THE PRESENTATION OF POLLEN IN CERTAIN ANGIO- SPERMS AND ITS COLLECTION BY APIS MELLIFERA

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1 [ 353 ] THE PRESENTATION OF POLLEN IN CERTAIN ANGIO- SPERMS AND ITS COLLECTION BY APIS MELLIFERA BY M. S. PERCIVAL Univei'sity College, Cardiff {Received ii January 955) (With I figure in the text) INTRODUCTION While investigating the pollen income of a hive of honey bees {Apis mellifera) it was found that some pollen types were collected in abundance, while others were collected rarely or not at all. Moreover, different pollens were collected at different times of the day, and the peak periods in the collection from different species varied strikingly. The first evidence that pollen production and pollen collection were connected was advanced by Synge (947). The present work is a continuation of the author's previous studies (Percival, 950, 95). Methods. A small number of plants or, in the case of trees and shrubs, branches was selected. Fvery ffower opening thereon was observed, so that each day a population of flowers in all stages of anthesis was available for examination. The plants were observed throughout the whole, or major part, of their flowering, if this was possible. In some cases the observations were continued in successive seasons. The species usually revealed its rhythm of pollen presentation within a couple of days, but the observations were continued to obtain information on the effect of weather conditions upon it. The unit observed was the 'flower form', whether inflorescence or single flower, but the distinction broke down occasionally, e.g. the inflorescence of Prunus laurocerasus might be taken as the flower form, but observations were also made on the separate flowers. Counts of stamens presenting pollen were taken at hourly intervals if possible. Certain crops (e.g. the Legumes) present their pollen in the bud, so the number of flowers reaching a stage of opening at which the bee could exploit them was noted instead. The opening and closing of the flowers was noted if it occurred within the period of foraging. The data of pollen collection by the bees was taken at the hive or on the crops. All the crops grew near the hives, so any effect of distance on collection could be discounted. Temperature and relative humidity were measured by means of a whirling hygrometer. Periods of sun, rain or overcast were recorded, but air movement was not. Time of presentation of pollen. Most of the species so far studied produce pollen throughout the period 7 a.m.-5 p.m., but the peak period of pollen presentation differs widely (Table i). The longest period of presentation is seen in Helleborus abchasicus, where it is continuous day and night. Aesculus hippocastanum, Pyriis communis, Prunus laurocerasus and 24 New Phyt. 54, 3

2 354 M. S. PERCIVAL Table i. Daily period of pollen presentation, based on observations of numbers of dehisced stamens at hourly intervals Duration of pollen presentation Peak period Percentage of day's pollen presented in peak period (a) ' Early morning' crops: Calystegia sylvestris Papaver dubiitm Hypericum perforatum Ligustrum vidgare Fuchsia magellanica Convolvulus minor Sarothamnus scoparius Sinapis arvensis Rosa spinosissima Centaurea montana Tradescantia virginica Sonchus oleraceus Helianthenmm chamaecistus Raphanus raphanistrum Aucuba japonica Clematis vitalba Cirsimn palitstre Ribes sanguineum Layia elegans Helianthus annuus Plantago lanceolata Brassica oleracea (6) ' Chiefly morning' crops: Buddleia variabilis Deutzia gracilis Crocosmia pottsii Sambucus nigra Epilobium montanum Ranunculus bulbosus R. repens Taraxacum offidnale Zea mays Anemone apennina A. nemorosa Ranunculus ficaria Epilobium adenocauton E. parviflorum Fragaria x ananassa Senecio jacobaea Epilobium parviflorum X E. adenocaulon Eschscholzia californica Cardamine pratensis Limnanthes douglasii Kentranthus ruber Petroselinum crispum Ilex aquifolium Aubrieta deltoidea Ulex gallii U. europaeus Cheiranthus x allionii Ribes nigrum Prunus cerasus Impatiens roylei Epilobium hirsutum Berberis darzvinii Aesculus hippocastanum (c) ' Midday' crops: Alisma plantago-aquatica Arctium vulgare Crocus aureus 5-7 a.m. 5-IO a.m. 6 a.m.6 p.nn. 6 a.m.5 p.m. 6 a.m.-6 p.m. 6-IO a.m. 7 a.m.s p.m. 8 a.m.-6 p.m. 8 a.m.i p.m. 8 a.m.-2 p.m. 6 a.m.-5 p.m. 7 a.m.2 n. 5 a.m.i p.m. 8 a.m.s p.m. 8 a.m.5 p.m. 6 a.m.s p.m. 8 a.m.3 p.m. 9 a.m.-5 p.m. 8 a.m.2 p.m. 7 a.m.-6 p.m. 4 a.m.-5 p.m. 7 a.m.5 p.m. 7 a.m.-5 p.m. 9 a.m.-4 p.m. 8 a.m.3 p.m. 8 a.m.5 p.m. 8 a.m.4 p.m. 8 a.m.-5 p.m. 8 a.m.5 p.m. 9 a.m.-3 p.m. 7 a.m.6 p.m. 9 a.m.4 p.m. 0 a.m.4 p.m. 9 a,m.-3 p.m. 0 a.m.-3 p.m. 9 a.m.4 p.m. 9 a.m.5 p.m. 8 a.m.-s p.m. 9 a.m.4 p.m. 9 a.m.4 p.m. 9 a.m.-5 p.m. 8 a.m.-s pm- 7 a.m.-s p.m. 8 a.m.-5 p.m. 9 a.m.-6 p.m. 9 a.m.-5 p.m. 7 a.m.-s P-m. 8 a.m.-s p.m. 7 a.m.-s P-m- 8 a.m.-s p.m. 8 a.m.-s P-m. 8 a.m.4 p.m. 6 a.m.-4 p.m. 8 a.m.-s p.m. S a.m.-6 p.m. 0 a.m.-i p.m. 0 a.m.-3 p.m. II a.m.-4 p.m. 6 a.m. 6 a.m. 6 a.m. 6-8 a.m. 6 a.m. 7-8 a.m. 7 a.m. 8 a.m. 8 a.m. 8 a.m. 8 a.m. 89 a.m. 8 a.m. 8 a.m. 8 a.m. 80 a.m. 8-9 a.m. 9 a.m. 9 a.m. 90 a.m. 70 a.m. 70 a.m. 8- a.m. 9 a.m. 90 a.m. 90 a.m. 9-0 a.m. 90 a.m. 0 am. 0II a.m. io-ii a.m. II a.m.-i2 n. II a.m.2 n. II a.m.-i2 n. II a.m.-i2 n. II a.m.-i2 n. a.m.2 n. 0 a.m.-i2 n. 9 a.m.-i2 n. 9 a.m.-i2 n. 9 a.m.-2 p.m. 9 a.m.-2 p.m. 9 a.m.-2 p.m. 9 a.m.-i2 n. 9 a.m.-i2 n. 9 a.m.-2 n. 8 a.m.-i2 n. 8 a.m.-i2 n. 8 a.m.-2 n. 8 a.m.-i2 n. 8 a.m.-i2 n. 8 a.m.-i2 n. 8 a.m.-i2 n. 8 a.m.2 n. S a.m. II a.m.2 n. 2 n.-2 p.m. 2 n.-2 p.m O i-3 6s-o 6o-o S S-9 5II 49-7 S4-O S I-I 77"3 79"3 6s-i l '4 68-6

3 Collection of pollen by Apis mellifera Table i {cont.) 355 Duration of pollen Ipresentation Peak period Percentage of day's pollen presented in peak period 'All-day' crops: Endymion non-scriptus Scilla sibirica Allium ursinum Rubus idaeus R. fruticosus R. loganobaccus Prunus laurocerasus Crataegus monogyna Arabis albida Lunaria annua Cheiranthus cheiri Leiicojum aestivum Allium porrum Magnolia stellata Reseda odorata Tropaeolum majus Bartonia aurea Digitalis purpurea Phacelia tanacetifolia a.m.-5 p.m. a.m.s p.m. a.m.-s p.m. a.m.-6 p.m. a.m.6 p.m. a.m.-s p.m. a.m.-6 p.m. a.m.s p.m. a.m.-s P-m. a.m.-s p.m. a.m.-s P-m. a.m.-6 p.m. a.m.s p.m. a.m.-s p.m. a.m.-s Pm. a.m.-7 p.m. a.m.-s p.m. a.m.s p.m. a.m.-6 p.m. II a.m.-2 p.m. II a.m.-2 p.m. II a.m.2 p.m.. So-o (e) (J) 'Chiefly afternoon' crops: Prunus persica Pyrus malus P. communis Tussilago farfara Aquilegia x hybrida Scilla hispanica 'Afternoon' crops: Magnolia x soulangeana Vicia faba ' Night' crop: Cucurbita pepo 9 a.m.s p.m. 8 a.m.5 p.m. 7 a.m.-6 p.m. IO a.m.s p.m. S a.m.-7 p.m. 8 a.m.-6 p.m. 8 IO a.m.6 p.m. a.m.s p.m. 2 n.4 p.m. 2 n.4 p.m. -2 p.m. -4 p.m. 2 n.-3 p.m. 0 p.m.-3 a.m ' Day and night' crop: Helleborus abchasicus 2 n.-4 p.m. 5-7 Fuchsia magellanica may share this feature, since the first readings, recorded in the morning for these four species, are high compared with the small values in the next -2 hr., suggesting that presentation has occurred during the night. Another species with a long period of presentation is Plantago lanceolata, which is 4 a.m.-5 p.m. The shortest period of presentation is that of Alisma plantago-aquatica which is at most 4 hr. Papaver dubium. Convolvulus minor, Arctium vulgare. Crocus aureus, Sinapis arvensis, Rosa spinosissima and Sonchus oleraceus follow closely with 5-6 hr. periods. On any one day, in any one crop, the period of anthesis may be much shorter. The whole crop of Alisma plantago-aquatica may present its pollen in 30 min., and individual inflorescences of Sonchus oleraceus and Taraxacum ojficinale may present all their day's quota of pollen within 0 min. An attempt has been made to grade the species according to the particular features of their times of presentation. ' Early morning' crops. First, there is a group of species which present the bulk of their pollen before 9 a.m. (50-00%). These have been named 'Early morning' crops. Within 24-2

4 356 M. S. PERCIVAL this group, marked differences occur in the time of the peak period of presentation, so they are further arranged as to the hour at which this occurs. ' Chiefly morning' crops. The second group may be called ' chiefly morning' crops, where % of the pollen is presented by noon. This group may be divided into subgroups showing high production over 2, 3, 4 or 5 hr. periods during the morning. Senecio jacobaea shows two peaks, one at 0 a.m. and another at noon; this is a result of two successive batches of florets presenting pollen. Aesculus hippocastanum shows a level rate of production of about 6% per hour from 6 a.m. to 7 p.m., but may still be included in this class as 63 % of its total pollen is presented by noon. 'Midday' crops. The third group may be called 'midday' crops. Only three species are as yet listed here. 'All day' crops. The fourth group may be called ' all day' crops, since pollen production is almost evenly divided between the forenoon and afternoon (44-58 % is presented up to noon). Three of these species show a well-marked peak of production from a.m. to 2 p.m. These are all monocotyledons, Endymion non-scriptus, S. sibirica and Allium ursinum. 'Chiefly afternoon' crops. The next group is the 'chiefly afternoon' one, where only 35-40% of the pollen is produced up to midday. Three rosaceous plants may be placed here, Prunus persica, Pyrus malus and P. communis. Aquilegia x hybrida, Tussilago farfara and Scilla hispanica complete the group. Helleborus abchasicus may be added as it produces 52 % of its pollen from noon to 4 p.m. (but see below). 'Afternoon' crops. Only two species observed so far can be classed as ' afternoon' crops. These are Magnolia x soulangeatia and Viciafaba, which present 84-9 and 75 % of their pollen respectively after noon. 'Night' crops and 'all day and night' crops. Two groups only remain. Each contains a single species. A 'night' crop of pollen is produced by the male flowers of Cucurbita pepo between 0 p.m. and 3 a.m. and an 'all day and night' crop is produced by Helleborus abchasicus. Taxonomic groups and pollen presentation. It was thought that individual families or genera might show similarities in the time of pollen presentation, but none could be demonstrated with the present scanty data. DURATION OF ANTHER DEHISCENCE The duration of anther dehiscence in each flower form ranges from 26 days in Helleborus abchasicus to a simultaneous dehiscence of all the anthers in Alisma plantago-aquatica, Curcurbita pepo etc. (Table 2). Of the eighty-one species, 28-4% had simultaneous dehiscence of anthers, 7-4% dehisced in the bud, 6-i % within -4 hr., and in four more species 70-77% of the flowers completed dehiscence on the flrst day of anthesis. So 56-8 % of the species have flowers which present their pollen during one foraging period. Fifteen species, = 8-5 % (marked with asterisk), have a majority of flowers completing dehiscence in two foraging periods. Hereafter the groups are small and vary in content. With the exception of the Leguminosae, which are all in the same group (dehiscence in bud), and the Ranunculaceae in the longest time groups, there are seemingly no phyletic links amongst the species comprising the others.

5 Collection of pollen by Apis mellifera 357 All the Ranunculaceae so far examined, except Aquilegia, have long periods of anthesis. These are from 2-8 days in Ranunculus ficaria to 8-26 days in Helleborus abchasicus. The anemones have a surprisingly long period of 7-4 days and rank next to Helleborus. The Compositae vary: Senecio jacobaea (4-7 days), Centaiirea montana (4-0 days) and Helianthus annuus (6-3 days) come in the groups of longest duration with the buttercups. It is interesting that' flowers' with a long period of anthesis are found at both ends of lines of floral evolution. Sonchus oleraceus, Arctium vulgare and Cirsium palustre have shorter periods of anthesis, the majority of inflorescences completing within 2-3 days (00% in Arctium and Sonchus, 88% in Cirsium). Table 2. Duration of pollen-presentation in a single flower or '' flower form' {a) All anthers dehisce before the flower opens: Ulex europaeus, U. gallii, Sarothamnus scoparius, Vicia faba, Rhododendron ponticum and Buddleia variabilis. (b) All anthers dehisce simultaneously: Berberis darwinii, Papaver dubium, Bartonia aurea, Brassica oleracea, Impatiens roylei. Ilex aquifolium, Rosa spinosissima, Ribes nigrum, R. sanguineiim, Epilobium parviflorum, Aucuba japonica, Cucurbita pepo, Ligustrum vulgare. Convolvulus minor, Calystegia sylvestris, Plantago lanceolata (single flower), Phacelia tanacetifolia, Kentranthus ruher, Alisma plantago-aquatica, Tradescantia virginica, Galanthus nivalis. Crocus aureus and Zea mays (single flower). (c) Anthers all dehisce within a few hours: Sinapis arve>uis (-2 hr.), Raphanus raphanistrum (2 hr.), Arabis albida (2 hr.), Cheiranthus x allionii (2 hr.) and Cheiranthus cheiri (in bud or 3-4 hr.). (d) Anthers dehisce over a period of one to several days: -2 days: Crocosmia pottsii (77 % in i hr.), *Epilobium hirsutum, Hypericum perforatum (70 % in i day), *Lininanthes douglasii, *Prumis cerasus. 3 days: Auhrieta deltoidea (70 % in i day), *Fuchsia 77iageUa?iica, *Fragaria x ananassa, *Sonchus oleraceus, *Scilla hispanica, *Aesculus hippocastanum, *Digitalis purpurea, * Allium ursinum. 23 days: * Arctium vulgare. -4 days: * Prunus laurocerasus, *Cardamine pratensis, *Deutzia gracilis, *Rubus fruticosus, Scilla sibirica, Endymion non-scriptus. Magnolia X soulangeana. -$ days: Cirsium palustre, Crataegus monogyna, Prunus persica, Pyrus malus. 2-s days: Magnolia stellata. -6 days: Rubus loganobaccus, Aquilegia x hybrida, Tropaeolum majus. Taraxacum officinale.7 days: Eschscholzia California. 27 days: Pyrus communis. 8 days: Leiicojum aestivum. 2-8 days: Ra?mnculus ficaria. 2-9 days: Rubus idaeus. 3-8 days: Reseda odorata (single flower). 3-9 days: Clematis vitalba. 47 days: Ranunculus bulbosus, Senecio jacobaea. 4-9 days: Ranunculus repens. s~9 days: Sambucus nigra. 4-0 days: Centaurea montana. 6-3 days: Helianthus annuus. 7- days: Anemone nemorosa. 84 days: Anemone apennina. 82 days: Helleborus abchasicus. The rosaceous species, with the exception of Rosa and Fragaria, often have a single stamen which lags behind the others in dehiscence for one to several days. This lengthens the overall duration of anthesis, and if we exclude these we find the period considerably reduced, e.g. Pyrus communis has a range of duration from 2 to 9 days, but 82 % of the flowers complete in 2-4 days. Two very dissimilar behaviours are seen in the Papaveraceae. In Papaver dubium the stamens dehisce simultaneously, yet in Fschscholzia californica the period of anthesis may be -7 days (69 % complete in 3-4 days). Duration of anthesis in individual stamens The time taken to complete pollen presentation in individual stamens also varies. In the anthers of Zea mays it appears to be momentary, while it may take 5 hr. for the dehiscence slit of the slowly backward-curving anther to proceed from the tip to the base in Fndymion non-scriptus. The longest time for complete presentation so far observed is that of Impatiens roylei, where it may take 2-3 days for the pollen to be fully released from the anther.

6 358 M. S. PERCIVAL THE AMOUNT OF POLLEN PER FLOWER-FORM AND COLLECTION BY APIS In a previous paper on pollen collection by Apis (Percival, 947) it was inferred from the data that if the crop grew near the hive and produced a fair amount of pollen per flower form it would be worked by the bees. This view requires modifying considerably in the light of the new data now presented. There are other factors which have to be taken into consideration. One is the need of the colonies for pollen, e.g. in the early spring pollen is in great demand. Another is the rhythm of the colony life throughout the season, e.g. in June and July the emphasis is on nectar-gathering. Yet another is the biological value of the pollen for the bee. Taking the last factor first. Maurizio (95) has shown that certain pollens are of particular biological value to the bees, in that they stimulate the development of brood food glands, ovaries and the fat body, and also prolong the length of life. These include Crocus albiflorus, Papapaver spp., Plantago spp., Pyrus and Trifolium spp., and Zea mays. Ranunculus pollen, however, substantially reduced the length of life of caged bees. It may be that the foragers may exercise a choice which is not dependent on the amount of pollen present, but on its biological potency. Crocus, Pyrus malus and P. communis produce -87, 0-83 and mg. of pollen per flower per day. All are assiduously worked in this district, but it must be remembered that all three flower at a time of pollen shortage. Plantago, Zea and Papaver are also difficult to assess, for all of them produce relatively large amounts of pollen (6-6-i6-o mg. per day). A supply of Ranunculus pollen alone is unable fully to supply the needs of caged bees. This makes a comparison between R.ficaria, R. bulbosus and R. repens and Pyrus pollens interesting, if each of the buttercups is similar in nature. R. ficaria blooms at a time of pollen shortage and is well worked although it produces only 0*38 mg. of pollen per day. R. bulbosus, producing 0-77 mg. of pollen per flower per day, usually begins to flower 3 weeks earlier than R. repens, and was well worked in 945 when apple blossom was scarce in the neighbourhood. Pollen collection from R. repens (producing 0-57 mg. of pollen) has very seldom been seen even when sheltered garden plants flowered as early as R. bulbosus; this, however, was an early year for apple, which began to flower on 4 April. It would seem then that Ranunculus pollen is not collected unless there is a shortage of the biologically potent Pyrus pollen, although R. bulbosus at least supplies roughly the same amount of pollen per flower as Pyrus malus (0-83 mg.) and is more abundant in this neighbourhood. The amount of pollen produced per flower form is given in Table 3. The total amount, as well as the amount available each day, is given. The latter should be of greater significance for the forager than the former. The presence or availability of the nectar is given in column 3, and column 4 indicates the pollen collection by Apis. The range in the amounts of pollen produced per flower form per day is from 54-7 mg. in Cucurbita pepo to g- i^ Sonchus oleraceus. An inspection of the list shows that there is no simple connexion between the amount of pollen available and its collection by bees. For example, Helianthus annuus pollen, yielded at a rate of 26-6 mg. per day per inflorescence, is seldom collected, whilst that of Alisma plantago-aquatica, yielded at the rate of o-o6 mg. per flower, is collected in abundance. Of the plants yielding 3-4 mg. or more per 'flower', 38-5 % are seldom visited by bees for pollen while only 8-5 % of those producing between 2-35 and i mg. are unpopular.

7 Collection of pollen by Apis mellifera 359 Table 3. Amount of pollen produced per ' flower-form' Species Total amount in mg. Amount per day in mg. Nectar available or present Pollen collection by Apis Zea mays Allium porrum Helianthus annuus Cucurbita pepo Sambucus nigra Centaurea montana Helleborus abchasicus Eschscholzia californica Magnolia x soulangeana Tropaeolum majus Calystegia sylvestris Aquilegia x hybrida Papaver dubium Petroselinum crispum Impatiens roylei Digitalis purpurea Bartonia aurea Taraxacum officinale Rubus loganobaccus Buddleia variabilis Arctium vulgare Ranunculus bulbosus Cirsium palustre Rosa spinosissima Ranunculus repens Anemone apennina Rhododendron ponticum Anemone nemorosa Scilla sibirica Cheiranthus cheiri Senecio jacobaea Tussilago farfara Ranunculus ficaria Crocus aureus Pyrus malus Scilla hispanica Endymion non-scriptus Rubus fruticosus Convolvulus minor Lunaria annua Pyrus communis (Marie Louise) Fragaria x ananassa Sarothamnus scoparius Cheiranthus x allionii Rubus idaeus Clematis vitalba Plantago lanceolata Crocosmia pottsii Tradescantia virginica Brassica oleracea Aesculus hippocastanum Magnolia stellata Galanthus nivalis Fuchsia magellanica Crataegus monogyna Prunus persica Raphanus raphanistrum Limnanthes douglasii Vicia faba Ulex europaeus Prunus laurocerasus so-o 28-0 i6-s S'4 5'2 5' 4' ? i'4-3 i' l-i I-I (pe'rfl.) i-i i-o i'o-o-7 i-o i-o SO-O I-o 3' O" " O i-i 2-4 O-5 O i-i -3-3 O O-2 O-2? I-I I-O O-9 O (illegitimate) -t- or - or -t- -I- 4- (i only) t- -H -4-

8 36o M. S. PERCIVAL Table 3 [cont.) Species Total amount in mg. Amount per day in mg. Nectar available or present Pollen collection by Apis Reseda odorata Leucojum aestivum Sinapis arvensis Aubrieta deltoidea Berberis darzvinii Arabis albida Hypericum perforatum Alliiim ursinum Ligustrum vidgare Ribes sanguineum Ilex aquifolium Prunus cerasus Ule.x gallii Cardamine pratensis Phacelia tanacetifolia Deutzia gracilis Aucuba japonica Ribes nigrum Epilobium parviflorum Kentratithus ruber Alisma plantago aquatica Sonchus oleraceus E. adenocaulon ) E. parviflorum x adenocaulon E. montanum ] O'S -s o-s 3 O'3 O-I O-I o-oi no samples O-I O-I O'S O"S? O'3 O-I O-I O-I o-oos? 4- -H and only 20 % of those producing between 0- and mg- So one must look for another explanation than quantity alone to account for the popularity of certain pollens. The plants were therefore classified as follows: () Pollen freely collected, nectar available in flower. (2) Pollen freely collected, no nectar in flower. (3) Pollen seldom collected, nectar available. (4) Pollen seldom collected, nectar doubtfully available or absent. (5) Pollen not collected, nectar available. (6) Pollen not collected, no nectar. (i) Pollen freely available, nectar available Exactly 50-0 % of the species fall into this group (Table 3). The amounts of pollen range from 7-0 mg. in Sambucus nigra to 0-06 mg. in Alisma platitago-aquatica. It would seem that the amount of pollen available per flower form is quite unimportant if nectar is also available. (2) Pollen freely collected, no nectar available Fourteen (6-7%) of the species fall in this group. Plantago lanceolata and Rosa spinosissimaflowerin the 'June gap' (a period at about the first week in June, when the fruit blossom is over and the clover has not yet come into bloom) and Clematis vitalba and Ulexgallu flower m early autumn. They yield from 3-6 mg. {Rosa) to mg. {Clematis) per flower per day. Even this last small amount appears to be an economic proposition for the bees in August and September, but it must be remembered that C. vitalba is an

9 Collection of pollen by Apis mellifera 36 Table 4. Weather conditions and pollen presentation Species Magnolia stellata Magnolia x soulangeana Helleborus abchasicus Anemone nemorosa A. apennina Clematis vitalba Ranunculus repens R. bulbosus R. ficaria Aquilegia x hybrida Berberis darwinii Papaver dubium Eschscholzia californica Bartonia aurea Brassica oleracea Sinapis arvensis Raphanus raphanistrum Lunaria annua Cardamine pratensis Arabis albida Aubrieta deltoidea Cheiranthus cheiri Cheiranthus x allionii Reseda odorata Hypericum perforatum Limnanthes douglasii Tropaeolum majus Impatiens roylei Aesculus hippocastanum Ilex aquifotium Ulex europaeus U. gallii Sarothamnus scoparius Vicia faba Rubus idaeus R. loganobaccus Rubus fruticosus Fragaria x ananassa Rosa spinosissima Prunus persica P. cerasus P. laurocerasus Crataegus monogyna Pyrus communis P. malus Deutzia gracilis Ribes nigrum R. sanguineum Epilobium hirsutian E. parvifiorum E. montanum F. adenocaulon E. parvifiorum x adenocaulon Fuchsia magellanica Highest R.H. recorded for anthesis (%) (flower opening) Lowest* or limiting temperature CC.) Below 0 Below -2 7* 6-2* Below 6 7* 5-2* 8* 5 (in sun) 2-7 (without sun) (without sun) Temperatures at which free anthesis occurs (daily averages in C.) io (if sunny) Flower opening Rain limiting snthcsis UiX J.. X X V^ Ji.J or flower opening ( or -) ^ ^ 4 -I- _ 4- -)- -l- -)- _ 4- _ p Flower [ opening j or or or -

10 362 M. S. PERCIVAL Table 4 {cont.) Species Aucuba japonica Petroselinum crispum Rhododendron ponticum Buddleia variabilis Ligustrum vulgare Convolvulus minor Calystegia sylvestris Digitalis purpurea Plantago lanceolata Phacelia tanacetifolia Sambucus nigra Kentranthus ruber Helianthus annuus Senecio jacobaea Tussilago farfara Highest R H recorded for anthesis (%) Lowest* or limiting temperature ( C.) (without Temperatures at which free anthesis occurs (daily averages in C.) Rain limiting anthesis or flower opening ( or -) or - or -f- or - -f- or - Arctium vulgare Cirsium palustre Centaurea montana Sonchus oleraceus Taraxacum ojficinale Alisma plantago-aquatica Tradescantia virginica Scilla sibirica S. hispanica Endymion non-scriptus Allium ursinum A. porrum Leucojum aestivum Galanthus nivalis Crocus aureus Crocosmia pottsii Zea mays Below (without sun) Below 4-7 if sunny 8-s if dull Below 0 7 (without sun) IS i4-3-2i-s i S (with sun) (S with sun) (9-4 without sun) (4 with sun) (9 without sun) (Flower opening) abundant crop in this district and this may influence the foragers. Three species flower at times of plenty, both with regard to nectar and pollen. Zea mays and Papaver dubium both produce abundant pollen (6 and 6-6 mg. per day respectively), and both have the particular biological value mentioned earlier, so we can explain their attraction for the bees on these grounds. It must be stated, however, that Zea is not so frequently visited as one would expect, nor is Plantago lanceolata, except, in the latter case, actually during the June Gap. Tropaeolum majus produces 0-9 mg. of pollen per flower per day. This is a relatively large amount and the crop is unfailingly popular as a pollen source. (3) Pollen seldom collected, nectar available Six species come in this category, and they appear to be potentially good pollen producers, so that no explanation can be offered to account for their relative unpopularity in

11 Collection of pollen by Apis mellifera 363 this district, except that they were but scantily represented. Hodges (952) lists Allium porrum as a pollen source. Cucurbita pepo was well worked in 945, but bees have been seen to clean themselves of the large grains which cover them after their visit. (4) Pollen seldom collected, nectar doubtfully available or absent Thirteen species (5-0%) are included in this group. The amount of pollen produced per flower per day ranges from 54-7 to o-i mg. The four species with no nectar are Magnolia stellata, Bartonia aurea, Eschscholzia californica and Tradescantia virginica which produce 7, 5-2, 2-9 and i-o mg. of pollen respectively. Magnolia stellatavith 7 mg. per day seems near the limit for economic collection of pollen by Apis, because it is soon abandoned, even though it flowers in early spring. The other three flowered at the time of the main nectar flow of clover and blackberry, and were almost entirely neglected despite the large amounts of pollen offered. Eschscholzia and Tradescantia are known to be well worked in other situations but apparently cannot compete with the major nectar and pollen crops. Amongst the remaining species, only Leucojum shows a low level of production of o- mg. of pollen per flower per day and the presence of nectar has not been observed. This amount, without nectar, would appear to be too low to hold the foragers. Eight of the remaining species, Kentranthus ruber, Lunaria annua. Convolvulus minor, Helianthus annuus, Crocosmia pottsii, Aquilegia x hybrida, Helleborus abchasicus and Digitalis purpurea all have deep-seated nectar. The bees attempt to work all of them for nectar, but failing, or partly failing, in their attempt, seldom turn their attention to collecting the pollen despite its abundance. Why this is so cannot be explained except on the grounds that these species flower at a time when the emphasis is on nectar gathering in the colonies. The neglect of Lunaria annua is likely to be a result of competition with the wallflower which yields twice as much easily available pollen. In Lunaria the anthers are pressed face to face and at flrst are mostly hidden within the corolla tube. Helleborus abchasicus produces i mg. of pollen per flower per day, at a time of pollen shortage, which should make it an adequate source; more data of bee visits are required. (5) Pollen not collected, nectar available There are five species in this group; Sonchus oleraceus. Ranunculus repens, Cheiranthus y. allionii, Senecio jacobaea and Fuchsia magellanica producing respectively 0-005, '57> 2-4, and 4 mg. of pollen per flower form per day. Sonchus oleraceus has virtually no pollen so that permits an obvious explanation. Ranunculus repens has been considered earlier. The last three species produce pollen at a level far above the minimum of free collection by the bees if nectar is available. Cheiranthus x allionii is well worked in some seasons. No explanation can be ofl^ered for the failure of the bees to collect the pollen of the other two species. (6) Pollen not collected, nectar absent Only one species came in this group, Hypericum perforatum, which yields 9 mg. of pollen per flower per day. Here the failure of the honey bee to collect pollen was probably due to strong competition from humble-bee workers, who whipped ofl the pollen early in the morning. Potentially this species should be a good source of pollen, for its yield per flower is even higher than Rosa spinosissima (6 mg.).

12 364 M. S. PERCIVAL WEATHER CONDITIONS AND POLLEN PRESENTATION The data for the species under observation are summarized in Table 4. The temperature ranges given for anther dehiscence are only those which were obtained at the time of the observations. This is true for the other factors. Limiting factors were seldom experienced, but one which is always effective is the presence of'free' water on the anther. In no case was an anther observed to dehisce if it was actually wet, although the filament might be bathed in water for half its length {Alliiim ursinum), without affecting anthesis. Relative humidity. A 00 % R.H. (as measured by a whirling hygrometer) did not prove to be limiting for anthesis in twenty-one species (26-8 %). Fourteen of these have exposed anthers. Twenty-three species (29 %) presented pollen between 95 and 99 % R.H. and twenty-one (25 %) between 90 and 94 %. It may be that all will present pollen in virtually saturated air, if this condition obtains without precipitation. Rain. Twenty-nine species (35 %) presented pollen during rain. The protection afforded by the position of the flower head or foliage is only partial in twelve, e.g. Berbetis darwinii, Cheiranthus cheiri and Cheiranthus x aluonii, Helianthus ajinus, Rubus idaeus, Ribes nigrum, etc. On the other hand, the corolla form in Impatiens roylei. Digitalis ptirpurea and Crocosmia pottsii (narrow corolla variety) afford complete protection and dehiscence proceeds normally if the temperature remains fairly high. Light intensity. A high light intensity accelerates the opening of Taraxacum, Tussilago, Sonchiis and the anemones, but these will open, although more slowly, in dull weather. No critical observations were taken. Temperature. The primary condition for pollen presentation would seem to be the complete maturity of the anther. The effect of temperature on anther dehiscence is just its effect on growth. This is seen from inspection of the data. A steady rise in the number of stamens ripening and presenting pollen occurs with increasing temperature. It was seldom that the limiting temperature for dehiscence could be ascertained. For Helleborus abchasicus it is less than C. Flower opening in Ulex europaeus, and anthesis in Ranunculus ficaria and Pyrtis malus cease at 5^ C. The difficulty in assessing the limiting temperatures in the field arises from the fact that the light intensity cannot be controlled. Scilla sibirica, Leucojum aestivum, Galanthus nivalis and Crocus aureus will open and present pollen at air temperatures of 4-7, 5 and 4 C. respectively if it is sunny; whereas temperatures of 8-5, "], 9-4 and 9 C. are necessary if it is dull. The lowest temperatures recorded for dehiscence in Lunaria annua, Arabis albida and Pyrus commiinis are 6, 5-2 and 5 C. respectively, but these figures may not be the limiting ones. Tussilago farfara. Taraxacum officinale, Plantago lanceolata and Ranunculus repens require 0 C. without sun for anthesis in the first two species and 9-0 C. for the second two. Fragaria x ananassa is a little higher; -7 C. is limiting if it is dull. The highest limiting temperature recorded is 5-3 C. in dull conditions for flower opening and partial presentation in Epilobium adenocaulon. Temperature and pollen collection. The February crops produce pollen freely at an average of 6-4 C. on a sunny day; but without sunshine from 9 to 0 C. is required for anthesis or flower opening. March crops average 8-8 C. for free anthesis and April crops 0 C. 0 C. has been stated to be the limiting temperature for bee fiight; inaction of the wing muscles is said to occur below this. It is seen that the February-Apri^crops have

13 Collection of pollen by Apis mellifera 365 pollen available at a slightly lower temperature than this. So there is a pretty balance here, the bee food being available in the flowers at just about the same temperature level that the pollinating insect can fly. There is yet another parallel. Crocus and Galanthus flowers open at 4 and 5 C. respectively if in sunlight, and bees were seen working these crops at 4 and 57 C. respectively if it was sunny. Direct sunlight compensates for the lower air temperature at a comparable level for both insect flight and flower opening. Extreme weather conditions may disguise a plant's normal rhythm of flowering and anthesis. For example, in the Dictionary of Gardening (R.H.S.) the flowers of Bartonia aurea are said to open in the evening and remain open until the following morning. During the wet, cold August of 950 (av. temp. 6-4 C, av. R.H. 94%) most of the flowers opened and presented pollen in the morning. During a sunny warm period in July 952 (av. temp. C; av. R.H. 75%) they opened chiefly in the afternoon. RELATIONS BETWEEN POLLEN PRESENTATION AND POLLEN COLLECTION BY APIS MELLIFERA The present data (Table 5 and Fig. i) indicate that in February, March and April, the chief period of pollen presentation and pollen collection each day is substantially the same. In May, June and July 65 % of the pollen crop is produced from 8 a.m. to noon. Table 5. Correlation between pollen presentation and pollen collection () Positive correlation in: Anemone nemorosa, A. appennina, Aubrieta deltoidea, Cheiranthus cheiri, Fragaria x ananassa, *Rubus fruticosus. Reseda odorata, Buddleia variabilis, Centaurea montana, Zea mays. (2) Correlation disturbed only for a short period in: Helleborus abchasicus, Brassica oleracea, Cardamine pratensis, Tropaeolum majus, Impatiens roylei, Ulex europaeus, Rubus loganobaccus, Prunus cerasus, P. persica, *Pyrus malus, Epilobium adenocaulon x parviflorum, E. adenocaulon, E. parviflorum, E. montanum, Plantago lanceolata, Scilla sibirica, Galanthus nivalis, Crocosmia pottsii. (3) Similar time curves of pollen presentation and pollen collection, but with non-coincident peak periods: *'Ranunculus bulbosus, fr. ficaria, f Arabis albida, * Vicia faba, Pyrus communis, *'Crataegus monogyna, *Prunus laurocerasus, Deutzia gracilis, fribes nigrum, * Aucuba japonica, * Sambucus nigra, Arctium vulgare, *'Taraxacum officinale, Tussilago farfara, Alisma plantago-aquatica, Limnanthes douglasii, *Endymion non-scriptus. Crocus aureus. (4) No correlation between pollen-presentation and pollen-collection in: *Clematis vitalba, *Sinapis arvensis, *Raphanus raphanistrum, Bartonia aurea, Aesculus hippocastanum. Ilex aquifolium, Ulex gallii, *Sarothamnus scoparius, Rosa spinosissima, Petroselinum crispum, *Rhododendron ponticum, Ligustrum vulgare. Convolvulus minor, Calystegia sylvestris, Scilla hispanica, Allium ursinum. * Major crops. t Peak period of pollen presentation in early morning, when the temperature is too low for bees to forage. but only 47 % of the crop is gathered in this period. In August there is even less agreement; 76% of the pollen production is between 8 and a.m., while only 34% of the daily total of pollen is gathered in this period. From May to August the daily rhythm of pollen collection does not alter greatly. It was indicated previously (Percival, 950) that there was a time relation between pollen presentation and pollen collection in certain species. Data of sixty species are now analysed. Positive correlation is found in ten species, and correlation which is upset for a short period only in flfteen species. In eighteen species the two curves are very similar but the peak periods do not coincide. No correlation was found in seventeen species. Therefore

14 366 M. S. PERCIVAL there is a degree of correlation in 7 %. The figure is 74% for minor crops and 64% for major crops. It would appear that the rhythm of pollen collecting is reasonably well related to that of pollen presentation in individual species. o 25 _ >^ 20 u "o 6^ ' total -o otal u 'o a m r-r a.m r-r May a.m July 0 5 n ^ ' r B 8 f -^ 2 TT" A C V.. p.m T" - r V 2 3 > p.rr ^ 3 ^^ 5 6 Dtal % of dai daily total o 5^ 5 6 _ dailly tot; "o &5 a.m i Apri Q a.m June U a.m. 5 6 i August _ ' ' > r~j_ ~T ' 9 i ^ 0 0 f r y 0 2 r s V 2 r ' p.m p.m 2 * 2 2 >.m -, ~-. 3 > ^^ Fig. I. Daily average curves of pollen presentation (continuous line) and pollen collection by Apis (broken (line) for February-August. ^ = February, B = March; C = pollen collection for February and March. N In sixteen of the eighteen species where peak periods do not coincide, the peak of pollen collection comes after that of pollen presentation. In seven of these this is a result of the temperature being too low for the bees to forage these spring species which have an early morning peak. Weather conditions in the early spring seldom permit foraging before 0 a.m. or after 2-3 p.m. On all the early spring species (except Crataegus, which is doubtfully classed here) we find a peak of bee activity between 0 a.m. and 2 p.m. So the early foraging, although it may coincide with pollen production, is more a function of the weather conditions. THE SIGNIFICANCE OF POLLEN COLLECTION BY APJS FOR POLLINATION Pollination is effected, in all the hermaphrodite or monoecious species so far observed, when the bees are collecting pollen, even where the dimensions of the flower and the disposition of its parts seem to render it unlikely, as in Helleborus abchasicus, Cucurbita

15 Collection of pollen hy Apis mellifera 367 pepo, Rhododendron ponticum and Magnolia x soulangeana. The bee vi^orks the anthers of the last species while holding on to neighbouring ones. The spread of the stamens is too great for her to work them from the carpel column as in Magnolia stellata, but the column may be scaled in leaving the flower. The worker need not touch the stigmas of the large primary flowers of Helleborus abchasicus when gathering pollen, but some were seen to visit young flowers which were not yet in anthesis and work the nectaries and then return to the older flowers. These later flowers are smaller and the bee is more likely to come in contact with the stigmas. This behaviour was interesting, for it is only in these later tertiary or quaternary flowers that a reasonable number of the nectaries are exploitable. The lips of the tube are pressed together in 84 % of the nectaries in the primary flowers, compared with 35 % in the later ones, so that the nectar is not available to the honey-bee. Bees working Rhododendron ponticum for pollen do not always distinguish the anthers from the stigma. One worker arrived at 9'37 a.m., left with a good load of pollen at 9-5 a.m. and during her visit made four attempts to reach nectar, scrabbled six stigmas for pollen and touched eight stigmas without scrabbling. So pollination is frequently effected. SUMMARY. The presentation of pollen in eighty-six species of angiosperms has been observed, together with the collection of the pollens by the honey-bee. Apis mellifera. 2. The plant unit observed was the 'flower form'. 3. The time of day at which pollen presentation occurs varies widely in different species. Eight time classes have been distinguished'early morning', 'morning', 'chiefly morning', 'midday', 'chiefly afternoon', 'afternoon', 'night' and 'night and day' presentation. Signiflcant differences occur between some groups and between the species comprising them, but whether the time of pollen presentation is a speciflc character is not proven. No phyletic signiflcance above the rank of species could be ascertained. 4. The duration of anther dehiscence per flower form ranges from simultaneous dehiscence in all the anthers to 26 days. It may prove to have a significance as a generic or family character. 5. The amount of pollen produced per flower form per day ranged from 547 to mg. It is of little consequence as an 'attractive' quality for the bees compared with the presence or absence of available nectar in the flower. 6. In times of shortage, the pollen of flowers without nectar, or with unavailable nectar, will be collected. 7. There is some evidence that the bees will exercise a preference for a pollen of particular biological potency. 8. Conditions limiting anther-dehiscence appear to be: {a) temperatures too low to permit the anthers to attain maturity, (b) presence of free water on the anther. Dehiscence will occur at 00 % R.H. n. Positive correlation or partial correlation between pollen collection and pollen presentation has been found in some species.

16 368 M. S. PERCIVAL REFERENCES BETTS, A. D. (920). The constancy of the pollen-collecting bee. Bee World, 2, 0. BETTS, A. D. (935). The constancy of the pollen-collecting bee. Bee World, 6, iii. BUTLER, C. G. (945). The behaviour of bees when foraging. J. R. Soc. Arts, 93, 50. EcKERT, J. E. (942). The pollen required by a colony of honeybees. J. Econ. Eiit. 35, 309. VON FRISCH, K. (950). Bees. New York: Cornell University Press, Ithaca. HODGES, D. (952). The Pollen Loads of the Honeybee. London: Bee Research Association. KNUTH, P. (905). Handbook of Ftower Pollination. Leipzig. LovELL, J. H. (920). The Flotver and the Bee. London: Constable. MAURIZIO, A. (95). Untersuchungen ilber den Einfluss der PoUenemahrung und Brutpflege auf die Lebensdauer und den physiologischen Zustand der Bienen. Report of the XlVth Int. Beekeeping Congr. p Leamington Spa. MAURIZIO, A. (953). Weitere Untersuchungen an Pollenhoschen. Beih. Schiueiz. Bienen-Zg, 2, H. 3, p MOLLER, H. (883). The Fertilisation of Flowers. London: Macmillan. PERCIVAL, M. (947). Pollen collection by Apis tnellifera. Nezo Phytol. 46, 42. PERCIVAL, M. (950). Pollen presentation and pollen collection. Nezv Phytol. 49, 40. PERCIVAL, M. (95). Pollen presentation and pollen collection. Report of the XlVth Int. Beekeeping Congr. Leamington Spa. RIBBANDS, C. R. (949). The foraging method of individual honey-bees. J. Anim. Ecol. 8, 47. SYNGE, A. D. (947). Pollen collecting by honeybees {Apis mellifera). J. Anim. Ecol. 6, 22. ToDD, F. E. & BISHOP, R. K. (940). Trapping honeybee-gathered pollen and factors affecting yield. J.Econ. Etit. 33, 866. VANSELL, G. H. & ToDD, F. E. (948). Bee-gathered pollen in various localities on the Pacific coast. Bull. U.S. Bur. Ent. and Plant Quarant. E-749.

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