.23 %), Poaceae (6.68%), Pedaliaceae (6.38%), Apiaceae (6.16%) and Fabaceae (5.38%). The families that represented the greater number of taxa were Asteraceae and Euphorbiaceae (each of them with 4 plant taxa); followed by Arecaceae and Cucurbitaceae (each with 3 plant taxa); each of the family viz. Brassicaceae, Fabaceae, Myrtaceae and Rutaceae represented by 2 plant taxa. The remaining 20 families represented by single plant taxon.


Major proportion of unifloral loads implies the floral fidelity behaviour of the bee species. Bifloral and multifloral loads could be due to the variety of flowering plants that were blooming simultaneously. This multifloral availability appears to divert the attention of some foraging bees (Alves & Santos 2014). Greater proportion of unifloral loads were obtained during March-April (spring-summer) and November-January (winter) derived from Borassus flabellifer and Brassica nigra, Phoenix sylvestris respectively. The importance of these plant taxa as polleniferous plant were also reported by Layek, Nandi, & Karmakar (2016) form West Bengal and Suryanarayana et al. (1992) from Bihar in India. In addition to the above mentioned taxa, other important polleniferous plants were: Acacia auriculiformis, Cocos nucifera, Coriandrum sativum, Poa gangetica, Sesamum indicum and Trema orientalis. The significance of some the above taxa as pollen contributor were also recorded in India as well as from other countries (by Noor et al., 2009; Karmakar, Layek, & Pal, 2011; Layek, Bhakat, & Karmakar, 2015). But the significance of Trema orientalis as polleniferous plant was not previously recorded by any author in West Bengal, India. The small percentage of pollen from: Bombax ceiba, Euphorbia tithymaloides, Flacourtia jangomas, Litchi chinensis, Nelumbo nucifera, Tridax procumbens indicate that these plants are either sporadic in distribution, fairly rare in abundance, do not produce sufficient amount of pollen for bee foraging, or produce pollen that is not preferred by honeybees due to low nutritional value (Dorea, Novais & Santos, 2010). Among the major pollen supplied families, Apiaceae, Pedaliaceae and Poaceae comprises of single plant taxon. On the other hand, largest represented families Asteraceae, Cucurbitaceae and Euphorbiaceae contributed moderate pollen to the bee species. Hence, the correlation between represented plant taxa of a family and their contribution as pollen supplier is low to medium (r = 0.40, n = 28).

The present study was undertaken to identify the polleniferous flora of the study area as well as floral fidelity behaviour of the bee species. Regarding pollen composition of each load, it was found that majority were unifloral type which signifies the floral fidelity behaviour of the bee species. Floral constancy level increases with the presence of excellent and huge polleniferous plants during March-April and November-January, whereas decreases during dearth period from June-August due to absence of very frequent pollen types in these regions. However, Trema orientalis play a major role to sustain the pollen flow for the bee colony during the dearth period in the studied area. The present work provides us with a considerable knowledge about plant diversity and the annual flowering pattern. By knowing the flowering pattern and the preferred plant species for pollen collection by A. mellifera, the apiculturists will get a proper knowledge regarding successful establishment of apiaries in that region.

Ethical statement: authors declare that they all agree with this publication and made significant contributions; that there is no conflict of interest of any kind; and that we followed all pertinent ethical and legal procedures and requirements. A signed document has been filed in the journal archives.


We are thankful to authorities of Vidyasagar University for providing necessary laboratory and internet facilities. We are also grateful to Apiarists for help us during collection of pollen loads of the bee species. Thanks are also due to Ujjwal Layek for helping us by preparing the tables and photo plates of the manuscript.


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Tripti Nandi & Prakash Karmakar *

Department of Botany and Forestry, Vidyasagar University, Midnapore- 721102, India;,

* Correspondence

Received 12-III-2018.

Corrected 21-VIII-2018.

Accepted 24-IX-2018.

Caption: Fig. 1. Location areas of collection of bee pollen load for analysis.

Caption: Fig. 2. Some pollen types obtained from pollen loads of Apis mellifera: A) Acacia auriculiformis; B) Borassus flabellifer; C, D) Brassica nigra; E) Chrozophora rottleri; F) Citrus x aurantiifolia; G) Cocos nucifera; H) Cucumis sativus; I) Delonix regia; J, K) Euphorbia tithymaloides; L) Luffa cylindrical; M) Monochoria hastate; N) Poa gangetica; O, P) Sesamum indicum; Q) Sida acuta; R) Syzygium cumini; S, T) Trema orientalis. Scale bars = 10 [micro]m.
Pollen loads of A. mellifera collected in North 24-Parganas,
West Bengal (India)

Months       No. of loads      Percentages of
               analyzed      different types of
                                pollen load
                            (mean [+ or -] std.


January          226         82.3 [+ or -] 4.2
February         242         79.3 [+ or -] 8.9
March            244         86.0 [+ or -] 4.3
April            216         89.4 [+ or -] 4.7
May              184         61.3 [+ or -] 7.6
June             120         53.3 [+ or -] 9.4
July             166         50.5 [+ or -] 4.2
August           202         50.1 [+ or -] 5.6
September        188         65.0 [+ or -] 4.3
October          210         71.0 [+ or -] 5.4
November         214         84.1 [+ or -] 7.8
December         222         80.4 [+ or -] 7.0

Months         Percentages of different types of pollen
                  load (mean [+ or -] std. deviation)

                   Bifloral             Multifloral

January       13.2 [+ or -] 2.7       4.4 [+ or -] 1.5
February      14.9 [+ or -] 3.4       5.8 [+ or -] 5.7
March         11.5 [+ or -] 2.1       2.4 [+ or -] 3.1
April          5.5 [+ or -] 2.1       5.0 [+ or -] 4.1
May           28.9 [+ or -] 4.9       9.8 [+ or -] 4.1
June          35.0 [+ or -] 6.4      11.6 [+ or -] 6.4
July          39.9 [+ or -] 7.1       9.5 [+ or -] 3.3
August        31.7 [+ or -] 2.9      18.1 [+ or -] 4.3
September     20.2 [+ or -] 0.4      14.8 [+ or -] 4.4
October       17.1 [+ or -] 3.4      11.9 [+ or -] 5.9
November      12.0 [+ or -] 6.5       3.9 [+ or -] 2.9
December      15.2 [+ or -] 3.7       4.3 [+ or -] 4.1

Pollen types obtained from loads of Apis mellifera in North 24
Parganas, West Bengal (India)

Pollen types
                            Jan    Feb    Mar    Apr    May    Jun
Amaranthus spinosus
Coriandrum sativum           F      VF
Borassus flabellifer                       VF     VF
Cocos nucifera               LF     LF     LF                   LF
Phoenix sylvestris           VF     F
Polianthes tuberosa
Helianthus annuus                   LF     LF
Mikania scandens             LF
Tagetes erecta               LF
Tridax procumbens                                               LF
Brassica nigra               VF     F      LF
Raphanus sativus             LF
Trema orientalis                                  LF     LF     F
Capparis zeylanica                         LF     LF
Cleome viscosa                                                  LF
Terminalia arjuna                                 LF
Cyanotis axillaris                                              LF
Alangium salviifolium                      F      LF
Cucumis sativus
Cucurbita maxima                           LF
Luffa cylindrica                           LF            LF     F
Chrozophora rottleri                                     LF     LF
Croton bonplandianum                              LF     LF     F
Euphorbia tithymaloides                                  LF
Ricinus communis
Acacia auriculiformis
Delonix regia                                     LF     LF
Bombax ceiba                               LF
Sida acuta
Moringa oleifera             LF     LF
Eucalyptus glob-ulus
Syzygium cumini                            LF
Nelumbo nucifera                                         LF
Sesamum indicum                                   F      VF
Poa gangetica
Monochoria hastata
Nigella sativa                      LF
Neolamarckia cadamba                                            LF
Citrus x aurantiifolia                                          LF
Citrus maxima                       LF     F
Flacourtia jangomas                        LF
Litchi chinensis                    LF
Holoptelea integrifolia             LF     LF
No. of pollen types          8      10     13     8      8      10

Pollen types
                            Jul    Aug    Sep    Oct    Nov    Dec
Amaranthus spinosus          LF     LF
Coriandrum sativum                                              F
Borassus flabellifer
Cocos nucifera               F      F      VF     VF            LF
Phoenix sylvestris                                              F
Polianthes tuberosa          LF     LF
Helianthus annuus
Mikania scandens                                         LF     LF
Tagetes erecta                                                  LF
Tridax procumbens
Brassica nigra                                           VF     VF
Raphanus sativus                                                LF
Trema orientalis             F      F      LF
Capparis zeylanica
Cleome viscosa               LF
Terminalia arjuna
Cyanotis axillaris           LF            LF     F      LF
Alangium salviifolium
Cucumis sativus              LF     LF     LF
Cucurbita maxima
Luffa cylindrica             LF     LF     LF
Chrozophora rottleri
Croton bonplandianum
Euphorbia tithymaloides
Ricinus communis                           LF     LF
Acacia auriculiformis        LF     LF     VF     LF
Delonix regia
Bombax ceiba
Sida acuta                                        LF     LF
Moringa oleifera
Eucalyptus glob-ulus                              LF     LF     LF
Syzygium cumini
Nelumbo nucifera
Sesamum indicum
Poa gangetica                       F      LF     VF     F
Monochoria hastata                  LF
Nigella sativa
Neolamarckia cadamba         F      LF
Citrus x aurantiifolia       F
Citrus maxima
Flacourtia jangomas
Litchi chinensis
Holoptelea integrifolia
No. of pollen types          11     10     8      7      6      8

                             No. of loads
Pollen types

Amaranthaceae                      7
Amaranthus spinosus                7
Apiaceae                          75
Coriandrum sativum                75
Arecaceae                       254.49
Borassus flabellifer              78
Cocos nucifera                  111.32
Phoenix sylvestris               65.17
Asparagaceae                     11.50
Polianthes tuberosa              11.50
Asteraceae                       36.83
Helianthus annuus                  8
Mikania scandens                 16.33
Tagetes erecta                     8
Tridax procumbens                4.50
Brassicaceae                    197.50
Brassica nigra                  184.67
Raphanus sativus                 12.83
Cannabaceae                      57.67
Trema orientalis                 57.67
Capparaceae                       11
Capparis zeylanica                11
Cleomaceae                       7.33
Cleome viscosa                   7.33
Combretaceae                      10
Terminalia arjuna                 10
Commelinaceae                    17.67
Cyanotis axillaris               17.67
Cornaceae                        27.67
Alangium salviifolium            27.67
Cucurbitaceae                    61.67
Cucumis sativus                   21
Cucurbita maxima                 5.50
Luffa cylindrica                 35.17
Euphorbiaceae                    45.17
Chrozophora rottleri             9.17
Croton bonplandianum              22
Euphorbia tithymaloides            2
Ricinus communis                  12
Fabaceae                         65.50
Acacia auriculiformis            52.50
Delonix regia                     13
Malvaceae                        10.17
Bombax ceiba                     3.17
Sida acuta                         7
Moringaceae                      6.33
Moringa oleifera                 6.33
Myrtaceae                        28.83
Eucalyptus glob-ulus             22.83
Syzygium cumini                    6
Nelumbonaceae                    2.50
Nelumbo nucifera                 2.50
Pedaliaceae                      77.67
Sesamum indicum                  77.67
Poaceae                          81.33
Poa gangetica                    81.33
Pontederiaceae                   7.67
Monochoria hastata               7.67
Ranunculaceae                    8.33
Nigella sativa                   8.33
Rubiaceae                        21.84
Neolamarckia cadamba             21.84
Rutaceae                         32.17
Citrus x aurantiifolia            11
Citrus maxima                    21.17
Salicaceae                         5
Flacourtia jangomas                5
Sapindaceae                      1.50
Litchi chinensis                 1.50
Ulmaceae                         18.50
Holoptelea integrifolia          18.50
No. of pollen types

VF: very frequent, F: frequent, LF: less frequent.
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Author:Nandi, Tripti; Karmakar, Prakash
Publication:Revista de Biologia Tropical
Date:Dec 1, 2018
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