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Bulletins 4000 - Research Publications

1993

Honeybee pollination of crops

Lee Allan Department of Agriculture, Western Australia

V. Kesvan

G. Kleinschmidt

P. Anning

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Recommended Citation Allan, L, Kesvan, V, Kleinschmidt, G, and Anning, P. (1993), Honeybee pollination of crops. Department of Agriculture and Food, Western Australia, Perth. Bulletin 4250.

This bulletin is brought to you for free and open access by the Research Publications at Research Library. It has been accepted for inclusion in Bulletins 4000 - by an authorized administrator of Research Library. For more information, please contact [email protected], [email protected], [email protected]. Bulletin 4250 ISSN 0729-0012 Agdex 100/20 • September 1993 ,

DEPARTMENT OF AGRICULTURE WESTERN AUSTRALIA Honeybee pollination of crops

By L.F. Allan, V. Kesavan, G. Kleinschmidt, P. Anning Department of Agriculture Western Australia Note:

of trade names does not imply endorsement or prefer- ence of any company's product by the Department of Agri- culture, and any omission of a trade name is unintentional. RecommendationsMention current at the time of printing. are

© Chief Executive Officer of the Department of Agriculture, Western Australia 1993 Cover picture — Pollination of cattalo

2 Honeybee pollination of crops Bulletin 4250 ISSN 0729-0012 Agdex 100/20 September 1993

DEPARTMENT OF AGRICULTURE WESTERN AUSTRALIA Honeybee pollination of crops

Authors L.F. Allan, Senior Apiculturist

South Perth, Department of Agriculture, Western Australia V. Kesavan, Horticulture Research Officer

Kununurra, Department of Agriculture, Western Australia G. Kleinschmidt, formerly Senior Lecturer, Apiculture

University of Queensland, Gatton, Queensland P. Anning, Principal Horticulturist,

Queensland Department of Primary Industries

Photographs Lee F. Allan

Editor J.A. Carpenter

Design F. Roberts

Honeybee pollination of crops 3 Contents 1. Introduction 5 2. Principles of pollination 7 2.1 Sex expression and mode of pollination 7 2.2 Outcrossing mechanisms 8 2.3 Agents of pollination 10 2.4 Pollination management 10 3. Honey bee food selection 11

3.1 Attractiveness offood source 11 3.2 Maximising pollination benefits 12 3.3 Foraging behaviour and bee management summary 13 4. Apiary management and nutrition 14 4.1 Food requirements of colony 14 4.2 Pollination hives 15 4.3 Inspecting pollination hives 15 4.4 Colony population level and economic use 16 4.5 Colony migration 17 4.6 Selecting apiary sites 18 4.7 Hive placement on site 18 4.8 Provision of suitable pollen 19 4.9 Crop isolation 20 4.10 Farmer's bee management summary 21 4.11 Pollination agreements 22 5. Effects of pest control methods on pollination 24 5.1 General principles 24 5.2 Chemicals as 'magic bullets' 24 5.3 Types of pesticides 25 5.4 Effects of pesticides on bees 29 5.5 How bees are accidentally poisoned 30 5.6 Direct effects of pesticides on plants 30 5.7 Poison hazards of some pesticides to honey bees 30 6. Further information 31 7. Glossary of technical terms 32 8. Index 34 ollination of horticult- growers who use pollination 1. ural and agricultural targeted at providing crown set Introduction crops is being recog- have realised improved returns nised throughout Australia by from quality fruit using this growers who wish to improve method. crop quality and quantity, to Li. Allan increase their returns from The pollination industry at Ktmunurra has become highly produce sold on local and export developed with the introduction markets. Some growers are able to target specific high value of honey bees. Here growers markets using planned pollina- have developed management tion to maximise their income. systems that include paid polli- nation services to produce Packaging of produce, par- quality produce designed to take ticularly fruit and vegetables, has advantage of market opportuni- changed in recent times with the ties. The production of hybrid seed crops such as sunflowers and horticultural crops including rockmelons, watermelons, pumpkins and to a lesser extent, mangoes and cashews has become highly profitable.

In the south west of the State, the high incidence of feral honey bees in some areas has been responsible for pollinating crops where bees are the primary vector. This means of pollination is referred to as incidental pollination. In many instances it is inadequate and leads to poor quality produce. The size and shape of some fruit and vegeta- Cashew orchard at Kan unarm bles sold on the local market provides clear evidence of aim of presenting the product in inadequate pollination. attractive stimulate an manner to The economics of introducing buyer with increased acceptance, managed pollination into benefits the For an to grower. integrated management example, apples sold in crop are now system needs to be carefully trays where much of the fruit is considered by the grower. While visible to the buyer. Accordingly feral honey bees provide some the public is becoming more pollination benefit through of quality and increasingly aware incidental pollination, the cost of selective of the produce offered acquiring managed honey bees for sale, may not be economic, even though improvements in Pollination of crops by honey crop quality and quantity have been bees, when implemented with an realised. integrated management system that includes irrigation, fertiliser Pollination requirements are application and pest control specific to the environment provide signifi- crop, programs, can and location. Growers need to benefits cant to growers. experiment with planned polli- nation using integrated Adequate pollination of crops an improves the quantity, size, management system to ensure shape, texture, colour and that economic benefits exist. flavour of fruit and vegetable crops. For example, rockmelon

Honeybee pollination of crops 5 To assist growers with this don service. The additional loss aspect, the Department's publica- of production for the remainder tion "Honeybee pollination — of the season caused by hives Technical data for potential crops becoming weak during the in Western Australia" by Rob period of pollination also needs Manning, provides a useful to be considered by the bee- guide. keeper. Generally, paid pollina- tion will be successful only if the Beekeepers in Western economic returns are favourable Australia migrate their hives for both the grower and bee- throughout the south-west keeper. portion of the State, following the nectar flows. During the Because beekeepers need to spring months, when most plan ahead to provide suitable pollination is required, most hives for pollination, it is recom- beekeepers have their hives mended that at least three north of Perth from Yanchep to months notice is provided. In Northampton. It is during this addition, a written pollination period that hive strength in- agreement between both parties creases and about one third of detailing the mutually agreed the beekeeper's annual income terms and conditions is recom- from honey production is pro- mended — see Section 4.11. duced. This spring build-up also enables the beekeeper to take This Bulletin provides infor- maximum advantage of addi- mation to both grower and the tional honey flows elsewhere in beekeeper on the complex issue the State during the rest of the of pollination so that both have a better understanding of the honey production season. subject and an appreciation of The cost to growers of con- the other's requirements. Each tracting hives for pollination section has been written by a during this period is therefore prominent researcher in this field likely to be high, since the and provides up-to-date infor- beekeeper must consider trans- mation on the subject. port costs and loss of honey production to provide a pollina-

6 Honeybee pollination of crops ollination is the reduce yields by diverting 2. Princiles transfer of photosynthates from vegetative of pollination pollen from the to floral parts. anther to the stigma of receptive flowers. For effective Pollination followed by pollination the pollen must be fertilisation is important in crops V. Kesavan viable and compatible. It is or plants grown for their fruit or obvious that pollination is seed; it is crucial to the success of relevant to flowering plants and cross-pollinated crops in which sexual reproduction where pollen transfer between different plants is mediated through offspring are produced by some fertilisation, that is, the union of agent or vector. In such crop species, understanding and male and female sex cells. an Pollination, however, is not management of pollination can lead better productivity and necessary for parthenocarpic to profitability. The mechanisms plants such as the triploid bananas and mangosteen that involved in pollination and develop fruits without fertilisa- fertilisation are varied and complex it involves the tion and for crops grown for as their vegetative parts. In the interaction between three enti- The of cross-pollination in Figure 1. process latter, flowering in fact ties: the flowering plant, the crop plants may pollinating agent or vector and the environment (Figure 1). sex, dichogamy compatibility 2.1 Sex expression and nectar / pollen mode of pollination

Most domesticated crop plants produce flowers that possess both male (staminate) and female (pistillate) sexes on the same flower. Such flowers are said to be bisexual or herm- aphrodite and are considered to be the original form in evolution. But variation around this com- mon theme abounds in nature, as demonstrated in the evolution of a range of sex expression in the cucurbits (cucumbers, melons, pumpkins and squashes). Sexual differentiation has culminated in the evolution of distinct male (androecious) and female (gynoecious) sexes as in higher animals with a mixture of floral foraging behaviour climate types during the intermediate visit / day crop management stages (Figures 2 and 3). In stocking rate other flora andromonecious cucurbits,

Figure 2. The evolution of sex expression in the cucurbits (after Whitaker and Davis, Original form Hermaphroditic 'Cucurbits', Leonard Hill, London, 1962) Intermediate form Andromonoecious Trimonoecious Gynomonoecious

End form Androecious Monoecious Gynoecious

Honeybee pollination of crops 7 eci 9 9 9 9 cc 9% sci fil 94 0 V' cif dl cc cc 9 df cl 9 9 9 9 cf 9%C)- cc 9 cif e e cif 9%9 cif cif y ? 9Y'y ic) cil e Cf eci'

Androecious Andromonoecious Trimonoecious Monoecious Hermaphrodite Gynomonoecious Gynoecious ci'df cif? 9?

Flower symbols: Hermaphrodite Staminate (androecious) Pistillate (gynoecious)

Figure 3. Schematic representation of sex in individual plants (After Frankel and Gahm, 'Pollination Mechanisms, Reproduction and Plant Breeding', Springer-Verlag, Berlin, 1977)

mangoes and cashews, the sex The different modes of races except for the removal of ratio in general is in favour of the pollination and reproduction off-types arising through occa- male flowers, determine the genetic structure sional outcrossing. of plant populations, which has The differentiation into two important implications for plant The production of F1 hybrid sexes is matched by two modes breeding. Self-pollination fa- seed is a special technique in of pollination, namely self- and pollination and is yours uniformity while cross- management cross-pollination. Self-pollination pollination promotes genetic largely a commercial venture involves the transfer of pollen diversity. The four fundamental undertaken by the seed compa- from the anther the stigma of nies where high premium is to populations are: a either the same flower or another paid for the F1 seed showing homozygous and homogene- flower in the same plant. Cross- • hybrid vigour. pollination is the transfer of ous pure-line varieties of self- pollinated for example, This leaves the highly pollen from one plant to the crops; van- wheat, rice, able open-pollinated species such stigma of another plant by a peas; the cucurbits and tree pollinating agent. Self-pollination homozygous, heterogeneous as crops • for fruits and seeds that is promoted by the hermaphro- landraces of self-pollinated grown require careful pollination dite condition, while separation found in subsistence crops management. of sexes, incompatible pollen and agriculture; male sterility promote 2.2 Outcrossing outcrossing. • heterozygous, homogeneous F1 hybrid varieties and mechanisms Charles Darwin, a keen vegetatively propagated observer of flowering plants, clones, such as maize, sor- Cross-pollination helps in noted that cross-fertilisation is ghum, onion, bananas, exploiting hybrid vigour in the not only beneficial to the species sugarcane; and short term and offers evolution- for its long survival and flexibility in the long term. It term heterozygous, heterogeneous ary evolution, but is also required for • is not surprising, therefore, to populations of cross-polli- maintaining vigour and fertility find a number of mechanisms nated crops, such as . in the short term. Even in highly promoting cross-pollination. cucurbits, Brassica spp., many self-pollinated crops, there is a tree crops. The important mechanisms small amount of outcrossing dioecy, dichogamy, each generation, providing are monoecy, Management of pollination is self-incompatibility and male genetic variability and flexibility, not needed in the case of self- sterility. pollinated pure lines and land 8 Honeybee pollination of crops Type A e.g. Hass

Type B e.g. Fuerte

Figure 4. Floral cycle in dichogamous avocado. Inter-planting types A and B allows cross pollination (Sedgley and Griffin, 'Sexual Reproduc- tion in Tree crops' Academic Pr., London 1989) Interplantirtg of these comple- S2XSIS2 SiS2XS/ S3 SiSzXS3S4 mentary types is recommended

82 81 S3 Si S4 S3 for maximum yield. 2.2.4 Self-incompatibility

Inability of fertile hermaphro- dite plants to produce progeny (zygote) after self pollination.

• Pre-zygotic self-incompat- ibility results from inhibition of pollen tube growth in the s2).. pistil and is under the control (vs.? of one or more genes with multiple alleles at the S locus. The genetic control may be in Figure 5. Gametophytic self incompatibility. Pollen grains carrying the same S alleles as the the pollen (gametophytic) or pistil are not viable. in the pistil (sporophytic). Source: Sedgley and Griffin, 1989. Examples are Brassica species, sweet potato, cocoa (Figure 5). maize, onion, cashews, 2.2.1 Dioecy Heterostyly: Plants with macadamia, • annonas, sporophytic incompatibility sapodillas. The male and female flowers have styles of varying length, separated spatially differ- are on • Protogyny: Female organs which results in reduction of ent plants; for example, paw- mature before the male pollen transfer. palms, paws, date asparagus, structures; for example, • Post-zygotic incompatibility: spinach, hops, hemp. avocado, sweet potato, taro, The zygote becomes nviable strawberries. 2.2.2 Monoecy due to abortion. For example zizyphus. The male and female flowers Protandry is more common mangoes, are separated spatially but than protogyny and could affect 2.2.5 Male sterility located on the same plant; for either single flowers or whole Production of sterile pollen, example, cucurbits, mangoes, plants. Among the plants exhibit- cashews, lychees, coconuts, oil ing protogyny, the avocado antherless flowers or anthers that palm. shows extreme flexibility for this fail to release pollen. Male condition with the female stage sterility is common in many 2.2.3 Dichogamy separated from the male stage by plants and occurs as a starting which the flower point for the evolution of Temporal separation, where a period during closes completely. Complemen- unisexuality. Male sterility is the male and female gametes in flowering designated tinder simple genetic control and the flower mature at tary types, same for cross-pollina- is used extensively in F, hybrid different times. A and B, allow tion since type A tree is essen- seed production, for example in • Protandry: Male organs tially female in the morning and tomato, onion, sorghum and mature before the female male in the afternoon and vice maize. structures; for example, versa for type B tree (Figure 4).

Honeybee pollination of crops 9 2.3 Agents of pollination Table 1. The effect of honey bees on fruit weight and fruit number in rocicmelon (data from Salvesrin, 1986) Cross-pollination requires the assistance of pollinating agents transfer the pollen between Treatment Total weight plot Total no. of fruits Fruit size (kg) to kg/6 rrt` flowering plants. The important agents are: No bees in cage 13.43 20 0.68 Bees in cage 28.50 26 1.11 • abiotic agents: wind and rain , Increase with bees 112% 30% 63% • biotic vectors: insects, birds and mammals (bats). mended to maximise yields 2.4.3 The environment Of these, wind and insects are through improved pollination the most important agents of and fertilisation. The prevailing weather pollination. Among the biotic conditions, management prac- vectors, honey bees play a key The foraging behaviour of the tices used for the crop and the role in regulated pollination of bees will influence the layout presence of competitive flora fruit and seed crops. Many crops and siting of crop genotype and have a profound effect on flower- have bees as the main vector and pollen donor trees. ing and vector activity. In gen- depend mainly honey bees for eral, high temperatures reduce on Recent work cashews inflowering their pollination. Crops also on (or promote maleness), use a Kununurra has shown the need combination of outcrossing pollen growth and ovule longev- for inter-planting superior mechanisms and more than one ity and thereby reduce the genotypes and provision of vector to achieve cross-pollina- g p effective pollination period insect pollinators. Fruit and tion. set (EPP). Supplementary pollina- yields in cashew have increased tion beyond EPP is not beneficial. 2.4 Pollination significantly with the introduc- It appears that EPP is extremely management tion of honey bees. short (about three hours) in 2.4.2 Honey bees and bee hives cashews. Other climatic factors In agriculture, pollination such as wind, rainfall and high management largely revolves The density of bees and the humidity affect vector activity. around the management of number of visits required for honey bees and bee hives. Since effective pollination determine The sugar content in the influences the attractive- pollination is an interactive the number of bee hives. For nectar of competitive flora. Apple process between the crop, the example, studies in the USA on ness blossoms preferred by honey vector and the environment, an rockmelons have shown that are bees to peach flowers because of integrated approach is war- each flower is visited 10 to 15 . higher in the ranted. A major concern is the times during the day and 7 hives a sugar content In the Ord River Irriga- integration of pesticide use with per hectare are required for high nectar. bee hive management. Some yields. Significant increases in tion Area, stmflowers have been aspects of integrated pollination fruit weight, fruit number and found to be more attractive to management relevant to agricul- fruit size of melons were re- bees than melons. highlighted in Section 5. corded at Griffiths, NSW with ture are A healthy plant is prerequi- the of honey bees (Table 1). a 2.4.1 The and pollen donors use site for adequate flowering and crop Trials in Victoria pumpkins on display to attract the biotic have shown that fruit is set Outcrossing mechanisms more Optimal irrigation, when the bee density (as vectors. such as dichogamy and self- meas- nutrition and practices such ured by the ratio of flowers to as incompatibility in the crop leads root pruning, girdling and inter-planting of donor bees) is higher. to geno- hormone sprays can improve that have cross-compatible types In fact, the introduction of flowering. But the use of pesti- pollen. A knowledge of floral cides conflict bee-hive honey bees in orchards is an may with biology is crucial to pollination accepted management practice in management. pesti- and pollen donor selection. many parts of the world. Bees cides late in the day and the use of pesticides with low toxicity In avocado, cashews, and bee hive management are cocoa, help in resolving this and macadamia, inter- discussed later in this Bulletin may annonas conflict. planting of pollen donors along (Sections 3 and 4). with the introduction of honey From this outline of principles bees in the orchard is recom- of pollination, it is clear that proper pollination management can increase crop yields.

10 Honeybee pollination of crops Honeybee 3. ee colonies exercise a Bees prefer new food sources selection 'Law of Profitability' that have similar odours to food in the collection of previously worked species. If nectar. The normal colony does only new species are available, not work nectar sources that will they prefer odours similar to return a net loss of energy to the previous sources (odour stimula- G. Kleinschmidt hive. Starving colonies will work tion for response). food behaviour poor sources, a Attractiveness of food that accelerates the death of the 3.1 colony. Such behaviour is nor- source mally associated with man's interference. The attractiveness of the food is determined by: For both nectar and pollen, types in the field force waits for the scout • sugar nectar bees to locate food sources and • concentration of sugars communicate the food to source abundance of the field force of bees in the hive • nectar (95 per cent of bees). On a daily • colour of flowers basis, the main field force waits odour of flowers for reinforcement before forag- • ing. Bees working different crops • plant physiology respond to bees returning with • distance. that crop odour and communi- cate with them. Sitgar types

The foraging procedure of a Bees prefer straight sucrose scout bee is to locate food by (cane sugar), glucose or fructose, sight (colour, shape), then aroma, or equal portions of each. and finally landing to sample the Concentration of sugars food. If the crop is attractive and the scout bee can obtain several The threshold level for sugar food loads, she communicates solution acceptance varies with the main field force (gather- between 20 per cent and ers). Communication activity is 30 per cent. Bees can determine accelerated by nectar that has a the highest concentration and high sugar content, causing the work this source first. When it is best sources to recruit most of the used, the next highest concentra- bees and the poor sources to tion is selected, but the reduction have few gatherers through also causes decreased communi- reduced recruiting. If the gather- cation and recruiting. Concentra- ers are satisfied, they work the tion is the species determiner. crop until reduced availability Abundance of nectar causes dissatisfaction, or until a better source becomes available, A large abundance of food if the original is The source poor. enables many bees to orientate to recruiting procedure be Figure 6. Recruiting procedure can the crop, making abundance the summarised by Figure 6. attractant. CO10111' offlowers Scout bees communicates Gatherers Bees can differentiate colours with wavelengths between 300 and 640 m (ultra-violet, blue, green, yellow). All other colours appear the same to bees, unless the flower reflects ultra-violet light. In that case, what appears as a colour such as red to us is the colour 'ultra-violet' to bees Many nectar guides are ultra- violet spots or stripes.

Honeybee pollination of crops 11 Odour of flowers The attractiveness of a crop moved in at 10 per cent can be varied by climate. If flower and the remainder at The floral odour is the stimu- weather conditions are poor, full bloom. lant that causes individual bee flight is restricted to little as as During unfavourable weather response. When colonies cannot 100 Flight activity is reduced • m. conditions, bees should be be re-located on the target crop by temperatures below 16°C or adjacent to in the to cause crop fixation, scent above 33°C, light at less than or crop. direction using floral odour may 65 klm/sq. m, wind at 13 km/h • Crops with dilute nectar be used. The first flowers of the and mist or light rain that dilutes sugar levels often increase soaked crop are in sugar syrup nectar. In these conditions it is sugar concentration if irri- (1:1 cane sugar and water) and essential to place the colonies in gated at early bloom. fed to the bees to reinforce the the crop. Crops requiring pollen crop odour in the hive bees. • collectors need hives with When the hive bees begin forag- Bees that fix to a crop tend to a large brood ing, the target crop scouts attract return to the same area in the area. the new recruits and enable a crop on each flight. For tree crops • Crops pollinated by nectar disproportionate number of this fixation area is one to three collectors require large adult recruits to be obtained. trees and on ground crops populations. approximately 10 sq. m in small Plant physiology Adjust planting times to areas where orientation is • avoid competitor food Many plant physiological accurate. In large homogenous crop flowering of trees factors influence either areas of monoculture the fixation sources or crop (tree reproduction cycles how the flower is area may be as large as 60 sq. m acceptance or indicate probable flowering approached. except at the corners where it is time 3 to 18 months before reduced to 40 sq. in. Where For example: cross-pollination is required, the flowering). pollen should be within weed flowers. • The lucerne tripping mecha- source • Remove 10 m of the recipient. nism causes bees to collect • Use landmarks to assist bee pollen elsewhere and to Bees located in a crop forage orientation. collect lucerne nectar without intensively within 100 Lu- m. • Place hives closer to the crop tripping the flower. seed yields be cerne can if competitor food sources 30 higher within 100 • The stiff stamens on Delicious per cent m cannot be avoided. apples encourage the bees to of the bees than 300 m further work nectar from the side, away. If bees fly to the crop from • When pollen transfer across thus avoiding both stamens 2 km away the field distribution rows or between trees is and stigma. is not localised but uniform over required, observe pollen plant the whole In agricultural location guidelines. Extra-floral crop. • nectaries on such long flight distances provide areas, • If cross-pollination is re- cotton more concen- not practical because closer trated than the flower. are quired, stock the crop to nectar competitor attract the bees. crops minimise food per flower. Distance 3.2 Maximising pollination This maximises the number of flowers visited flight. If More is expended benefits per energy the field is over-stocked, the with a longer flight distance to a excess bees forage elsewhere. crop. Poor food sources may be Colony foraging behaviour attractive if bees are placed in the must be manipulated to maxim- • When contamination by crop, whereas a short flight ise pollination benefits. pollen from other areas must distance make that be avoided, stock the can crop Locate hives in the when crop unattractive. Location of hives to • crop heavily. Heavy stocking will sufficient food is available to maximise distance to competitor use enough of the available encourage bees to fix to the food sources whilst minimising foods, minimising the attrac- target crop. This is usually at distance to the target crop is a tiveness to bees flying in from 10 per cent flower. When a consideration of hive placement. the other areas. crop is not attractive bees are These attractiveness factors moved in at 40 per cent • Maximise flight efficiency by allow bees to differentiate flower because they will work placing groups of hives in non-symmetrical between varieties within a the poor crop for two to three groups so' that the bees easily species. The age of the flower days until more attractive can identify the location. Lost may make it more or less attrac- distant food sources are tive. located; or half the bees are bees reduce pollination. Hives

12 Honeybee pollination of crops in tidy symmetrical patterns 3.3 Foraging behaviour and bee management summary or rows cause the field bees to become disorientated. Provision of pollen - planting arrangement Check for flight activity • crops Bee food value - determines hive locations at the time of day the plant provides pollen, not when it - irrigation program suits Nectar is excreted you. - variety at pollen dehiscence and bees Time to bees in less than 10% early set cease working when the crop move - is attractive. Their time not - 10% average sense allows return to the 40% machine harvest or low attraction crop at excretion times only. - 10% and 50% crop physiological problem • If weather conditions are - be poor, bees must protected Crop order - prefer last crop worked from prevailing winds and scent direction they will use a flight path - behind a wind break. They Competition - mow weeds, use distance; plant to avoid will favour the leeward side competition with other crops or trees; or the sunny side of trees, or hive placement both. Hive management - nectar or pollen bees Flower attraction - soil nutrients - soil moisture - age synchronisation - male/female synchronisation Lost bees - use landmarks - non-symmetrical hive groups Climate and bee flight

Wind - more than 13 km/h, use windbreak - more than 22 km/h, minimum flight Light - more than 65 klm/sq. m Rain - dilutes nectar Temperature - 9-15°, flight less than 100 m unless hive very strong colony;

- 16-32° optimum flight; - more than 33°C, flight reduces. In poor weather — flight 100 m; place hives in or adjacent to crop in small groups. In good weather — flight at least 500 m in crop, so groups of 20 to 30 hives on crop corners or near orientation points.

Honeybee pollination of crops 13 4.1 Food requirements of a Bees are unable to discrimi- 4. Apiary- colony nate between pollens on the basis management of nutritive value. The bees are The basic dietary constituents attracted by substances in the and nutrition pollen. In nature, bees and plants of adult honey bees are nectar or honey, and pollen. Nectar and that required insect pollinations complementary. The honey are carbohydrate sources were and pollen contains all other attractive pollen ensured bee G. Kleinschmidt factors required for life, visitation and pollination for the plant; in return, the plant pro- Honey contains sugars, which \Tided suitable pollen to support make up 95 to 99 per cent of the honey bees. solids. Honey is basically a This plant/insect relationship source of energy, and a material does not necessarily exist with to be converted into fat an d plants selected and bred by glycogen. Bees need a blood man. Many of the varieties have sugar level above 0.5 per cent for new lost their ability to attract flight and blood sugar levels or support bee colonies. usually average 2 per cent, Pollen provides proteins, fats, As well as the individual minerals and vitamins and is plant/insect relationship in essential for growth of emerging nature, the bee diet was further bees and the development of safeguarded by the presence of a hypopharangeal glands. range of plants, which allowed colonies to divide field workers Emerging bees fed only between two or three target honey decrease in weight, body crops. This diversification protein and have a high mortal- ensured a balanced diet. Modern ity rate. Bees provided with agriculture's monocultures honey and pollen increase in reduce food diversity as well as weight and body protein and often providing inferior foods, mortality is low. When a range of foods are Insects accumulate stores of available, colonies work several nutrients in their body tissues to target crops for pollen, but the be mobilised and later used for majority of nectar collectors work nutritional purposes. Honey bees the most attractive source. The also store honey and pollen in colony field workers divide into combs. The combination of these about 25 per cent pollen collec- stores allows bees to rear brood tors, 58 per cent nectar collectors, for short periods when diet is and 17 per cent collecting both deficient, pollen and nectar. When the hive has a large brood (reproductive) When field food sources are area or is stimulated to expand deficient, apiarists can corn- egg laying, the number of pollen pletely replace nectar by sucrose collectors is increased. (cane sugar). The biological effectiveness of materials fed to In Western Australia, the bees to replace pollen has not major nectar and pollen sources been satisfactory. are eucalypts, coastal heath and weeds. Fruit and seed crops are of Proper nutrition is one the generally poor food sources for factors influenc- most important honey bees, the notable excep- ing longevity of emerged bees. tion being canola. The pollen The substitution of incorrect quality from sunflowers, pears natural foods the or excessive and kiwi fruit is very low. Bee down of body run nutrients colonies rim down on such results in short lived bees and pollens. Sunflower pollen at colony decreased populations. 15 per cent crude protein, is 5 per cent below the minimum

14 Honeybee pollination of crops needed for light work and 10 per cent below the minimum needed for bees to perform heavy work. In this case, the bees make up the deficiency from their bodies. Since bees have an exo-skeleton, the body run down is internal and not observed, as would be the case with mam- mals.

Continued access to native forests and coastal heath lands are essential for strong colonies with healthy bees. Reduced access to these areas may affect the beekeepers' ability to provide the strong hives needed for Access to natural resources is essential to build strong colonies for pollination of agricultural effective pollination of agricul- crops tural in the future. crops bees covering at least eight of the Colony defences increase as 4.2 Pollination hives super top bars when the hive available nectar decreases. When cover is removed. Such hives are bees are forced to use their honey colony defence is Study of the topic 'Colony nearing the third hive body stage stores, a strong mounted. When field is population level and economic and are good value at current nectar bees will rob use' (Section 4.4) shows that rental levels, scarce, attempt to other colonies. Handling colonies economic considerations deter- In circumstances, it is this time robbing mine the strength of the colony some at causes to not unusual for predominantly escalate rapidly. Both robber that is available for pollination three storey hives to be provided, bees and colony defenders will services. Whilst unusual an These instances when both attack in the immediate circumstance lack of honey are persons or the apiarist and farmer have vicinity. will the availabil- prospects vary worked together for ity of hives, in the long term rent some years and co-operation is at high Plants have an optimum levels determine colony strength. a level. The continued co-operation temperature and relative humid- If pollinating bees required are is virtually unwritten long ity for the release of nectar and early in the second an very season, a term contract and the approach pollen. This release may be at factor the effect of winter — on of each is flexible in attempt to any time during the day, but in colony breeding will have an — a foster co-operation and long term warm climates is usually early in major influence available on stability, the day. Some crops such as colonies. This can be partially pumpkins provide food early in compensated for by special Such co-operation ensures the day and are worked by bees nutrition procedures if rental discussion, understanding, from 5 to 10 am. By 11 am bees levels permit such special man- consideration and an operation tend to rob and sting if hives are agement. of the highest order. These are opened. not the 'one off' situations that An hive used for average with the specula- Observation to determine the pollination would be two story are common a tors. time of day the crop is attractive Langstroth hive with twelve to bees is important for assess- combs well covered with bees 4.3 Inspecting pollination ment of the bee density in the and the remaining six combs hives crop, as well as for indicating with reasonable bee This cover. when colonies can be inspected hive would also have at least Bees vary hive defence, with minimum difficulty. combs in the lower brood seven depending on the amount of box that least Colonies tend be are at 60 per cent nectar available in the field. Bees to more worker brood. Such hives meet difficult to control when heavy are easier to handle when ample the specified strength level operated adjacent in nectar is available than when equipment is most contracts. to them, Immediately after nectar is scarce. Ample nectar is characterised by whitening of mowing or discing weeds or To ensure that the hives are around the hives, the field wax on combs and clear liquid in grass satisfactory, most apiarists bees disoriented and they the empty cells in the brood are are supply a two storey hive that has liable to sting. area. more

Honeybee pollination of crops 15 Adverse weather conditions also affect the temperament of hives. It is therefore prudent to inspect hives on warm sunny days when the bees are actively foraging.

Growers are encouraged to inspect hives with the supervi- sion of the beekeeper, so that the standard of pollination hives agreed to is assured. Reputable beekeepers will gladly agree to this request at a suitable and mutually agreed time. Allow several days for the bees to orientate in the crop before inspecting hives. Strong colonies with at least seven frames of brood are required for pollination

Table 2. Honey flow hive contents (data from Table 3. Colony population change in one month (data Kleinsclunidt et al., 1975) from Kleinschmidt et al., 1974)

Population Brood combs Hive bodies Honey/day Birth Death Net Result

30,000 4.5 - 7.5 2 33,505 45,089 -11,584 Down 35,000 4.5 - 9.0 2 - 3 2 kg 18,691 32,936 -14,245 Collapsed 40,000 5.0 - 10.0* 3 43,335 43,061 + 274 Held 45,000 5.7 - 11.3* 3 - 4 4.5 kg 50,000 6.3 - 12.5* 4 60,000 7.5 - 15.0* 4 - 5 *Require double broodnest or comb movement.

two to three hive bodies and, Table 3 illustrates the effect of Do not inspect the hive area depending longevity, 4.5 9 three different brood levels the the day after the bees have been on to at combs of brood. start of flow colony removed. Bees that had not a on populations during the flow. returned to the hive the previous As colony populations exceed Colonies with only about 19,000 night will be in the general area 40,000 bees they require at least cells of brood experienced and sting moving in a net may persons three hive bodies and more than loss of about 14,000 bees the first that It could be several area. ten brood combs. Such colonies month and the hives days before the is were area coin- require either double brood obviously weaker, whereas hives pletely safe. nests, bee and brood supplemen- with about 43,000 brood cells 4.4 Colony population tation or brood manipulation to maintained their strength. level and economic build populations averaging use 50,000 bees. When the honey flow location 4.4.1 Optimum population level provides ample pollen, colonies Strong hives with a popula- carrying in at least 40,000 cells of As colonies increase in tion of 45,000 to 60,000 bees brood maintain their strength. strength, the number of bees that requirehanicala mechanical lifting Colonies with inadequate brood system. The loader also are surplus to those needed for can experience an initial reduction in hive maintenance increases facilitate hive management in the strength, then slowly increase field and assist in hives rapidly. These surplus bees are moving populations. available for the collection of from one honey flow to another. If the honey flow does not honey that the apiarist may The foraging activity associ- provide pollen, the colonies extract. with ated with a heavy honey flow inadequate brood at the start will In field production trials, results in high bee mortality. The collapse. In reality, the pre-flow colonies averaging 45,000 bees initial reduction in colony history would be the major population during the early part produced 4.5 kg of honey per contributor to colony collapse. day, whereas hives of 35,000 bees of the honey flow is significant if hives do not have adequate Longevity good honey produced 2 kg per day on warm on a weather honey flows (Table 2). brood. and pollen flow can be increased Colonies of 35,000 bees require from an average of 26 to 30 days to 43 to 50 days by suitable pre-

16 Honeybee pollination of crops Table 4. Births and longevity (Kleinschmidt and Kondos, 1977) Longevity Eggs/day 20 days 30 days 40 days

1,116 20,000 30,000 40,000 1,300 23,400 35,000 46,800 1,700 30,600 45,900* 61,200* 1,900 34,200 51,300* 68,400* 2,100 37,800 56,700* 75,600*

*50,000 bees = 1,900- 2,380 eggs/day, therefore these require brood movement. flow and honey flow nutrition, for the near That is, on excellent breeding future are good. conditions with increased ion- Strong colonies gevity, a daily egg laying rate of do often set a about 1,200 will result in colonies crop much faster Beekeepers use mechanical loaders and move hives at night of 50,000 bees, than weak colonies. In hybrid sunflowers, specialised pollination is paid a In environmental average this may allow harvest three to fee for a service and conditions conditions, laying between a rate four weeks earlier. However, in are defined in advance in an 1,900 and 2,400 eggs per day for normal circumstances the agreement. a period of 9 to 12 weeks is apiarist's income does not justify needed breed populations of A strong apicultural to the use of his strongest hives. enter- 50,000 bees. Table 4 illustrates prise must base decisions on this interaction of birth and The general trend is to hire viable economic considerations longevity on colony population. the 10 per cent of hives with less in the same way that a farmer than 40,000 bees (usually about uses sound financial advice. This 4.4.2 Economic use 30,000 - see Table 2), because philosophy alone indicates the The ultimate in management such colonies have a lower honey doubts involved when the yield is to have all hives at optimum yield potential. In addition, the of a crop is placed at risk by population level for honey apiarist may make up the con- speculation. In most instances production, but this is rarely tract hive number with hives farmers can expect to get what achieved. In average build containing 40,000 to 50,000 bees; they pay for — this might not be bonus the farmer, what required. conditions, 80 per cent of hives these are a to is could exceed 50,000 bees, The net result in practice is 4.5 Colony migration 10 per cent could have from that to 20 cent of hives 40,000 to 50,000 and 10 cent up per per be allocated for pollination Hives be 8 10 frame less than 40,000 bees. On long may can or a by apiarist because: size and often placed the income an are on term average, gross pallets. When hives loaded of each hive must be $150 to $200 the lower 20 cent have are • per with entrances facing the cab of for the apiarist's economic reduced yield potential; the truck, there would be six survival. On today's operating • the apiarist's cash flow is hives in layer. If side costs this production must be per row a improved; and entrances used, there would maximised while minimising the are be four hives the truck. cost of production kilogram income is diversified. across per • Hives usually loaded in two of honey. are The hive rent level and bee layers, giving eight or twelve per A honey surplus from polli- value of the crop will vary these row across the truck. Unloading that multiples of nation crops is unusual. Often, factors. As value increases, a in groups are these is efficient. bees come off the crop weaker range of management proce- most than they went both in dures to maximise bee activity in on, Hives two stories high weigh number and longevity, because the crop become economic. from 40 to 60 kg and three storey of low protein pollens and hives weigh 50 to 100 kg. Strong pesticides. Overseas, intensive prepara- tion of hives for pollination is two story pollination hives An apiarist's better hives carried out, and the philosophy would number 17 per tonne. would be too valuable to risk on of `cheapies' or 'freebies' is a pollination contract of considered too speculative a risk $30/hive, especially if prospects — the apiarist overseas providing

Honeybee pollination of crops 17 Closed entrance migration

Hives may be moved with the entrance either closed or open. The major disadvantage of closed entrance migration is over-heating of the colony and melt-down of the combs. If the closed entrance method is used, hives are closed after dark. The night must be cool and dry and the colonies must not have fresh nectar. Loading must be delayed until early morning if bees have fresh nectar.

When colonies are populous, closed entrance hives must be Pallets with four six hives facilitate quick and loading of hives loaded quickly and the load kept or easy moving for air circulation, to At the site bee flight diverted well above minimise melt down in the new • public thoroughfares stock middle of the load. The apiarist's or The newly placed bees are tracks; equipment must be in good disorientated initially and need condition for closed migration, is provided; at least a day to locate food, • water because bees rush out of any orientate and settle down. site adjacent bright opening. • not to light particularly fluorescent; Mechanical loading systems The hives must be bound are either a 'boom' moving single • shade during the heat of the together with emlock strap- an hives, or a system using pallets day in hot climates; ping similar method. The or of four or six hives. The pallet closed method is preferred only • protection from fire hazards. system uses a fork lift or hydrau- when hives have to be trans- lic loader, and may lift one or Hives sink into the ferred by hand for transit the may on two pallets at a time. ground during wet weather. To farm unloaded by hand. or minimise this problem, the soil Hives closed during pesticide should not be cultivated before When closed hives are application overheat and melt receiving the hives. Hives placed opened, the bees rush out. down the in closed same as bare ground overheat Entrances should be smoked and migration. Hives should on may entrance because of the reflection of heat. opened without using a light. be closed just before daylight The operator must continue to and opened before the day 4.7 Hive placement site quickly down the and on move row warms up (usually before then leave the for at least area 8.30 am). Avoid neat symmetrical hive one day. 4.6 Selecting apiary sites patterns. Such tidy apiaries Open entrance migration promote drifting of bees. Bee orientation is assisted by placing Hives moved 'open entrance' A good bee site has the hive lines on the contour with loaded before dusk and following features: are occasional shrubs or rocks in the moved after dark. Some bees will • access to pollen and nectar row. Hives not on pallets should be the outside of the hives. on within 1 kin; be 2 m apart or in pairs. Place Open entrance moving is facili- hives with the good drainage; entrances at tated by hive loaders and gener- • different angles but in general ally regularly attempted not • protection from prevailing towards the sun. unless a mechanical loading and winds; unloading system is available. When no orientation marks protection from pesticide drift Loads of open entrance hives • are available during summer in (in scattered trees must avoid fluorescent lights and or on an agricultural area, hives are windward side of crop); stopping in light areas and placed in semi-circular groups adjacent to gates. When the • landmarks for bee orientation; with all entrances facing out. vehicle stops some bees may fly, This layout forces bees to orien- all weather particularly to lights. • access; tate, whereas straight lines do not encourage orientation and

18 Honeybee pollination of crops a a bb aa bb a abbbb a a

aaaa aa a aaaaa aaaa aa a aaaaa (1 in 15) (1 in 9)a aba ab a aaaaa aaaa aa a aaaaa aaaa aa a abaab a aba ab a aaaaa a aaaaa a aaaaa Common planting ratios for trees a aaaaa a abaab bees fly back down farm tracks For tree crops, the pollen If hives are located in neat and enter the first hives con- supplier should be within 10.5 m symmetrical lines, the bees tend tacted. of the recipient. to drift to the first hives in the row. Hives should be in non- If 4.8 Provision of suitable Bees tend to follow rows. symmetrical groups to minimise pollen pollen plants are not located in drifting. Place about 24 hives in and the be- each row, spaces each group and locate the groups Hive placement and stocking tween trees in the row and at land marks such as corners. between is different, rates are determined by: rows very the bees will not effectively move A group of hives in a non- • whether pollen movement is the pollen. Common planting symmetrical pattern in the within between varieties; or ratios for trees are seen as above, middle of a crop can orientate bees the position and maxim- the number of seeds per to • For ground the general flower for the preferred shape crops, ise flower visitation in the crop. rule is widths exceeding ten of fruit; not This is important if locations at hybrid seed produc- metres. In the sides of a crop are close to number of fruit plant • the per tion of sunflowers, row patterns competitor food sources. When a for the desired market size of and of 8 female:2 male, 12:4 14:4 competitor food source is located fruit; satisfactory whereas 16:2 are on one side of the crop, bees have significantly reduced seed should be located the • the time the flower is open not on and receptive; and sews.t in some rows. sides or corners adjacent to the competition. bees placed • the gross value of the crop. For ground crops, at the end of rows fly down the Number of seeds for fruit shape Pollen movement If the bees are located at rows. fruit the sides they have to The number of seeds in Pollen movement within one corners or work until with required varies according to the variety, for example, white across a row sufficient food is located. This accepted shape of the fruit. clover, can be achieved by bees Stone-fruit have side larger flight pattern can be intensified one fixed to small localised areas. than the other, because of by locating larger groups of one When pollen movement is ovules seed, whereas hives to force bees to forage two sets a between varieties or between areas the hives, apples and pears are expected to male and female plants, bee of the crop distant to After foraging, the bees fly out of symmetrical. Apples require 5 to flight patterns must be less 7 seeds evenly spaced in the the rows and follow farm tracks uniform and the pollen plant fruit. back to the hives. located within the fixation range.

Honeybee pollination of crops 19 Some fruits require many seeds; for example, a watermelon Considerable risk must receive at least 1,000 pollen grains on each of the three lobes crop of the stigmas.

Flowers of cucurbits open for 2 km 2 km Hives one day only. They must receive 10 to 12 bee visits during that day. Apple flowers can be crop crop receptive for 5 to 7 days. Apples require 3 to 5 visits during that Little risk time. Bee stocking rates are Hives varied the according to quantity crop of pollen movement and the time available for that movement. Number offruits 2 km 2 km

The number of fruits per plant varies according to the crop crop ability of the plant to develop the fruit and the desired size of the Minimum risk fruit. Some fruit trees require Hives only 2 per cent of flowers to set crop fruits, whereas seed crops require a high percentage of florets to set seeds. There are 3 km 3 km specific preferred sizes for processed cucumbers and restaurant pawpaws and crop crop rockmelons. Stocking rates are increased or decreased depend- ing on the market size prefer- Figure 7. Contamination of sunflower crops is affected by location of hives and the target and ence. contaminating crops Gross value of crop • temperature, kilometre to them. The attractive- Market-price seed prices ness of a species often varies • stocking rate determine if higher stocking , between varieties. seed produc- competing flora, and rates to maximise • Temperature tion economic. The seed are • distance. value for new introductions is Flight distance is influenced Pollen viability often very high and warrants by temperature. At 9 to 15°C, maximum production, whereas bees flight Some pollens viable for restrict to 100 m. At 12 high stocking rates not are 13°C, hives forage are only short periods particu- to strong economic when seed is plentiful very p 800 whereas the weak hives larly in hot weather. Others m and prices lower, still restricted remain viable for long time and are to 100 in. At 14 a 16°C, bees overfly the 4.9 Crop isolation be passed from bee to bee in to may may food available the hive. at 200 and 800 and work crops up to 1.5 km When honey bees are used to Crop attractiveness distant. Such progression as spread pollen from donors to a daily temperatures increase is the hive location and recipients, Very attractive crops will normal. the crop isolation are important encourage bees to overfly inter- if the risk of foreign pollen is to mediate flora. A crop three Stocking rate be minimised. kilometres distant could be A field stocked attractive. On the other hand, at a rate that Major factors to be considered most of the available food crops such berseem clover, uses as satisfies adjacent hives and these are: kiwi fruit and pears have a low crops are then unattractive to • pollen viability/temperature, sugar concentration in their nectar and bees will not fly a • crop attractiveness to bees,

20 Honeybee pollination of crops distant colonies because food 4.10 Farmer's bee management summary abundance does not permit profitability. Before planting

Competing flora • Bees — acquisition, contract An attractive alternative food — access — storms between the target source crop — other factors and distant crop that may provide pollen contamination — safety — floods often satisfies colony require- — pesticides ments. It may pay to temporarily likely contamination leave the weeds between the two — crops. • Competition — timing of flowering — weeds and trees Distance — target crop attraction As well as the effect of the • Pollen — self above factors on distance, hive — cross — timing location in relation to the target — compatibility and contaminating crops is important. Figure 7 shows — plant arrangement examples of distance effects in One month before flower the contamination of sunflower confirm crops. • Bees — contract — expected date — stocking rate — apiarist's telephone number — pre-bee plant protection program — neighbour's plant protection — local aerial operator — agreement for pesticide emergency — weeds — locations — trailer access — irrigation — complete adjacent farm operations (apiarists colony stimulation?) Pollination period

• Bees, when — 10% of flowering — 40%; machine harvest, or low attraction — 10 and 50%; crop physiological problem • Where — access (8 t truck) — rain — competition — crop attractiveness — isolation — placement pattern • Is adjacent farm work completed?

Honeybee pollination of crops 21 4.11 Pollination Agreements should include agreements the following subjects: • Name and address of partici- Various kinds of pollination pants, the crop and its loca- agreements can be used when tion. bees rented for pollination. are Number and strength of These from verbal to • vary colonies. written agreements. Too fre- quently, a pollination agreement • Dates of delivery and removal ends in dissatisfaction, to the of hives, detriment of both and grower A showing number beekeeper, because of • map exact some and location of hives the condition not clearly agreed on property. upon in advance. Often these misunderstandings occur be- • The right of access to the cause neither party has encoun- growers property, detailing tered conditions peculiar to the roads for servicing hives. of bees in agricultural use or Protection of colonies from apicultural practices. • pesticides and other farm Because of these and other operations. that reasons may arise, an • Supply of water for bees and explicit agreement should be protection against hazards insisted by both parties. upon such as fire and flooding. Usually no penalty is included in agreements for either party, but • Pollination fees, including amount, time, place and it may be wise to agree on a mutually accepted arbitrator, method of payment. should disputes occur. • Availability of adequate lines of communication — dates, times and phone numbers when each party can commu- nicate with the other. • Rewards, including discounts for prompt payment, services in excess of prescribed amount, or other benefits to either party. • Penalties for delayed pay- ment, damage to bees or equipment by the grower, failure to deliver or remove colonies on specified dates.

22 Honeybee pollination of crops Pollination agreement (example)

(1) The BEEKEEPER: agrees to provide standard colonies of bees at the rate of hives per hectare for the pollination of hectares

of situated in the district of and owned by

(the GROWER) over the period to

• The beekeeper shall not be responsible for the replacement of beehives injured by chemical poisoning or other damage after the bees have been placed on the property.

• The beekeeper has the right to remove his beehives after first notifying the grower if chemicals injurious to bees are to be applied to crops within the 1500 m flight range of the bees and to keep bees from the crop during the danger period without penalties under this agreement.

(2) The GROWER shall be entitled to inspect, or cause to be inspected by official government apiary inspector, each colony of bees after giving reasonable notice to the beekeeper of his intent over the period of the agreement.

(3) The BEEKEEPER agrees to maintain the bees in proper pollinating condition by judicious inspection and supering or removal of honey as needed.

(4) The GROWER agrees to provide suitable dry locations for the bees and to assume the responsibility of providing water to the bees. If there are no directions given as to a suitable location, the BEEKEEPER, according to his judgement shall place the hives in such a way as to ensure maximum pollination of the target crop.

(5) The GROWER agrees to pay $ rental per beehive colony for the duration of the contract. Payment shall be made to the BEEKEEPER as follows: $ on delivery and $ (the balance) being paid on or before (date). Additional moves or settings of beehives shall require $ per hive per move.

AND/OR the GROWER agrees to BEEKEEPER being entitled to % of the crop yield (based on expected yield increase through bee pollination)

(6) In the event of the GROWER not harvesting the crop, the expected yield shall be determined by an independent authority.

(7) In the event of crop failure after the bees have been brought to the crop through circumstances beyond the control of GROWER or BEEKEEPER, the GROWER agrees to pay the BEEKEEPER the agreed fee per hive.

(8) This agreement is not assignable or transferable by either the GROWER or BEEKEEPER.

Signed: BEEKEEPER (Date)

Signed: GROWER (Date)

Signed: WITNESS (Date)

(Justice of the Peace, Commissioner of Declarations)

Honeybee pollination of crops 23 Effectsof 5. rom a farmer's perspec- • avoiding contamination of control tive, the principal role non-target crops, flowering of crop pollination is to weeds (slash) and open water; pest optinnun fruit seed set ensure or timing to avoid and consequently the production • sprays methods on foraging bees; and of a high yielding, quality crop. pollination Because of this focus, any effect • applying pesticides by on beehives that are used will ground equipment rather only be of importance if current than aeroplane if foraging or future pollination is impaired. bees are present in the flower- P. Arming Production of a honey surplus is ing crop. largely inconsequential when the product of interest is the agricul- Timing is particularly critical. Spraying at night reduces kills by tural crop. 50 per cent and reduces the Successful modern agricul- hazard of the pesticide by one tural production results from a class. Fields need to be inspected high level of management before spraying during the day knowledge and control. to ensure bees are not actively foraging. Beekeepers and farm- ers rapidly learn that different crops are attractive at different times of day. For example, most cucurbits are pollinated in the morning, making morning spraying risky to bees. If highly toxic sprays need to be used, then the beekeeper should be advised early enough for hives to be moved from the crop until the hazard has passed. 5.2 Chemicals as 'magic bullets'

Dependence on chemicals for all pest control is a mistake. Other methods also have a role. For example, mosaic disease in Incorrect use of insecticides can cause 5.1 General principles massive losses of field bees and death of cucurbits is transmitted from hives, seriously affecting the beekeeper's infected crops by aphid vectors. livelihood Optimum pollination requires Spraying to kill the aphid is only that the farmer and the bee partially effective. Crop hygiene supplier both have good a is required, in this destroy- knowledge of and pesti- case pests ing diseased residues. cides. Communication between crop Reflective mulch to repel the both parties is essential. Farmers aphid is also useful. should involve beekeepers in planning a pest control program. Complete reliance on chemi- cal control often fails in the long Some key points in the pest term. For example, the cotton control program are: industry was effectively de- ▪ scouting for pests and target- stroyed in the Ord River Irriga- ing specific control methods; tion Area, Western Australia, by resistance to insecticides in boll choosing the least harmful • Similar increases in chemical and formulation for worm. resistance have occurred in during the pollination many use types of insects and diseases, for period; example, powdery mildew in cucurbits, potato moth in toma- toes and tobacco.

24 Honeybee pollination of crops Integrated pest management (IPM) • cannot be applied safely to toxicity and wide spectrum of flowering crops; pests affected makes it an impor- In the long term, systems of tant tool during bee pollination. integrated pest management • can be applied in late evening (IPM) offer the most sound basis after foraging; Organophosphates: A wide for successful production. variety of organophosphates crop • can be applied whenever bees are These that combine used in agriculture. Unlike are systems are not foraging; all the available forms of pest organochlorines, they persist be applied safely at suppression systematically to • can any only for a few days and do not lower pest populations safely, time. accumulate in body fat, economically and in an environ- Residual toxicity (RT) Organophosphates usually kill mentally acceptable way. Apart insects on contact but some are from chemical methods, biologi- The RT25 of a pesticide is the absorbed into the plant and cal control, cultural control and residual time required to bring travel through the sap-stream to plant resistance methods are the mortality of bees down to give systemic action against sap integrated. 25 per cent where bees are feeding insects. Their toxicity to exposed to field-weathered spray bees ranges from very high to For example, the citrus deposits. As a rule of thumb, low. Examples: dimethoate industry is benefiting from an chemicals with an RT25 of less (Rogor0), chlorpyrifos IPM program with reduced use than two hours can be consid- (LorsbanC), methamidophos of pesticides, lower costs, re- ered non-hazardous when bees (Nitofol0), methadithion duced risk of insects developing are not foraging (for example, (Supracide0), monocrotophos chemical resistance, less pesticide endosulfan). Those reaching (AzodrinC). residue in produce, less environ- RT25 within eight hours can be mental and health hazards, applied at dusk (for example, Carbamates: Carbamates, like encouragement of natural methomyl). When chemicals organophosphates, are short of enemies pests, less chance of with a longer RT25 are required, lived (a few days) and do not minor pests becoming major the bees should be removed or accumulate in body fat. Their ones and increased stability of confined for an appropriate toxicity to bees ranges from very the biological systems in or- period, high to very low. Examples: chards. methomyl (Lannate0), carbaryl Table 5 lists some pesticides (Carbary10), pirimicarb Departments of Agriculture and their hazard to honey bees (Pirimor0). Australia devel- in are active in and Table 6 provides an alpha- for oping IPM programs a range betic index of the common trade Pyrethroids: Pyrethroids are of perennial including crops names of the pesticides. Missing synthetic insecticides with strawberries, lychees and chemical related grapes, values indicate gaps in the structures to the pawpaws. At this stage there is current information. These plant extract, pyrethrum. Most limited vegetable progress in values are only guides, since household insect sprays contain crops. other factors can influence pyrethroids of types with low mammalian toxicity. Generally 5.3 Types of pesticides toxicities. For example, chemicals remain hazardous for longer pyrethroids are very toxic to periods at lower temperatures. bees, but they repel bees, so that Pesticides are classified in the effective toxicity in the field four broad roles insecticides, 5.3./ Main groups of insecticides is low. Examples: cypermethrin miticides, fungicides and herbi- (Ripcord®), permethrin (Am- There are four major chemical cides. The main class directly bush®), deltamethrin (Decis0). affecting bees is insecticides, groups of insecticides — organo- which is scarcely surprising. chlorines, organophosphates, Biological insecticides: In carbamates and pyrethroids. However, a small number from addition to chemical insecticides, the other poison bees. groups can Organochlorines: Most several biological insecticides are For example, the fungicide organo- chlorines persistent, now used. For example, strains pyrazophos (AfuganO) is are very of a with half lives of several in the bacterium Bacillus systemic organophosphate that years the environment. They also thuringiensis selectively control kills both adult bees and their accumulate in animal fat. Conse- several insect pests without larvae. The herbicide 2,4-D can quently, the majority banned bees, wildlife, fish or affect bees in chemical are some from in agriculture for beneficial insects. Long-term formulations. use — example, DDT, dieldrin, endrin, sustainable agriculture will rely on development of more alterna- Pesticides also chlordane. However, endosulfan can be put into tives to chemical insecticides. four classes in terms of their is an organochlorine without hazard to bees: these problems. Its relatively low

Honeybee pollination of crops 25 Table 5. Poisoning hazard of some pesticides to honey bees Source: Jones, W.A. and Holtkamp, R.H. (1991). Pesticides and bees. Northern Territory Department of Primary Industry and Fisheries: Agnote No. 485 (Agdex 481/681)

Bee toxicity Pesticide Trade names Pesticide RT25 Use Residual group (hours) class (hours)

acephate Orthene I >72 1 >72 aldicarb" Temik I 4 alpharnethrin* Dominex I 3 ametryn Primatol Z H 4 amitrole Amitrol-T, lAreedazol TL Plus H 3 azimethiphos Alfacron I 1 azinphos-ethyl Gusathion A, Kilathion, Cotnion-Ethyl I 1 azinphos-methyl Gusathion, Co-Thion I 61 1 24-120

Bacillus thuringiensis Delfin, Dipel, Thuricide, Biobit, Novosol I 4 bendiocarb Ficam I 1 >24 benomyl Benlate, Tersan F 4 bromoxynil Bromoxynil, Brominil, Buctril, Bromicide and H 4 various mixtures bupirimate Nimrod F 4

carbaryl Sevin, Carbaryl, Bugmaster and various mixtures I 70—>168 1 >168 carbofuran Furadan I 168—>336 1 168-336 chlorfetwinphos Birlane I 1 >24 chlorpyrifos Chlorpyrifos, Lorsban, Chlorfos, Dursban, Reldan, I >24 1 >24 Killmaster, Lawn Beetle Bombs, Fix Ants, Deter, Pyrinex chlorsulfuron Glean, Siege H clofentezine Apollo M copper compounds Copper, Copper Hydroxide, Copper Oxychloride, F Copper Curit, Bordeaux, Copudul, Cuprox, Oxydul, Kocide, Spectrum, Blue Mantel cyfiuthrin* Baythroid I 3 cyhalothrin* Grenade I 3 cypermethrin* Cymbush, Nurelle, Ripcord, Polytrin, Domirtex, I >72 3 Alphacord cyromazine Vetrazin, Vetrazine I 4

deltamethrin* Decis, Cislin I 3 demeton-S-methylt ivietasystox(I) I <2 3 0 diazinon Neocid, Gesa ,on, Diazinon, Nucidol, Amidaz, I 49 1 >24 Jetdip, Campitell Pennside Flowable Microencapsul- ated Insecticide dicamba Banvel, Dicamba H 3 dicofol Kelthane M <2 4 dimethoate Dimethoate, Perfekthion, Rogor, Saboteur, Roxion I 7—>72 1 72 diquat Reglone, Vegetrol, Watrol and various mixtures H 3 disulfoton" Disyston I <2 4 <2 diuron Dimon, Aguron, Diurex, Karmex, Di-on, Diugranz H 4

endosulfan Endosulfan, Thiodan, Endosan I <2-3 3 5

fenamiphos Nemacur N 1 fenitrothion Foliation, Fenitrothion, Fenitrogard, Sumithion I 1 24-120 fellation Lebaycid, Baytex I 1 48-72 fenvalerate* Sumicidin I 6 3 6 fluazifop Fusilade H 4 fluvalinate* Mavrik, Klartan I <2 3

glyphosate Glyphosate, Roundup, Zero, Comkil, Slain H 4

hexazinone Velpar H 4

iprodione Rovral 4 isofenphos Oftanol >24 1

lime sulphur Lime sulphur F 4

maldison Maldison, Malathion, Malathon, Hy-Mal, I 40 1 24-168 Brarthait M mancozeb Mancozeb, Dithane, Tatodust, Manzate F 3 MCPA MCPA, Thistle Killem and various mixtures H 4 metalaxyl Ridomil, Apron F 4

26 Honeybee pollination of crops Bee toxicity Pesticide Trade names Pesticide RT25 Use Residual group (hours) class (hours) methamidophos Monitor, Nitofol I 7-25 1 24 rnetlndathion Supracide I 24-80 1 72 rnethiocarb Baysol, Mesurol S 1 >72 methomyl Lannate, Nudrin, Marlin I 2 1 24 mevinphos Phosclrin I <5 1 24 monocrotophos Azodrin, Nuvacron, Monocron, Cronofos I >24 1 >24 omethoate Le-Mat, Folirnat 1 1 >24 oryzalin Surflan H 4 oxythioquinox Morestan M/F 4 0 paraquat Paraquat, Gramoxone, Spray Top, Robquat, Nuquat H 4 and various mixtures parathion Parathion, Folidol, Paramul I 20 1 >24 permethrin* Ambush, Coopex, Perigen, Byron D, Pythrin, I 14-42 3 Permasect petrolewn oil D-C-Tron, Spray Oil, Spraying Oil, White Oil, I 3 <3 Winter Oil, Summer Oil, Albarol, Lovis, Bryspray Oil No. 2 phorate** Thimet I 3 2-5 phosmet Imidan I >24 1 24-96 picloram Tordon and various mixtures H 4 pirimicarb Pirimor I <2 3 <2 promecarb Carbamult I 1 propargite Omite M <2 4 <3 propoxur Baygon, Blattanex I <2 4 propyzamide Kerb H 4 pyrazophos Afugan F 1 rotenone Derris dust, Rotomite and various mixtures I 3 simazine Simazine, Gesatop, Simatox, Simagranz H 3 and various mixtures sulphur Sulphur, Thiovit, Lansul, Elosal, Ktunulus, I/F 4 Brysulph, Le-Sulf sulprofos Helothion I 3 temephos Tempor, Abate, Atlas Mosquito Block I <2 3 3 tetradifon Tedion I <2 4 <2 thiodicarb Larvin I <2 3 thiometon Ekatin I 3 thiram Thiram, TMTD F 4 triadirnefon Bayleton F 4 trichlorfon Trichlorphon, Dipterex, Lepidex I 3 2-5 triclopyr GarIon H 4 trifluralin Treflan, Trifluralin, Triflurex, Tridan H 4 vamidothion Kilval 1 zineb Curit, Zineb 3 ziram Zirain, Fttlasin 3

2,4-11) 2,4-D and various mixtures 3 2,4,5-T 2,4,5-T mid various mixtures 4

*In laboratory tests pyrethroids have been classified as Use Class 1. However, repellency to bees has been shown in field trials and consequently bee mortality is lower than normally expected. Very toxic in glasshouse situations.

**Used in soils as granules, consequently bees not exposed to deposits.

1- This has caused the death of bees and should not be used when they are actively foraging. < Less than >Greater than

Pesticide group: Use class:

F = fimgicide 1. Cannot be applied safely to flowering crops. H = herbicide 2, Can be applied in late evening after foraging. insecticide 3. Can be applied whenever bees are not foraging M - miticide 4. Can be applied safely at any time. nematicide S = snail killer and bird repellent

Honeybee pollination of crops 27 Table 6. Common trade names of products

Trade name Active constituent Trade name Active constituent Trade name Active constituent

Abate ternephos Dirnethoate dimethoate Afugan pyrazophos Dipel Bacillus Malathion maldison Aguron diuron thuriligiensis Malathon maldison Albarol petroleum oil Dipterex trichlorfon Maldison maldison Alfacron azimethiphos Disyston diquat Mancozeb mancozeb Alphacord cypermethrin Disyston disulfoton Manzate mancozeb Ambush permethrin Dithane mancozeb Marlin methomyl Amidaz diazinon Diugranz diuron Mavrik fluvalinate Amitrol-T atnitrole Dim:ex diuron MCPA MCPA Apollo clofentezine Diuron diuron Mesurol methiocarb Apron metalaxyl Dominex alphamethrin Metasystox(I) demeton-S- Atlas Mosquito Block temephos Dorninex cypermethrin methyl Azodrin monocrotophos Dursban chlorpyrifos Monitor methamidophos Monocron monocrotophos Morestan oxythioquinox Banvel dicamba Ekatin thiometon Baygon propoxur Elosal sulphur Bayleton triadimefon Endosan endosulfan Nemacur fenamiphos Baysol methiocarb Endosulfan endosulfan Neocid diazinon Baytex fenthion Nimrod bupirirnate Baythroid cyflutluin Nitofol methamidophos Benlate benomyl Fenitrogard fenitrothion Nucidol diazinon Biobit Bacillus Fenitrothion fenitrothion Nudrin methomyl thuriligiensis Ficarn bendiocarb Nuquat paraquat Birlane chlorfenvinphos Fix Ants chlorpyrios f Nurelle cypermethrin Blattanex Fo lido l parathionhi Nuvacron monocrotophos propoxur Fo limat omethoate Blue Mantel copper corn- pound Folithion fenitrothion Fulasin ziram Oftanol isofenphos Bordeaux copper corn- pound Furadan carbofuran Omite propargite Branbait M maldison Fusilade fluazifop Orthene acephate Bromicide, brornoxynil Oxydul copper com- pound Brominil brornoxynil Garlon tridopyr Bromoxyrtil bromoxyn il Gesapon diazinon Bryspray Oil No. 2 petroleum oil Gesatop simazine Paramul parathion sulphur Brysulph Glean chlorsulfuron Paraquat paraquat Buctril brornoxynil Glyphosate glyphosphate Parathion parathion carbaryl Bugmaster Gramoxone paraquat Perfekth ion dimethoate Byron D permethrin Grenade cyhalothrin Perigen permethrin Gusathion A azinophos-ethyl Permasect permethrin Campbell Pennside diazinon Gusathion azinophos- Phosdrin mevinphos FlowableMicro- methyl Pirimor pirimicarb encapsulated Insecticide Polytrin cypermethrin Carbamult promecarb Primatol Z ametryn Helothion sulprofos Pyrinex chlorpyrifos Carbaryl carbaryl Hy -Mal maldison Chlorfos chlorpyrifos Pythrin permethrin Chlorpyrifos chlorpyrifos Cislin deltamethrin Imidan phosmet Reglone diquat Co-Thion azinophos- Reldan chlorpyrifos methyl Jetdip diazinon Ridomil metalaxyl Comkil glyphosphate Ripcord cypermethrin Coopex permethrin Robquat paraquat Copper copper coin- Kannex diuron Rogor ditnethoate pound Kelthane dicofol Rotomite rotenone Copper Curit copper corn- Kerb propyzamide Roundup glyphosphate pound Kilathion azinophos-ethyl Rovral iprodione Copper Hydroxide copper corn- Killmaster chlorpyrifos Roxion dimethoate pound Kilval vamidothion Copper Oxychloride copper corn- Klartan fluvalinate pound Saboteur dimethoate Kocide copper com- Copudul copper corn- pound Sevin carbaryl pound Kumulus sulphur Siege chlorsulfuron Cohtion-Ethyl azinophos-ethyl Simagranz sirnazine Cronofos monocrotophos Simatox simazine Cuprox copper corn- Larmate methomyl Simazine sirnazine pound Lansul sulphur Slam glyphosphate Curit zineb Larvin thiodicarb Spectrum copper corn- Cymbush cypermethrin Lawn Beetle Bombs chlorpyrifos pound Le-Mat omethoate Spray Oil, Spraying Oil petroleum oil Le-Sulf sulphur Spray Top oil paraquat D-C-Tron petroleum Lebaycid fenthion Sulphur sulphur Decis deltamethrin Lepidex trichlorfon Sumicidin fenvalerate Derris dust rotenone Lime sulphur lime sulphur Sumithion fenitrothion Deter chlorpyrifos Lorsban chlorpyrifos Summer Oil petroleum oil Di-on diuron LOViS petroleum oil Supracide methidathion Diazinon diazinon Surflan oryzalin Dicamba dicarnba

28 Honeybee pollination of crops 5.3.2 Formulations pests because of the delayed release of the insecticide from the The formulation of a pesticide capsule. Trade name Active constituent greatly influences its toxicity to bees. Unfortunately the capsules are a similar size to pollen grains Tatodust mancozeb Most toxic and they adhere to the body Tedion tetradifon Teknar Bacillus • dust and microencapulated hairs of foraging bees. The bees thitriligioisis insecticide, collect the capsules along with Temik aldicarb Tempor temephos pollen and store it in the hive. • wettable powder, Tersan benomyl They remain toxic in the comb Thimet phorate for months. When fed Thiodan endosulfan • ultra low volume (ULV) = many to Thiovit sulphur undiluted pesticide, developing larvae, the micro- Thiram thiram encapsulated insecticide kills Thistle Killem MCPA • emulsifiable and water them and the hive declines in Thuricide Bacillus soluble concentrates, flairingielisis strength. TMTD thiram • granules. Tordon picloram There appears to be no safe Treflan trifluralin toxic Trichlorphon trichlorfon Least way to use micro-encapsulated Tridan trifluralin pesticides where pollinating Trifluralin trifluralin Triflurex trifluralin 5.3.4 Mixtures of pesticides insects are required. Overseas trials where they have been used It is for farmers to Vegetrol diquat common on flowering crops have resulted Velpar hexazinone include a number of pesticides in in substantial honey bee losses. Vetrazin cyromazine a single spray application. Vetrazine cyromazine Usually an insecticide, a miticide 5.4 Effects of pesticides on and fungicide mixed. The bees Watrol diquat a are Weedazol TL Plus arnitrole obvious advantages are a single White Oil petroleum oil cost of application, speed and This is discussed in three Winter Oil petroleum oil convenience. sections, repulsion and attrac- tion, effects adult workers, Zero glyphosphate Rarely do chemical labels on Zineb zineb and effects on brood and queen. Ziram ziram indicate that this practice might alter the effect of any of the pesti- 5.4.1 Repulsion and attraction cides. Studies of the hazards of Pyrethroids repel bees; this certain insecticide formulations effect short lived but show that when miticides is serves to bees from this highly (including dicofol, tetradifon protect or toxic insecticide Bees propargite) added to insecti- group. are remain in the colony for cides, they greatly increase the a recov- period of less than 24 hours toxic hazard to bees. A similar ery after which foraging patterns increase in toxicity occurs when resume. acidifiers are added to an insecti- cide. Other insecticides also have effects foraging behaviour. This suggests that bee on more The organophosphate poisoning than may occur one methamidophos (Nitofol0) has would expect from the indi- a effect honeybee forag- vidual toxicities of pesticides in severe on and pollination efficiency. mixtures. ing This effect is believed to be due 5.3.5 Micro-encapsulated pesticides to intoxication with a sub-lethal dose rather than to repellent Pesticides be can encapsu- effects. Honeybee foraging the lated in tiny plastic capsules, on treated fields can be reduced for 30 to 50 in diameter. These ,Lin at least two days after spraying. micro-encapsulated pesticides are applied as a spray in the Most flowers have a maxi- usual manner and have a larger mum pollinating period of one to residual effect against insect two days. When the intended pollinators are repelled from the crop, these flowers are unlikely

Honeybee pollination of crops 29 to be adequately pollinated. may recover its strength in ideal • Field bees flying through Consequently a crop of inferior conditions in a month or more. aerial spray application while fruit may be produced. For However, for optimum pollina- foraging. example, bottle shaped tion, such hives need be cucum- to Field bees flying several bers would be expected. replaced immediately. • kilometres to attractive crops 5.4.3 Effects brood and such canola strawberry Lack of bees can lead to a on queen as or complete lack of pollination. For clover, which are sprayed Field bees can gather pollen without knowledge of the example, a generation of and nectar that is contaminated beekeeper. rockmelons can be lost, missing with pesticides at levels that are any planned marketing advan- not lethal to adults. The source of 5.6 Direct effects of tage. Later flowers will set contamination may be either pesticides plants further out from the of the on crown direct surface contact plant, usually off plastic or any contamination of nectar and There is evidence that mulch and in the drains between some pollen systemically, that is, pesticides can interfere with the rows. Here soil contact can lead through the sap stream. reproductive parts of the flower. to discolouratiort and disease if rain occurs. Bee larvae are killed by low The fungicides cupric hydrox- levels of contamination with ide, mancozeb and chlorothalonil Bees that have been repelled organophosphate insecticides, (Bravo®) reduce the percentage from a sprayed crop can learn to such as 2.5 ppm. Recovery of the of rockmelon pollen that germi- avoid the crop. If alternative hives is slow due to limited nates and the rate and length of pollen and nectar sources are foraging, disorientation and germ-tube elongation. Benomyl found to be attractive in more consumption of all food stores. (Benlate(D) has little effect. this period, future pollination of very There are major differences a crop will be compromised. between different organo- Similar effects on pollen 5.4.2 Effects on adult workers phosphates. Queens cease laying viability by some fungicides have after contamination with been recorded on apples, pears The effects of pesticides on methamidophos, and do not and pecan. Some fungicides adult workers the are most recommence for 52 days. damage the receptive stigmatic noticeable. If field bees come into surface of pecan. direct contact with very toxic Poisoning of brood and queen practical implications of pesticides, a pile of dead bees within the hive is not obvious to The will be found at each hive farmers. However, it is critical, this are to avoid spraying flowers entrance. Hives that have been since it can severely reduce the with particular fungicides. In the exposed to toxic pesticides effectiveness of pollination. case of rockmelons, where the become aggressive. effective pollination period is 5.5 How bees are 21 days or less, each day is Different pesticides produce accidentally poisoned critical. It is possible that some different symptoms in poisoned poor fruit set may be due to bees. Regurgitation of nectar The application of insecti- direct effects on the flower rather from the honey stomach is cides, particularly at flowering than effects on bees. mainly related to organo- times of is the most crops, 5.7 Poison hazards of phosphates. When a wet, sticky hazardous to bees. The following some mass of dead and dying bees is hazards are not so obvious. pesticides to honey bees found in front hives, on Drift of toxic dusts organophosphate poisoning is • sprays or The names of the recom- to adjoining usually implicated. Carbamates on crops or mended treatments are given in flowering weeds. cause bees to slow down and terms of standard common lose the ability to fly, becoming • Contamination of flowering names of the active constituents 'crawlers'. ground cover when crops are in registered proprietary prod- sprayed. ucts. This name is given on the Experienced farmers will label, usually near the propri- check in front of hives after • Insecticide dusts that adhere etary product name. spraying. If no freshly dead bees to foraging bees. The dusts are seen, the spray program is contaminate pollen and kill You must use only a regis- assumed to be non-damaging. the larvae during feeding. tered pesticide, and it must not Where large numbers of bees be used for in are • Insecticide contaminated any purpose or the killed the effectiveness of the water that bees collect. any manner contrary to colony as a pollinating unit is directions on the label unless a immediately reduced. The hive permit has been obtained.

30 Honeybee pollination of crops Further Pollination for profit. Pro- 6. • ceedings of a seminar held at inforrrtation_ the Frank Wise Institute of Tropical Agriculture Re- search, Kununurra — March 1992. • The economics of honey production and a pollination overview in Western Aus- tralia. Department of Agricul- ture, Perth, April 1992. • Pollination workshop. Hon- eybee Research and Develop- ment Council, Canberra, April 1992.

• Honeybee pollination — Technical data for potential crops in Western Australia. R. Manning, 1993, Depart- ment of Agriculture, Western Australia publication. • Bulletin 4159 'Beekeeping in Western Australia' by L. F. Allan, Senior Apiculturist and R.J.G. Manning, Research Officer, Department of Agriculture, Western Aus- tralia. • Honey production, economic value and geographical significance of apiary sites in Western Australia, R. Man- ning, Honeybee Reseach and Development Council, Canberra, September, 1992.

Honeybee pollination of crops 31 Glossaryof Allele: One of two or more forms Exo-skeleton: The thick cuticle 7. of a gene occupying the same of an insect that has the same technical locus on chromosomes that pair. strengthening function as the See also multiple allele. (endo-) skeleton of a mammal terms androecious: Male; androecium Fl hybrid: The first generation = the male parts of a flower, of offspring in a cross between the stamens two parental types (F1 = First filial generation); the first hybrid androgynous: Male and female Words in the definitions that offspring of given mating flowers in the flower a in italics defined same of genetically unlike are are cluster parents; the individuals are genetically andromonoecious: A plant with alike, which contrasts with male (stamina te) flowers and the second generation (F2), bisexual flowers in which each individual is different anther: pollen sac at the top of the stamen field workers: (or field bees) Older sterile female bees (workers) Brood: The young of the bee; that work from the hive, describes the eggs, larvae and away collecting nectar, pollen, pupae developing in an area of comb, usually in the lowest prop ohs and water; younger workers feed and care for brood, box of a hive — hence brood comb, brood box build and repair comb, and defend the colony Chromosome: Self-duplicating frame: A rectangular wooden rod-like structures in the cell frame that be removed nucleus that carry the genes can from the hive; the bees build in a linear arrangement comb within the frame, on a clone: A group of genetically wax sheet (comb foundation) identical individuals, resulting fitted into the frame by the from asexual or vegetative beekeeper reproduction, such as cuttings gametophyte: The haploid (with or tissue culture only one set of chromosomes) colony: All the bees inhabiting phase in the life cycle of plants a hive — queen, drones, workers that produces the gametes; in and brood flowering plants, abbreviated, being restricted to few cell comb: A double layer of wax a cells; in man-made hives, these divisions in the anthers and ovaries are built on a sheet of wax placed within a wooden frame; genotype: The genetic constitution hence brood comb — comb of an individual, in contrast containing young of the bees to its appearance (phenotype), cross-pollination: Transfer of pollen hence an individual described by its genetic constitution; from an anther of one plant a of individuals with to a stigma of another and group genetically different plant identical genetic constitutions for the characteristics under Dichogamy: Maturation of stamens consideration and stigma of a flower at glycogen: A carbohydrate storage different times, preventing self-se pollination; pollen shedding and in animals, glycogen is the in muscles receptivity of the stigma are energy source not synchronised gynoeciurn: The female parts of dioecious: Male and female flowers a flower — ovary, pistil are on separate plants; the gynomonoecious: A plant having plants are effectively unisexual bisexual and female (pistillate) flowers

32 Honeybee pollination of crops Heterogeneous variety: A plant Outcrossing: Crossing or pure line: A lineage of individuals variety in which individuals hybridising between genetically that are homozygous, obtained have different genetic different plants by successive self-fertilisation; constitutions; individual plants of individuals derived The part of the pistil that a group breed true (be homozygous) ovary: solely from may contains the ovules a common homozygous ancestor heterostylous: Having styles ovule: The structure in the fruit differing in length shape, Self-incompatibility: The inability or that contains the female gamete leading differences in the produce fruits with normal to (egg cell) and becomes the to transfer of pollen by insects seeds following self-pollination seed after fertilisation; one or heterozygous variety: Having more ovules are contained in self-pollination: The transfer of unlike genes for a particular the ovary that develops into pollen from an anther to a stigma characteristic—the individual the fruit of the same plant or clone plants do not breed true Parthenocarpic: The development sporophyte: The diploid (having hive: The structure housing a of a fruit without sexual two sets of chromosomes, one bee colony; or the colony itself fertilisation; hence usually from each parent) generation without fertile seeds in the life cycle of plant; homogeneous variety: Each plant a this of the life cycle is similar genetically, but photosynthate: The carbohydrate part may produces the be homozygous (true breeding) product of photosynthesis, spores or heterozygous (as in an Fl which is the conversion of light stamen; staminate: Stamens are variety) energy into chemical energy the pollen-producing structures in cells carbon dioxide in flowers, consisting of anthers homozygous variety: Having green — and in the presenceand filaments stalks; identical each of the water, or genes on sunlight, combined into staminate flowers male pairs of chromosomes —breeds are are carbohydrate, eventually flowers, having stamens but tnie for the characteristics under forming and starches functional female consideration; genetically sugars no parts pure in the plant stigma: The tip of the pistil, honey flow: A heavy flowering on pistil; pistillate: The female which pollen germinates of community of plants, a flowerroductiveof providing large quantities of rep organan a style: The slender stalk-like the style and stigma nectar for colonies placed - ovary, extension of the pistil between nearby by beekeepers pollen: The male gametophyte the stigma and the ovary; pollen generation of flowering plants; tubes through it reach hypopharangeal glands: Paired grow to dust-like bodies produced in the ovules glands in the head of bees; the withers, containing the male particularly well-developed The stories of hives, fertilising cells supers: upper in worker honeybees, in which usually containing only combs these glands produce brood pollen tube: An extension of the of honey and pollen; the bottom food and an enzyme that pollen grain following story or brood box usually converts sucrose (cane sugar) germination of the pollen grain contains the brood as well glucose and fructose the stigma. The tube carries to on Trimonoecious: Male, female and the male gametes (sperm) Incompatibility: A condition in bisexual flowers the throughplantthe stigma,thema down on same which otherwise normal pollen style, to the ovule grains unable to function are triploid: Having three sets of properly certain pistils propolis: Resin-like material from on chromosomes instead of the plants, collected b bees to Landrace: A variety that has p y usual two (diploid); most seal and repair hives evolved by natural selection triploid plants are sterile in agricultural system protandry: The anthers mature an Vector: The carrier of pollen from and shed pollen before the stigma Monoecious: Separate male and plant to another usually of the flower is receptive, one - female flowers the same insects, birds wind on same preventing self-pollination or plant Zygote: The single diploid cell rotogyybecomes: The stigma multiple allele: of three p n g ma (having two sets of one or receptive beforee forms of occupyingchromosomes)an formed by the more a gene mature and shed pollen in the single locus chromosome fusion of the haploid and a on a flower, encouraging egg same cross- (having set of Nectar: Sugary solution produced pollination sperm one chromosomes each). The by plants, usually in the flowers; zygote divides produce the embryo transformed by bees into honey to

Honeybee pollination of crops 33 8. Index A agents of pollination 10 hazards - poison 30 agreements - pollination 22 heath 14 armonas 9, 10 hemp 9 apiary sites 18 hives-inspecting 15 apples 10, 12, 19, 30 hives- location in crop 12, 18 asparagus 9 hives - migration 17 attractiveness of the food 11 hives - number per hectare 10 avocado 9, 10 hives - pollination 15 hives - rent level 17 hives - strength 16 honey - composition 14 bananas 7, 8 honey bees - crawlers 30 bats 10 honeybees-dead 30 bee hives. (See hives) honey bees - effects of pesticides 29 bees. (See honey bees) honey bees - feral 5 berseem clover 20 honey bees - flight distance 12 birds 10 honey bees - food requirements 14 Brassica species 8, 9 honey bees - food selection 11 honey bees - orientation 12 honey bees - robbing 15 hops 9 canola 14 hybrid seed crops 5, 9 carbamates 25 hybrid vigour 8 cashews 5, 8, 9, 10 citrus 25 clover 19, 20 cocoa 9, 10 incidental pollination 5 coconuts 9 information - further 31 colour of flowers 11 insecticides 25 cotton 12 insects 10 crawlers 30 inspecting hives 15 crop isolation 20 integrated pest management 25 cross-pollination 8 inter-planting 10, 19 cucumbers 7, 20, 29 IPM 25 cucurbits 7, 8, 9, 20, 24 irrigation 12 isolation distance 21 isolation of crops 20

Darwin, Charles 8 date palms 9 dead bees 30 kiwi fruit 14, 20 definitions 32 Ktuntrturra 5, 10, 24 dichogamy 9 dioecy 9 distance between crops 21 distance to competitor food sources 12 lucerne 12 lychees 9, 25

effective pollination period 10 effects of pesticides on bees 29 macadamia 9, 10 EPP 10 maize 8, 9, 10 eucalypts 14 male sterility 9 mangoes 5, 8, 9 mangosteen 7 melons 7, 10 Fl hybrid seed 5, 8, 9 micro-encapsulated pesticides 29 feral honey bees 5 migration 17 fire 18 migratory beekeeping 6 flight distance 12 mixtures of pesticides 29 flower colour 11 monoecy 9 flower odour 12 food requirements of bees 14 food selection by honey bees 11 formulation of a pesticide 25 nectar - abundance 11 nectar - attractiveness 11 nectar - sugar concentration 11, 12 nectar - sugar concentration 10 glossary 32 nectar - sugar content 11 grapes 25 nectar sources 14

34 Honeybee pollination of crops sunflowers 5, 10, 14 sweet potato 9 odour of flowers 12 oil palm 9 onion 8, 9, 10 9 Ord River. (See Kummurra) taro 20 organochorines 25 temperature time of control 24 organophosphates 25 pest 10 orientation 12, 18 tomato toxicity of pesticides 25 outcrossing 8 8 outcrossing mechanisms 8 tree crops types of pesticides 25

9, 20, 25 pawpaws ultra-violet peaches 10 11 pears 14, 19, 20, 30 peas 8 pecan 30 water 18 pest control effects pollination 24 — on watermelons 5, 19 pest control timing 24 — weather conditions 12 pesticide drift 18 weeds 14 pesticide formulations 25 wheat 8 pesticide mixtures 29 white clover 19 pesticides micro-encapsulated 29 — wind 10, 13, 18 pesticides — poison hazards 30 pesticides — types 25 poison hazards 30 pollen composition 14 — zizyphus 9 pollen sources 14 pollinating agents 10 pollination 7 pollination — affected by pest control 24 pollination — incidental 5 pollination agreements 22 pollination benefits 12 pollination hives 15 pollination industry at KimumuTa 5 pollination management 10 pollination mode 7 pollination services — notice for 6 pumpkins 5, 7, 10, 15 pyrethroids 25

rain 10 rent level 17 residual toxicity 25 rice 8 robbing 15 rockmelons 5, 10, 20, 29, 30 row patterns 19 RT25 25

S locus 9 sapodillas 9 selection of apiary sites 18 self-incompatibility 9 self-pollination 8 sex expression 7 shade 18 sorghum 8, 10 spinach 9 squashes 7 strawberries 9, 25 sugar concentration 11, 12 sugar content of nectar 10 sugar types 11 sugarcane 8 1126-3713/9/93-5600

Honeybee pollination of crops 35 Print Post approved PP 665002/00030