FAR Foundation ForFOCUSFOCUS Arable Research Issue 07 November 2012

ISSUE Pollination 7

• The process of pollination • Honey bee biology and behaviour • Obtaining and managing honey bee colonies for pollination • /crop management • • Towards diversifying pollinators in crop fields

® ADDING VALUE TO THE BUSINESS OF ARABLE FARMING™ Introduction Pollination is the movement of pollen from the anthers of a flower to the stigma of the same or a different flower. Pollination is one of the most important parts of the economic production of many crops. However, it is often the most poorly understood and least likely to be optimised. In some cases, it is not managed at all and growers just trust there will be enough bees or other in the vicinity of the crop to ensure that pollination occurs. Even if beehives are introduced for pollination, their performance may not be optimised and the levels of pollination may not be measured. For many crops, obtaining optimised and reliable pollination may be one of the best ways of improving the economics of the production of the crop.

The aim of this manual is to provide growers, beekeepers, and pollination specialists with the information necessary to optimise the pollination of -pollinated commercial crops. The manual begins (Section 1) with a description of the process of pollination, including a summary of the species involved. Honey bee biology and behaviour is described in Section 2. Section 3 covers issues around obtaining and managing honey bees for pollination. In Section 4, management strategies to protect honey bees are outlined while Section 5 covers specific issues related to pollination of a range of crops. Section 6 looks at other pollinating insects such as native bees, bumble bees and flies.

This report has been prepared by The New Zealand Institute for Disclaimer & Food Research Limited (Plant & Food Research), which Unless agreed otherwise, The New Zealand Institute for Plant & has its Head Office at 120 Mt Albert Rd, Mt Albert, Auckland. Food Research Limited does not give any prediction, warranty or assurance in relation to the accuracy of or fitness for any particular This report has been approved by: use or application of, any information or scientific or other result contained in this report. Neither Plant & Food Research nor any Mark Goodwin of its employees shall be liable for any cost (including legal costs), Scientist/Researcher, Pollination and Apiculture claim, liability, loss, damage, injury or the like, which may be Date: 24 June 2011 suffered or incurred as a direct or indirect result of the reliance by any person on any information contained in this report. Stuart Tustin Science Group Leader, Crop & Fruit Production Systems Limited protection Date: 24 June 2011 This report may be reproduced in full, but not in part, without prior consent of the author or of the Chief Executive Officer, The New Zealand Institute for Plant & Food Research Ltd, Private Bag 92169, Victoria Street West, Auckland 1142, New Zealand.

2 FAR Focus 7 Crop Pollination

Contents

1. The process of pollination...... 2 4. Orchard/crop management...... 30 • 1.1 Flower parts • 4.1 Conditions within the orchard • 1.2 Self and cross pollination • 4.2 • 1.3 Vectors for pollen movement • 4.3 Surfactants • 1.4 Bee species • 4.4 Removing beehives before spraying • 4.5 Mowing grass 2. Honey bee biology and behaviour.... 10 • 4.6 Beekeeper/grower co-operation • 2.1 Feral honey bee colonies • 2.2 Beehives 5. Crops 34 • 2.3 Honey bee castes • 5.1 Buckwheat • 2.4 Stinging • 5.2 Carrots • 2.5 Swarming • 5.3 Field beans and Broad beans (Vicia Faba) • 2.6 Varroa • 5.4 Linseed • 2.7 Honey bee foraging • 5.5 , Birdsfoot - trefoil • 5.6 Lucerne () 3. Obtaining and managing honey • 5.7 Oil Seed Rape bee colonies for pollination...... 17 • 5.8 Radishes • 3.1 Obtaining hives • 5.9 Red • 3.2 Colony strengths • 5.10 White clover • 3.3 Queens • 3.4 Swarming 6. Towards diversifying pollinators • 3.5 Identifying problems with in crop fields...... 41 colonies - auditing • 6.1 Value of pollinator diversity • 3.6 Managing colonies • 6.2 Towards increasing pollinator diversity • 3.7 Sugar syrup feeding within crops • 3.8 Robbing • 3.9 Pollen trapping and feeding Appendix...... 47 • 3.10 Attracting honey bees to flowers • 3.11 Honey bee stocking rates

© Foundation for Arable Research (FAR) DISCLAIMER This publication is copyright to the Foundation for Arable Research and may not be reproduced or copied in any form whatsoever without written permission. This FAR Focus is intended to provide accurate and adequate information relating to the subject matters contained in it. It has been prepared and made available to all persons and entities strictly on the basis that FAR, its researchers and authors are fully excluded from any liability for damages arising out of any reliance in part or in full upon any of the information for any purpose. No endorsement of named products is intended nor is any criticism of other alternative, but unnamed product. 1. The process of pollination

1.1 Flower parts 1.2 Self and cross pollination 1.3 Vectors for pollen movement 1.4 Bee species 1.1 Flower parts To gain the best understanding of the information provided in this manual, it is necessary to have an understanding of the names of different parts of flowers, their appearance and function.

The flower parts are (Figure 1): • Sepals that enclose the flower buds. They open and fold back so the petals can open.

• Petals that enclose the reproductive Stigma structures. In insect pollinated flowers, these are usually coloured and conspicuous to attract insect visitors. Anther The petals usually have to open before Pistil pollination can occur.

• Anthers that produce the pollen. Anthers are usually at the end of a Filament filament. An anther and its filament are Ovary referred to as a stamen. The anthers must open or split to release the pollen. Petal

• Pollen grains contain the male genetic Sepal material that must be moved to the female reproductive structures.

• Stigmas, which are at the end of a pistil, are the female structures on which the pollen must be deposited.

• The ovary is normally at the base of a flower and contains from one to more than 1000 ovules.

• Ovules are the female structures that must be fertilised to produce seeds.

• Nectaries produce to attract animal flower visitors. These are usually situated at the base of the petals. Figure 1. Diagram of a generic insect pollinated flower.

Seeds and fruit are expensive for a plant to produce, pollen grain wall (germination) and grow through the while few resources are required to produce a pollen stigma tissue to reach the ovule. The pollen tube then grain. For this reason, usually produce relatively combines with an ovule to create a seed (fertilisation). few ovules compared to the number of pollen grains they produce. There may be millions of pollen grains For pollination to occur, all of these things must happen. produced for each ovule. For the production of a commercial crop it needs to happen reliably and often. To produce a seed, pollen must be moved from an anther to the stigma of a compatible flower that Over millions of years, plants have evolved complex is capable of setting seed. To start the process, relationships with the agents that move the pollen to the anthers must open or split to expose the pollen their stigma. For most plants, these systems work (dehiscence), and the pollen must then be transported sufficiently well to ensure enough seeds are produced while it is still alive. for the survival of the species. However, the pollination of plants grown commercially can be much more Depending on the plant species, the pollen may have difficult. Often, humans have selected plants without to be moved a few millimetres or many metres. Once reference to their pollination systems. This can be on the stigma the pollen tube must break through the seen in hybrid seed production in radishes. For a

The process of pollination 3 normal radish flower, pollen only has to be moved a Natural selection of plants has favoured the transfer few millimetres to reach a stigma on an adjacent flower. of genetic material between different plants (out- However, to produce hybrid radish seeds, the pollen crossing) to maximise the species’ ability to cope with may have to be moved several metres to another plant. variations in its environment. Although plants requiring Plants are also often now grown in places where the out-crossing are the most common, many plants are pollinators they have evolved with are not present. completely self fertile. Further complicating matters, plants are also now forced to grow in a different manner to how they would As well as plants that are completely self fertile and grow in their natural environments. For example, kiwifruit plants that require out-crossing, some plants are partly is a vine that climbs trees in its natural environment in self fertile. They can produce seeds by themselves forests in China; however, commercially it is grown on but will produce more if they are cross pollinated e.g. structures that are less than 2 m tall. strawberries.

In their natural environment plants often grow in relatively small patches or as isolated plants. There are usually 1.3 Vectors for pollen sufficient pollinators in these natural ecosystems to movement ensure they are pollinated. However, commercial crops are usually grown in large , sometimes There are a large variety of vectors in natural kilometres in extent. In such situations there are usually ecosystems that carry pollen between flowers, too few natural pollinators in the vicinity of the crop to including wind, water, insects, birds, bats, and reptiles. ensure all the flowers are pollinated.

In their natural ecosystems, the plants may also not need to have every ovule fertilised to produce enough seeds to ensure survival of the species. However, we often now require these plants to have much higher seed set to produce a commercially viable crop. 1.2 Self and cross pollination systems form two basic patterns, out- crossing and self pollination.

1. Self pollination is where a flower produces pollen and fertilises itself or other flowers on the same plant. An example of this is can be seen in the pea that is completely self fertile. The pollen is placed on the stigma before the flower opens. Some self-fertile plants may still need an agent to move pollen from the anthers to the stigma, e.g. tomatoes.

Self pollination is often the aim of breeding programmes as it eliminates pollination problems.

2. Out-crossing is the opposite of self pollination. The plant has a mechanism to decrease the chance that self pollination will occur and to increase the chance that pollen will come from another plant. There are a number of mechanisms plants use to achieve this:

• Male and female flowers on different parts of a plant, e.g. chestnuts and maize.

• Male and female flowers on different plants e.g. kiwifruit.

• Flowers that are female at one time and male at a different time e.g. avocado.

• Flowers that are male and female at the same time but the pollen is unable to pollinate flowers on the same plant e.g. white clover.

• Flowers that are male and female at the same time but the pollen is unable to pollinate flowers on the Figure 2. Maize showing male flowers and corn cobs. same variety e.g. nashi.

4 The process of pollination

Figure 3. Anthers on a maize flower liberating pollen. Figure 4. Stigmas on a maize flower.

However, the following discussion only deals with Maize plants (Figure 2) are a good example of a wind the common vectors that are significant for commercial pollinated plant. The male flowers are produced at the crops in New Zealand. These are wind, birds, flies and top of the plant where the pollen produced has the bees. greatest chance of being blown by the wind. The petals are unscented and inconspicuous. The female flowers, 1.3.1 Wind attached to what will later be the corn cob, are lower Many plants have evolved to use wind to carry their down and have inconspicuous petals without scent pollen from an anther to a stigma. The most well known or nectar. wind pollinated plants are the grasses, which include The anthers produce copious amounts of pollen ryegrass, wheat, barley, maize and rice. Gymnosperms because few of the pollen grains will reach a stigma. (cone bearing trees, conifers) are also wind pollinated. The pollen can be usually seen if the male flowers are Allergies to the pollen of wind pollinated plants are the knocked (Figure 3). cause of fever in many people. Pine trees produce so much pollen at times that it can look like smoke in The stigma of the female flowers are very long and pine plantations and can be seen accumulating along have small branches (Figure 4) on them so they have the sides of roads. a large surface area to maximise the chance they will intercept a pollen grain floating past. Wind pollinated plants typically have a range of basic characteristics. These are: Wind pollinated plants will occasionally be visited by insects collecting pollen. Honey bees collect pollen • Light pollen that can be blown for large distances. from maize flowers and accumulations of pine pollen • Anthers that are held higher than the stigma so the when they cannot get pollen from other sources. pollen can be blown further. However, this does not aid pollination of these plants. • Large stigma to catch pollen out of an airstream. 1.3.2 Animals • Inconspicuous flowers. Animal pollinated flowers are usually conspicuous and often large. They are usually scented and produce • Flowers that are unscented. pollen grains that are heavy and at times sticky so they will stick to animal flower visitors. • Flowers that do not produce nectar.

The process of pollination The process of pollination 5 Figure 5. A silvereye drinking Figure 6. A fly collecting nectar Figure 7. Bee on a cherry flower. nectar from a peach flower. from an almond flower.

Although many commercial crops are completely 1.3.5 Bees wind pollinated and others animal pollinated, some Various bee species contribute to pollination worldwide. appear to be both wind pollinated and insect Of these only honey bees, cutter bees, alkali bees, pollinated. Kiwifruit are an example of this. and bumble bees are managed to any extent for pollination. Most managed insect pollination is carried Kiwifruit have large conspicuously coloured flowers out by honey bees (Figure 7), while the others are usually that produce scent. Female flowers also produce only used for specific crops like tomatoes (bumble bees) non-viable pollen to attract insects that feed off and Alfalfa (alkali bees and leaf cutter bees), where they pollen. These are characteristics of insect pollinated are more efficient pollinators than honey bees. flowers. However, the flowers have many of the attributes of a wind pollinated flower as well. The male vines produce large numbers of flowers with copious 1.4 Bee species amounts of pollen. The flowers hang downwards to allow the pollen to fall out of the flower and, in their Various bee species in New Zealand contribute to natural environment, the vines climb trees so when pollination. Some of these bees are managed, such as the pollen is released into the air it can travel large honey bees, bumble bees, leafcutter bees and alkali distances. The pollen is dry and carried in the air to bees. Other bee species also contribute to pollination such an extent that much of the pollination carried but are not currently managed to any extent. This group out in Italy is by orchardists blowing pollen from male includes native solitary bees. to female flowers with large fans. The stigmas of the Although unmanaged bees will at times contribute female flowers are large and fleshy, which increases to pollination, their value is limited because their their ability to collect pollen out of the airstream. presence cannot usually be guaranteed. Because 1.3.3 Birds their pollination cannot be guaranteed, growers usually need to introduce honey bees at the same Birds visit flowers of a range of commercial crops to stocking rates that they would have done if the collect nectar and hence carry out some pollination unmanaged bees were not present. (Figure 5). They tend to be less efficient than bees. 1.4.1 Honey bees Some flowers are, however, designed to be pollinated by birds, e.g. feijoas. Feijoa flowers have sepals with There are a number of species of honey bee worldwide. a high sugar content. Birds pull off the sepals and in The (Apis mellifera) is the most doing so shake pollen onto the stigma and transfer it commonly managed bee for pollination and honey to other flowers. production in temperate countries. The Asian bee (Apis ceranae) is managed in some tropical countries but they 1.3.4 Flies usually produce smaller colonies and they are generally Flies are important pollinators of some commercial more difficult to manage. The Asian bee is not present crops such as onions, and contribute to the pollination in New Zealand. of many crops as they are attracted to the same Honey bees are the most important insect pollinators flower rewards that bees are attracted to (Figure 6). of cultivated crops worldwide (Figure 8). While some Nashi (Asian pears) appear to have evolved to use insects visit the flowers of only a small number of plant flies. Although they have similar flowers to European species, honey bees are generalist foragers. They will pears, nashi flowers smell like rotten meat, which visit almost any flower from which they can harvest attracts flies. nectar or pollen.

6 The process of pollination Several of the bumble bee species have become very common in New Zealand and can be observed in most during the summer. They are frequent visitors to many flowering crops in New Zealand.

Lifecycle New bumble bee queens are produced and mated in the autumn. They overwinter and start nests in the spring. The nests are usually built in the ground, often in abandoned mouse and rat nests. The queen builds the first wax cells, , lays eggs, feeds the developing larvae, and keeps the nest warm. As the queen has to do all the work initially, the first workers produced are small and poorly fed. When there are enough workers, the queen stays in the nest while the workers and look after the developing larvae. When mature, a colony may have up to 200 bees. New queens and male bees are produced in the autumn, and the colony, Figure 8. Honey bee colonies introduced for carrot workers and male bees then die leaving the new pollination. queens to over winter.

Because of their life cycle, feral (unmanaged) colonies Honey bees are one of the few pollinating insects that are not present in the winter. In the spring, they only can be managed. They can be delivered to a crop have a single queen. They reach their maximum when required, will start foraging almost immediately population and foraging force in early summer after and can be removed when required. Because they many commercial crops have finished flowering. produce large colonies that are present throughout the year, honey bees can usually be sourced irrespective Bumble bees forage for both nectar and pollen as do of when a crop flowers. There are also various honey bees. They will visit most of the flowers that honey management options available to influence the honey bees visit. Because the colonies are much smaller than bees’ flower visiting behaviour. honey bee colonies, they collect much less pollen. They collect even less nectar because, unlike honey Unlike the other managed insect pollinators, honey bees have uses other than the pollination services they provide. Beekeepers can harvest and sell honey, pollen, wax, royal jelly, venom and propolis. The bees themselves can also be harvested and sold. A hive may also be used for the pollination of more than one crop. In New Zealand, a beehive might be used to pollinate apples, then avocados and finally kiwifruit. After that, it will collect a honey crop. In the autumn, a kilogram of bees might be removed from the hive and exported. Beekeepers therefore do not usually have to recoup the complete yearly costs of managing honey bee colonies from the return they receive from supplying them for pollination of a single crop. This makes them more economic to use for pollination than other managed pollinators, where the pollination fee must cover the complete yearly cost of managing them. 1.4.2 Bumble bees Four species of bumble bee were brought to New Zealand from England in two introductions, in 1885 and 1906. (Figure 9).

The species are:

• The large earth bumble bee (Bombus terrestris).

• The large garden bumble bee (Bombus ruderatus).

• The small garden bumble bees (Bombus hortorum).

• The short haired bumble bee (Bombus Figure 9. A queen bumble bee visiting an almond subterraneous). flower.

The process of pollination The process of pollination 7 are almost exclusively used for glasshouse pollination, mainly for tomatoes. They are not used for other crops because, despite being better pollinators than honey bees, they are usually too expensive.

Although bumble bees have been shown to be efficient pollinators of a range of crops their use is generally restricted to the pollination of high value crops like glass house tomatoes because of their high cost.

Purchasing bumble bee colonies Bumble bee colonies can be purchased. Once ordered they are delivered by courier with instructions for Figure 10. Commercially 10. Commercially reared bumble bee colony. reared bumble bee colony. their care. The nests contain a queen and about 200 workers. They will survive for up to 3 months. They can be sourced at any time of the year. bees, they do not store it during the winter. A strong bumble colony will therefore visit only a small number Feral bumble bee colonies It is possible to encourage feral bumble bee queens to of flowers compared with a strong honey bee colony. establish nests near crops. Bumble bees will occupy Bombus terrestris colonies are produced commercially artificial hives that are placed in appropriate locations in many countries including New Zealand (Figure 10). near a crop. These usually consist of wooden or This allows colonies to be produced through the year concrete boxes placed on the surface of the ground and to be moved into a crop when needed. or slightly below ground depending on the bumble species of interest. However, only a proportion of Advantages/disadvantages nesting boxes will be occupied each year. Bumble bees have several attributes that make them better pollinators than honey bees: Because bumble bees only store relatively small amounts of nectar compared with honey bees, they • They will forage in more marginal conditions than must forage on most days. In many parts of New honey bees so are less affected by adverse weather. Zealand there are a large enough number of species of flowering plants to ensure that they can find food • Bumble bees, particularly the larger ones like B. throughout the spring, summer and autumn. If there terrestris, are more likely to touch the stigma of is not a good supply of flowers throughout this time, flowers. planting plants that flower at the appropriate times may • They have a behavioural trait called buzz pollination. increase the success of feral colonies. Bumble bees vibrate their wing muscles while visiting flowers, which increases the amount of 1.4.3 Leafcutter bees pollen they can extract from some plant species. Leafcutter bees (Figure 11) are managed in for lucerne pollination. They are better • T h e y m o r e e a s i l y a d a p t t o f o r a g i n g i n g l a s s h o u s e s a n d pollinators of lucerne than honey bees. They were tunnel houses. introduced into New Zealand in 1971 but did not prove successful here, possibly because the weather was • Some bumble bee species have long tongues and not suitable. In 1984, the population of leafcutter bees can reach the nectar of flowers that honey bees was estimated to be about 5 million. In 2009 it was cannot easily reach. estimated that there were less than 100,000. • They are less aggressive than honey bees. Lifecycle Bumble bees also have disadvantages compared with Leafcutter bees overwinter as pupae inside their cells. honey bees: As temperatures rise in the spring, they emerge and mate. The females then build tunnels which they line • Their colonies are small, often less than 200 with cut pieces of leaf — thus their name. They lay bumble bees compared with up to 60,000 honey eggs in these cells and supply the developing larvae bee workers in a colony. with nectar and pollen. The larva pupates and then either emerges as an adult, if it is early in the season, • They are relatively expensive. This is because honey or stays as a pupa and overwinters if it is late in the bees are generally easier to manage than bumble season. bees, and will collect a crop of honey, which in part subsidises the cost of providing them for pollination. A full description of how to manage leafcutter bees can be found in “Leafcutting bee life history allocation Large numbers of artificially reared bumble bee details and management techniques”, written by DEC colonies are used for pollination in New Zealand. They Read and BJ Donovan.

8 The process of pollination overwinter as pupa in the nesting holes and emerge in the spring. They mate on emergence. The females then excavate new holes in which they lay eggs. They then forage for pollen and nectar to provision the cells. Their life cycle ends in late summer when the adult females die.

Solitary bees may contribute to the pollination of a crop because of the proximity of their nesting sites. There is the potential for developing some of the bee species as managed pollinators in the future.

Figure 11. A leafcutter bee.

1.4.4 Alkali bees Like the leaf cutter bee, the alkali bee is important for lucerne pollination. Alkali bees were introduced to New Zealand in 1971. They are a ground nesting bee that prefers that has a high salt concentration. They are of similar size to honey bees. They emerge from the nesting site in early summer, mate and form new Figure 12. A New Zealand native solitary bee tunnels in which they rear new bees. They collect pollen (Leioproctus species) on an onion flower. and nectar to feed the developing larvae. The bees forage from December to March so are unavailable to crops that flower early in the spring, but their life cycle does coincide with lucerne flowering.

Alkali bees will inhabit man-made nest sites. The nest site may need to be protected with a roof in high rainfall areas as rain can drown nests.

There have not been any recent surveys of the alkali bee populations in New Zealand so their current distribution, numbers and importance for pollination are unknown.

Alkali bees have been observed in Canterbury, Central Otago, Marlborough in the South Island and Manunui in the North Island. There is a viable population in a man-made site in the Wairau Valley2.

A full description on how to establish alkali bees at a site and manage them can be found in “Alkali bee establishment and maintenance for lucerne pollination”, written by BJ Donovan and DEC Read. 1.4.5 Native New Zealand bees There are many native solitary bee species in New Zealand (Figure 12). Although each female bee builds a separate nest which consists of a hole in a bank or the ground there are usually a large number of other individuals nesting at the same site so it looks like a colony. However none of the nesting holes join together and the females all act as individuals. They bees

The process of pollination The process of pollination 9 2. Honey bee biology and behaviour

2.1 Feral honey bee colonies 2.2 Beehives 2.3 Honey bee castes 2.4 Stinging 2.5 Swarming 2.6 Varroa 2.7 Honey bee foraging

10 Honey bee biology and behaviour Western honey bees are managed in almost all countries. They are kept in areas where their hives are covered by snow in the winter and in high temperatures in the tropics. This ability to survive extremes of temperature is a function of the way the bees manage the internal temperature of their hive and their food reserves, rather than because of human assistance. Because of this, they can be imported and used for pollination almost anywhere a crop is grown.

Most honey bee colonies are managed; however, they also live as feral colonies.

2.1 Feral honey bee colonies Figure 13 a. Beehives.

Feral honey bee colonies live in cavities in trees, caves, buildings, and other man-made structures. They are usually smaller than managed colonies, swarm more often, and are often more aggressive. They can be long lived but in most countries, including New Zealand, the presence of the varroa bee mite has meant that feral colonies can survive for only one or two years. The first record of the varroa bee mite in New Zealand was in Auckland in 2000. It has now killed most feral colonies in New Zealand.

Feral colonies can add significantly to pollination if there are enough of them present but there are problems associated with relying on them for pollination. It is Figure 13 b. Removing a frame from a beehive. difficult to assess whether there are enough feral colonies in the vicinity to pollinate a crop until after the crop has started flowering. At that stage, it may be too late to introduce managed colonies if there are 2.3.1 Queen too few feral colonies. Feral colonies also cannot be Queen bees are reproductive females. There is usually manipulated to improve their pollination in the way only one queen in a hive. She will often live for two that managed colonies can. Better and more reliable or three years, although many beekeepers replace pollination can usually be achieved by introducing queens yearly. The queen lays all the eggs needed to managed colonies. produce the other castes of bees. She can lay over 1000 eggs in a day. The queen will usually only leave Better and more reliable pollination can usually be the hive on her mating flight, if the colony swarms, and achieved by introducing managed colonies rather then finally when she dies. If a queen dies and the than relying on feral honey bee colonies. colony or beekeeper cannot replace her, the colony will also eventually die.

2.2 Beehives A beehive (Figure 13 a) is the man-made structure that a managed honey bee colony lives in. It usually consists of a floorboard that the boxes sit on, one or more boxes and a hive lid. There are usually between six and 12 frames (Figure 13 b) inside each box. The frames carry the honey comb, developing larvae, pollen, and honey stores. Beehives will also often contain a feeder so that the beekeeper can feed the colony sugar syrup if they do not have enough stored honey. 2.3 Honey bee castes A honey bee colony usually consists of three castes of bees - a queen (Figure 14), drones and many thousands of workers.

Figure 14. Honey bee queen.

Honey bee biology and behaviour Honey bee biology and behaviour 11 Beekeepers replace queens by removing or killing the summer when it is very active or six months during the old queen and either releasing a new queen from a winter. cage or installing a queen cell containing a queen that is about to emerge. The new queen will start laying When the queen lays a worker egg (Figure 16 a) it takes soon after she is released. If the old queen is replaced three days to hatch into a larva. The larva (Figure 16 b) with a new queen, there should be little interruption with is fed by the workers for the next four days. The cell is egg laying. However, if the old queen is replaced with capped over and the larva spins a cocoon. The larva a queen cell, it may take several weeks for the queen turns into a pupa under the capping (Figure 16 c). This to emerge, mate and start laying, which will slow down cannot be seen unless the cell capping is removed. the development of the hive. In this case there may be The fully formed worker bee emerges from its cell 21 times when there are no larvae in the colony, which will days after the egg is laid (Figure 16 d). reduce the amount of pollen the colony collects.

For this reason, beekeepers should not replace queens with queen cells when the hives are introduced to a crop for pollination as it may cause an interruption in brood rearing and reduce pollen collection.

Beekeepers should not re-queen colonies with cells while the hives are being used for pollination of crops requiring pollen collectors as there will be a break in the brood cycle. a b 2.3.2 Drones A drone is a male bee (Figure 15). The drone’s only function is to mate with a queen when it goes on its mating flight. They are only present in the hive in the spring, summer and autumn. The workers evict the drones in the autumn. As they do not visit flowers and cannot feed themselves, the drones starve. They have no role in pollination. c d

Figure 16. Development of a honey bee showing (a). egg, (b) larva, (c) pupa with the cell capping removed, (d) Bee emerging from its cell.

In the spring, summer and autumn, a colony will normally consist of all three castes of bees and all stages of developing bees including eggs, larvae, pupae and fully formed bees. In temperate countries, they are normally at their maximum population in the late summer. However, they can be managed to have large population sizes at other times of the year. Figure 15. Drone (male) honey bee. Workers forage for water, propolis, pollen and nectar.

Water is collected to cool the hive and to dilute the 2.3.3 Workers honey that is fed to larvae. Bees prefer to collect water (Figure 17) that has an odour. For that reason, they are Worker bees are non reproductive females. There may often attracted to chlorinated swimming pools and be more than 60,000 workers in a very large honey bee muddy puddles. A honey bee colony will die if there is colony. Everything done in and outside the beehive, no water available, but this is usually not a problem in except laying eggs, is done by the worker bees. This New Zealand. Because bees like contaminated water, includes making wax, building comb, feeding larvae, care needs to be taken when spray tanks are washed keeping the hive clean and warm, defending the hive out as honey bees may be attracted to the washings. and foraging. The jobs they do depend in part on their age. They start carrying out tasks inside their hive and Propolis is sap that is collected from trees. Workers are referred to as house bees. They then graduate use it to fill any holes and gaps in the outside of to guard bees that defend the colony, and lastly to the beehive that the bees do not want to use as an foragers. A worker may live for only six weeks in the entrance (Figure 18). They also use it to block any gaps

12 Honey bee biology and behaviour Figure 17. A honey bee collecting water. Figure 18. Propolis in a beehive. The propolis is the orange material at the end of the black frames.

Figure 19. A nectar forager sampling a flower with its Figure 20. A pollen forager scrabbling across the top tongue. of the anthers.

inside the hive that are too small for the bees to move with pollen, which they then brush off and pack into the through. Propolis is harvested from some beehives pollen baskets on their back legs. and sold as a human health product. While some bees visit flowers to collect only nectar Nectar is collected from flowers and provides the or only pollen, many bees will collect both pollen and carbohydrate that the colony needs. Bees will usually nectar on the same foraging trip. collect as much nectar as they can. What they don’t use they convert into honey and store for times when there is none available. The nectar and honey is eaten 2.4 Stinging by adult bees and fed to larvae. If there is no nectar It must always be remembered that honey bees are available and a colony runs out of honey, it will die not domesticated. All we do is provide them with a within a few days. suitable nesting site and encourage them to stay. If they consider a person or other animal a threat to their A nectar forager can be identified because it probes colony, they may attack them. When they sting, it is flowers with its tongue (Figure 19). generally in defence of their colony. Pollen is collected by worker bees to provide the Their propensity to sting depends on a number of minerals, vitamins and protein needed by a larva to factors; one of which is their race. The least aggressive develop into an adult bee. A colony can survive for strains may only consider a person to be a threat if they months without pollen but they will stop producing place their fingers in the entrance of their hive but other brood. Bees collect pollen by scrabbling across the strains may attack anybody within 20 m. anthers of a flower (Figure 20). Their bodies gets coated

Honey bee biology and behaviour Honey bee biology and behaviour 13 Beekeepers often select strains of bees with reduced aggression However, colonies placed in crops for pollination may range from very docile to very aggressive so all colonies should be treated with caution. Even the more docile bees can be provoked to attack by loud noises, bumping hives, or opening hives without a smoker. Honey bees are also very sensitive to weather. On a pleasant sunny afternoon when the colony is collecting nectar, it may be quite docile. However, the same colony may be aggressive in the early morning, evening or during bad weather when its bees cannot forage.

All honey bee colonies should be treated with caution. Figure 21. Blowing smoke into the front of a hive.

Bees are very aggressive at night. Although the bees will not usually fly at night unless you shine a light on The following are the symptoms of a serious reaction: the hive, they will crawl. Even the most docile colony in daylight will only have one thought at night, which is • Severe rapid swelling around the sting site but to sting whoever is disturbing them. Bees will also extending to other areas (e.g., around eyes, lips and usually be more aggressive on the day they are moved general puffiness of face). into a crop. • General rash. Bees will sting if they become caught in clothing, or hair, which may happen if you are standing in their flight • Breathing difficulty, choking sensation, asthma, lips path. If caught in hair, the bee needs to be removed, turning blue. and killed as quickly as possible as they will usually • Vomiting. sting if not removed. • Collapse and loss of consciousness. To minimise the chance of being stung: As these symptoms can lead to death, administer oral • Don’t stand in the colony’s flight path. antihistamines if possible and get the person medical • Don’t open, knock or interfere with the beehive. assistance as soon as possible. When summoning assistance it is important to stress the urgency of the • Avoid mowing close to hives. situation.

• If you need to work close to hives talk to the It is good practice to check with staff and anyone else beekeeper first. working in the crop during the time the hives are there for pollination to see if they are allergic to bee venom. The aggressiveness of a colony can be temporarily If they are allergic, they should seek medical advice as reduced using the same method that a beekeeper there is a chance that they may be stung. uses. This is by blowing smoke into the hive entrance (Figure 21). As the colony has to be approached closely before doing this, the beekeeper should be consulted 2.5 Swarming beforehand. The beekeeper might also be able to provide protective clothing and a smoker. Honey bees swarm as a normal part of their colony’s reproductive cycle (Figure 22). The colony produces People’s reactions to stings vary considerably. The a new queen to head the colony while the old queen sting should be removed as soon as possible. This is with half the bees to form a new colony. This best done by scraping the sting out with a fingernail. usually happens in spring when the colony is collecting Squeezing the sack on the bee sting will not increase small amounts of nectar. A colony may also swarm if the amount of venom injected. For most people, the it runs out of space in its hive. A colony can swarm only effect of a sting is a sharp pain and possibly some several times in a season. localised swelling. Localised swelling is usually not a life threatening problem unless you are stung on the throat The swarm will usually hang from a tree or other object or tongue. However, more generalised symptoms can within 100 m of the parent colony and stay there while be more serious. bees from the swarm hunt for a suitable cavity. The swarm may stay in the same place for a few hours The symptoms generally appear within a few minutes, through to several weeks. If a swarm cannot find a but in some cases may be delayed for as long as suitable cavity to occupy, it may set up home where it is 24 hours. hanging, build comb and rear larvae. In warm climates, these colonies may survive the winter.

14 Honey bee biology and behaviour to control them, which has resulted in higher hive losses and increasing costs in maintaining hive numbers and providing pollination services. 2.7 Honey bee foraging 2.7.1 Flower utilisation by colonies Honey bees are very efficient at exploiting the flowers surrounding their hive. Most bees forage within a 1 km radius of their hive but they will fly in excess of 5 km to exploit a very rich patch of flowers. A colony may therefore have a foraging range of more than 70 square kilometres.

The workers from a colony are consistently sampling Figure 22. Honey bee swarm on a traffic sign. the flowers within the colony’s foraging range and moving the colony’s foraging effort to the most attractive flowers. When a colony is moved to a crop, its When a swarm leaves its parent hive, the workers bees usually forage on flowers from the crop as these gorge themselves with honey hence for the first few are the first ones found. However, if the colony can find days are usually docile and unlikely to sting people. more rewarding flowers, it may move its foragers from However, the swarm can become aggressive if it the crop onto these new flowers. has been present for a longer time and has begun to The attractiveness of a group of flowers depends on get hungry. a number of factors. These include the distance the Bees from a swarm will visit flowers for nectar. However, bees have to fly to reach it, the number and density of as they have nowhere to store the nectar they will flowers, the amount and attractiveness of pollen, the collect much less nectar than a similar sized colony. amount and the sugar concentration of the nectar, and They do not normally collect pollen as they have no what the colony requires. larvae to feed. Because of this, swarming is usually Competing flowers can be a major problem for some detrimental for pollination. The beekeeper should be crops. Honey bee colonies may be introduced to the asked to replace any hive that swarms. crop in very high densities but if the flowers are not Beekeepers can usually minimise swarming by very attractive and there are large numbers of more ensuring colonies have spare room in their hive and attractive flowers surrounding the crop, the bees may that the queen is less than one year old. Some strains desert the crop completely. of bees are more likely than others to swarm. 2.7.2 Timing of foraging If you check flowers of a crop at different times of day, Colonies that swarm while being used for pollination you’ll find large variations in the number of honey bees should be replaced. visiting flowers. This is because of variations in the time of day that pollen and nectar are produced by the If a swarm has landed in an inconvenient location, a flowers. If honey bees are not foraging at a particular beekeeper will be needed to remove it. If they are not time of day it is usually because there is no pollen or causing problems they can be left alone and will usually nectar available rather than that the bees are ignoring fly away after a few days. the reward the flowers are offering.

If bees are not visiting a crop at a particular time of 2.6 Varroa day this is most likely to be because the flowers are Unfortunately, any discussion of honey bee biology not offering a reward at that time. would not be complete without including varroa. Varroa is a mite that evolved on Apis cerana where it infests drone brood. Some time before 1940 varroa jumped 2.7.3 Weather and foraging species onto the Western honey bee that had been Honey bees will not usually readily forage below 15°C. introduced into Asia. It has spread since then to almost However, for most plants, cold weather will stop flowers all countries, and can be found in all beehives in New producing pollen and nectar before it will stop bees Zealand. If colonies are not treated with miticides twice from flying to visit flowers. Honey bees do not forage a year, varroa will usually kill them. This has added in heavy rain. significantly to the cost of keeping bees, and much of this cost has been added onto the cost of providing 2.7.4 Effect of colony size hives for pollination. In most countries, varroa have For a colony to survive, its workers must look after developed increasing resistance to the chemicals used the larvae in the hive and forage for nectar, pollen and

Honey bee biology and behaviour Honey bee biology and behaviour 15 water. Up to a certain size, the colony has to manage these competing demands on the worker bees. The more larvae they have to feed, the more pollen and nectar they need to collect. However, as the number of bees in a colony increases there will be more worker bees than is required for the colony to meet its daily demand for nectar and pollen. These surplus bees will devote their time to collecting nectar, which will be turned into honey to be stored for the winter. For this reason, beekeepers normally want their colonies to have as many workers as possible when they are using them to collect a honey crop.

The makeup of a colony therefore has a large effect on what the worker bees collect. The more brood in a colony, the more pollen the bees will collect. However, as the ratio of bees to brood increases, the amount of nectar a colony will collect increases. 2.7.5 Floral constancy Individual honey bees normally exhibit floral constancy while foraging. In a paddock of clover and dandelions, some bees will visit all clover flowers while other bees will visit all dandelion flowers. Very few will visit flowers of two different species during the same foraging trip. According to the famous naturalist Charles Darwin, this behaviour enhances pollination as it reduces the chance of pollen being carried to the wrong flower species. However, the behaviour can have a negative effect on crop pollination. Artificial selection to develop a plant species into a commercial crop often produces male flowers that look significantly different (in the eyes of the honey bee), from the female flowers to which the pollen needs to be moved. This may limit the amount of movement between the flowers if bees start to treat the different sexes of flowers as though they are different species; which is an issue in some hybrid carrot and radish varieties. 2.7.6 Foraging areas Rather than foraging randomly over a patch of flowers, individual honey bees tend to have foraging areas. These are groups of flowers from the same plant species that a bee will come back to on successive foraging trips. The size of these foraging areas depends on the density of flowers and the amount of nectar and pollen per flower. These foraging areas are reached by the bees flying over the crop rather than by visiting flowers on the way. Foraging areas are an important consideration because they affect the movement of bees in a crop and the likelihood that a bee will encounter a pollinizer.

16 Honey bee biology and behaviour 3. Obtaining and managing honey bee colonies for pollination

3.1 Obtaining hives 3.2 Colony strengths 3.3 Queens 3.4 Swarming 3.5 Identifying problems with colonies - auditing 3.6 Managing colonies 3.7 Sugar syrup feeding 3.8 Robbing 3.9 Pollen trapping and feeding 3.10 Attracting honey bees to flowers 3.11 Honey bee stocking rates

Honey bee biology and behaviour Obtaining and managing honey bee colonies for pollination 17 3.1 Obtaining hives It may take a beekeeper a large amount of time to prepare colonies suitable for pollination, especially if There are three methods of obtaining managed honey they are required early in spring. In many cases, some bee colonies for pollination; growers who own their own of the preparation work carried out by beekeepers has hives, hives placed for free for harvesting honey, and to occur during the previous autumn. It is therefore hives that are hired from a commercial beekeeper. usually important to order hives early to ensure supply. 3.1.1 Grower owned hives When hiring honey bee colonies, many beekeepers and Some growers are also beekeepers who use their own growers find it preferable to use a pollination contract hives to pollinate their crop, often to reduce costs or that specifies the responsibilities of both parties. ensure availability. This can work well, as long as care is Contracts are useful as there is no confusion over taken to ensure that the colonies are large enough when what the grower thinks they are hiring and what the the crop flowers. It is usually important to move colonies beekeeper thinks they need to supply. They become into the crop when it flowers rather than having them very important if there are any problems with what is permanently sited next to the crop (see section 3.6.1; supplied and what happens to the hives once they are ‘Moving colonies’). There are many examples where the in the crop. A typical contract may specify: decision of growers to buy hives and manage them have • Names and addresses of the parties concerned ended in failure. This is because the skills required for and the date of the agreement. growing crops and keeping bees are very different. The hives often get neglected in favour of growing the crop, • Location of the crop. from which the grower’s income is derived. Because of this, most growers who take up beekeeping to provide • Number of colonies hired. hives for pollination do not continue with it. • Strength of colonies (number of frames of brood There are examples where growers buying and and bees). managing colonies have proved successful. Most • Distribution of hives throughout the crop. are successful because the grower has employed a beekeeper to manage the colonies. • Length of notice to be given before shifting bees in and out of the crop. 3.1.2 Free hives Some beekeepers place hives in a crop for free because • Rental fees and terms of payment. the crop will allow the hives to produce a honey crop, • Any special management practices such as sugar e.g. white clover. Although the grower has no direct syrup feeding. costs, there are significant risks in using free pollination services as the grower will have little or no control over • An arbitrator in the event of a dispute. the size of the colonies that are introduced, how many are introduced, or how they are managed. • Permission for an independent audit of the strength of the colonies. Feral colonies or managed colonies on permanent sites in the surrounding area are also occasionally relied on • Action to be taken if an audit is failed. to provide a free pollination service. The risk with this approach is that their numbers may vary from year to • Remedial action to be taken if problems occur. year. They are also likely to be at a distance from the • Protection from spray damage. crop, which will decrease the number of bees from the hives visiting the crop unless the crop is particularly • Witness to the agreement. attractive. As they are permanently situated, fewer of their bees will visit the crop than from colonies that are An example of a generic pollination contract is introduced for pollination. This is because at the time presented in Appendix 1. the crop flowers, the bees from permanently sited hives will already be foraging on flowers elsewhere. These 3.1.5 Rental fees bees will usually not move onto the newly foraging crop The cost of hiring a honey bee colony will depend on unless is very attractive. a number of factors. The most significant of these are the opportunity costs. This relates to the amount of Varroa has all but eliminated feral colonies in New money the beekeeper could make from the hives if they Zealand, so reliance on feral colonies alone is no longer were not used for pollination. If the hives can collect a viable option. as much honey while they are used for pollination as they could anywhere else, there may be no opportunity 3.1.4 Hiring hives cost. A good example of this is clover seed crops Hiring hives is the most common solution for obtaining where beekeepers put hives near the crop, often free managed hives needed for pollination. Hives are usually of charge, because of the honey crop they can collect. hired directly from beekeepers or from agents working However, for kiwifruit, most beekeepers have to forgo a for beekeepers. This approach has the advantage that honey crop when they introduce hives; this is reflected the growers can specify exactly what they require. in the cost of renting colonies. If honey prices increase,

18 Obtaining and managing honey bee colonies for pollination the average cost of renting colonies for kiwifruit has beekeeping experience as well as experience with pollination is likely to rise accordingly. the crop.

Also affecting the rental prices is any hive management needed to get colonies to a particular strength, the 3.2 Colony strengths distance they need to be transported, any special It is tempting to think of hives as the wooden boxes that management required while the hives are in the crop, the colonies are housed in. A lot of thought is usually and any damage that they suffer through use. given to the number of these wooden boxes that will Factors that affect the cost of managing colonies be hired as this is what pollination fees are calculated outside pollination time may also affect prices. When on and they are easy to count. Less thought is given varroa was found in New Zealand, beekeepers’ costs by growers to the strength (amount of brood and the significantly increased because of treatment costs. number of bees) of the colonies. However, the strength Because of this, the cost of hiring hives for kiwifruit of the colonies used is usually much more important pollination almost doubled. than the number of beehives. A large colony may collect more than 100 times more pollen and nectar As with any product or service, supply and demand is than small colony. There is therefore little point in also a significant driver for hive rental prices. talking about beehive numbers without also specifying the size of colony. 3.1.6 Finding beekeepers If using honey bees for the first time, growers will need The strength of a colony is influenced by a number to contact a beekeeper. The easiest way of doing this of factors. In temperate climates, colonies are usually is to talk to other growers in the area who are using at their smallest during winter. They grow in strength hives. Alternatively, the internet will provide contact through the spring and summer and are at their peak information on beekeeper organisations that can size in late summer and early autumn. Honey bee provide details of local beekeepers that may be willing colonies can sometimes have large numbers of bees to provide pollination services. but no brood (larvae and pupae), if there is no queen or there is a new queen that has yet to start laying. Pollination associations and agents However, brood cannot survive without worker bees to Beekeepers sometimes establish pollination feed it and keep it warm. Because worker honey bees associations. These associations take up a wide range collect pollen to feed their larvae, colonies without of functions. Some meet only to discuss issues of brood will collect little pollen. Colonies will not naturally common interest. Others work together to educate have large amounts of brood and few bees. members, provide quality assurance programmes for their members’ hives, co-ordinate advertising and It is sometimes possible for a beekeeper to produce some also act as agents for the placement of hives in large colonies outside this annual cycle by feeding crops and the collection of pollination fees. pollen and sugar to the bees. Beekeepers can also influence the size of colonies by adding or removing In some larger growing industries, there are people frames of bees and brood. who act as agents for pollination hives. They organise the rental of hives for growers and often have some When introducing hives for pollination it is important arrangements with beekeepers to guarantee quality. to specify the size of the colonies as well as the The beekeeper will usually deliver the hives into a single number of hives. location (dump site) and the agent will then arrange their delivery to the crop. The size of colonies used for pollination are often Agents provide several advantages for beekeepers and described as the number of frames covered with bees growers. When committing large numbers of hives to a and brood. This is complicated by the variation that particular crop, it is a very complicated logistical issue occurs in the sizes of frames. The most common frame for beekeepers to deal with a large number of growers, size in New Zealand is the ‘Langstroth’ full depth frame. pick up hives from widely distributed sites, and position However, there are also frames used that are ¾ and ½ them in crops at night. They also need to be checking this size. colonies for strength before moving them and carrying out any management required while the hives are in the Their surface areas (one side) are: orchard. Using an agent means that the beekeeper just has to check colony strengths and deliver the hives to Langstroth - Full depth 23.8 x 46.5 (11,000 cm2) the dump site. ¾ depth 18.5 x 46.5 (860 cm2) ½ depth 13.3 x 46.5 (681 cm2) Agents can be of use to growers as well. Discussing the strength of colonies and colony management The following discussion assumes that Langstroth full requirements with a beekeeper often develops into a depth frames are being used, as these are the most very technical discussion on honey bees in which a common. The measurements will need to be converted grower may soon find themselves out of their depth. if a beekeeper is supplying hives with different frame These discussions can be left for an agent who usually measurements (see above).

Obtaining and managing honey bee colonies for pollination Obtaining and managing honey bee colonies for pollination 19 When discussing the size of colonies it is worthwhile to specify the following. 3.2.1 Amount of brood Even if bees are only needed to collect nectar from a crop, colonies should still have brood. The presence of brood ensures colonies will function normally, and that new bees will be emerging to replace any that die. The amount of brood (eggs, larvae and capped cells containing pupae) is usually measured as the number of frames of brood present in a hive. Usually, frames will not be completely full of brood (Figure 23). For this reason, the number of the frames of brood in a hive is usually discussed as the full frame equivalents, i.e. the Figure 23. A honey bee frame 60% covered with number of frames that would be completely full if the brood (the area of brown cells on the bottom half of areas of brood on each frame were added together. the frame). For instance, a colony of six frames that are 60% full of brood will have 3.6 full frame equivalents.

When the brood area is being checked, the beekeeper or auditor will normally count the number of frames with brood and estimate the proportion of each frame that is covered with brood. The proportions are added together to determine the total amount of brood. 3.2.2 Age of brood The age of brood can also be specified if it is important Figure 24. A frame with an area of white larvae. that the colony collects large amounts of pollen. The more unsealed cells with larvae that are still being fed, the more pollen a colony will collect. A typical specification is that the colony should have at least 25% of the brood as unsealed larvae (Figure 24). 3.2.3 Position of brood If it is important that bees collect pollen, then most of the brood should be as close to the hive entrance as possible, as this encourages the foraging bees to collect more pollen. If the colony is housed in two boxes this can be achieved by having the brood in the bottom box. 3.2.4 Bee numbers

It is usual to specify the number of frames completely Figure 25. A frame covered with bees. covered with bees. In a normally functioning colony, there will be a greater number of frames of bees than brood. A colony may have between 1 and 20 or more frames of bees. A full depth frame of bees completely covered with bees (Figure 25) would have about 3,000 as the workers will fill up the cells the queen wants to adult bees. There should be enough bees on the lay in if they have no other room. Enough empty comb frames so that the honey comb below the bees cannot should be available to allow the queen to continue be easily seen. laying while the colonies are in the crop and to store the nectar the colony collects. 3.2.5 Empty comb It is common to specify the amount of empty comb, Enough empty comb should be present to store especially if the colonies are going to be in the crop any nectar or sugar syrup collected. for more than two weeks. If there is not enough empty comb for the queen to lay in, the area of brood will reduce. This will limit the amount of pollen collected 3.2.6 Honey stores and eventually reduce the number of bees in the hive. Colonies should have enough stored honey so they This is particularly a problem if a colony is collecting do not starve while in the crop if there is little nectar large amounts of nectar or is being fed sugar syrup, available.

20 Obtaining and managing honey bee colonies for pollination 3.3 Queens be taken before any problems start to affect pollination. Alternatively, it may be possible to have the hives Each colony needs to have a queen. It may be useful to audited before they are introduced to the crop. specify the age of the queen. Young queens tend to lay more eggs than older ones. A colony with a queen that is less than one year old will normally grow faster and Audits should occur as soon as possible after the have a larger demand for pollen than a colony headed hives are introduced to the crop. by an older queen. Older queens are also more likely to swarm. Audits may take a variety of forms depending on the reason why the audit is being carried out. 3.4 Swarming 3.5.1 Audits to a standard Hives should not be overcrowded with workers as they This consists of determining whether colonies meet a may swarm. The colonies should be managed so they specified standard. The results are usually reported as do not swarm while they are being used for pollination. the percentage of hives that meet or fail the standard. This may consist of adding an extra box of empty comb, No credit is given in the audit to colonies that are ensuring the colony is headed by a young queen or significantly over the standard. The method has the removing queen cells regularly. advantage that it is easy to carry out and for everyone to understand. 3.5 Identifying problems with 3.5.2 Average strengths colonies — auditing In this method the average number of frames of bees, brood, empty comb in each hive is determined. This Having specified a particular standard for the hives that approach has the advantage that it more clearly reflects are being hired, it is often important to check the hives the pollinating potential of the colonies and that the to ensure that they meet the required standard. beekeeper gets credit for any strong colonies provided, It is usually not possible to determine the strength of which may compensate for any weak colonies. colonies by observing the number of bees entering and leaving hives as this is affected by factors in addition to 3.5.3 Problem hives the size of the colony. If there is little nectar or pollen for This is where colonies that do not have as much activity the colonies to collect or the weather is not suitable for at their entrance are audited to determine if there is a the bees, there may be few bees flying. Even standing problem with them. close to the hives may confuse the bees and reduce the number of bees entering the hive. However, if some hives have large numbers of bees entering and leaving 3.6 Managing colonies and others do not, this may indicate a problem. 3.6.1 Moving colonies The best way of determining if the colonies supplied Colonies are normally moved into a crop at night to meet the required standard is to have a beekeeper ensure that all the foraging bees are in their hives when open and inspect them. If there is a written contract they are moved. or a verbal agreement with a beekeeper that specifies some or all of the above then it is possible to have the Bees have good memories so they can find their way hives audited by an independent person to ensure they back to their hive. For this reason, if a beekeeper is fulfil the requirements. It is usual to gain permission going to move a hive it must be moved more than 3 from the beekeeper before having the hives audited. km. If a hive is moved a shorter distance, the foragers An audit may consist of checking some or all of the may recognise where they are and return to the location hives or just the hives that are causing some concern. where the hive has been moved from. Colonies should therefore not be moved within a crop once the bees have started to forage. If colonies need to be moved If you think there is a problem with the hives, get within a crop, they should be removed completely from them audited. the crop and new colonies brought in and placed in the new location. In some instances, a beekeeper will open and go through any hives with a grower. Alternatively, with Colonies should not be moved within a crop. sufficient training and the appropriate permission from the beekeeper, growers can do their own auditing. The most common arrangement is for an independent When hives are moved from a crop, bees are likely to beekeeper to carry out the audit. In some industries, be left behind, even if the hives are moved in the middle hive auditors advertise their services. of the night. These bees will usually settle in small bunches that look like very small swarms. If they are Any audit should take place as soon as possible after not in the way, they can be left and will eventually die. the hives are placed in a crop so remedial action can If they are a problem, the beekeeper should be asked

Obtaining and managing honey bee colonies for pollination Obtaining and managing honey bee colonies for pollination 21 to remove them or to provide advice on how they can be removed. 3.6.2 Situating colonies within a crop Distance from the crop Although bees can fly large distances (>5 km) if the need arises, they usually only fly as far as required to collect the pollen and nectar they need. The number of bees from a hive visiting a crop often decreases with increasing distance to the crop. This trend is more pronounced during bad weather when bees are even more likely to forage close to their hive. Colonies therefore should be as close (< 20 m) to the crop as possible. If the crop is very large, hives may need to be Figure 26. Honey bees placed in a carrot crop. placed amongst the crop (Figure 26).

Place the hives close to (within 20 m) the crop.

Distribution within the crop The distribution of honey bee colonies within a crop is often a controversial issue between growers and beekeepers. This is because it is easiest for the beekeeper to drop off all the hives in a single or several large groups (Figure 27). However, many growers want the hives spread evenly throughout the crop with the hope that there will be an even distribution of bees through the crop.

There is no simple answer to whether hives should Figure 27. A large group of beehives in a kiwifruit be placed in one or several large groups or spread orchard.

70

60

50

40

30 Bees per flowers 1000 20

10

0 0 50 100 150 200 250

Distance (m)

Figure 28. Number of bees on kiwifruit flowers with increasing distance from a group of beehives.

22 Obtaining and managing honey bee colonies for pollination evenly through the crop. If hives are spread evenly in foraging on kiwifruit was because kiwifruit flowers do throughout a crop, the foraging bees on the crop not normally produce pollen till after 9 am. will tend to spread themselves evenly throughout the crop. However, the same may not occur if hives are Place colonies in a warm, sunny situation. placed in large groups. If the density of hives is high enough that there is pressure on the supply pollen and nectar available in the crop, bees from large groups of hives should spread themselves evenly over the crop. 3.7 Sugar syrup feeding However, if there is more pollen or nectar than the bees can collect, they will tend to forage close to their hives Feeding sugar syrup to colonies (Figure 29) is a simple as this requires the least energy. In this situation, there way of increasing the amount of pollen collected by a will be a high density of bees close to a large group of colony. This is usually done for crops that have flowers hives and the bee density on flowers will decrease with that produce only pollen e.g. kiwifruit or for crops increasing distance from the hives. where pollen foragers are better pollinators than nectar foragers, e.g. apples, pears and almonds. The results This was seen in a kiwifruit orchard where hives were of syrup feeding can be dramatic. Colonies fed sugar introduced into a 10 ha orchard in three large groups of syrup typically collect two to three times as much 30 hives. A large decline in the number of bees visiting kiwifruit pollen as unfed colonies, making them two to flowers was observed with increasing distance from three times more valuable pollinators4. these hives (Figure 28). Why syrup feeding should increase pollen collection is Another example of this is where the pollination of not entirely clear. It has been suggested that it causes squash was reported to decrease from a group of 20 bees that have been collecting nectar to change to beehives at the end of a field3. gathering pollen. When a nectar collecting bee returns with its load, it passes it to the house bees waiting just In summary, for some crops, and in other crops in inside the hive entrance. The house bees then store the some years, large groups of beehives will produce nectar in cells to make honey. an even distribution of bees over the crop. However, irrespective of the crop or the year, single or small When sugar syrup is fed to a colony the house groups of hives distributed throughout or around the bees consume the sugar syrup instead of waiting crop are more likely to result in an even distribution of at the hive entrance. As there are fewer house bees bees on the crop. available to accept nectar loads, the nectar collectors have to wait longer to get rid of their load. This is Because of this, hives should not be placed in large thought to discourage bees from collecting nectar so groups unless research or experience has shown they collect pollen instead. that large groups give suitable pollination for the crop. Group sizes should be limited to a maximum of Because syrup feeding works by changing honey bee four hives. behaviour rather than simply by increasing the food supplies, it works regardless of how much honey the Put a maximum of four hives in each group unless colony has stored. Sugar syrup feeding has been it has been demonstrated that larger group sizes shown to increase pollen collection from almonds, will also give an even distribution of bees. sweet cherry, field beans, red clover and kiwifruit.

It is important to remember that the beekeeper will have to drive around the crop in the dark to find the proposed hive sites. It is usually a good idea to provide the beekeeper with a map of the proposed hive locations with ditches, low wires or other hazards clearly marked on it.

Position It is good practice to place colonies in as warm a situation as possible. This will encourage the bees to forage in marginal conditions. The placement of the hives in front of a windbreak where the colonies will get early sun is best. Avoid windy locations.

There is no need to take this to its extremes, however. It was noted that bees do not visit kiwifruit flowers till 9 or 10 am. Growers tried to encourage bees to forage earlier by placing hives on packing crates so they were a metre above the ground where it was warmer. However this made no difference as the delay Figure 29. Feeding a colony sugar syrup.

Obtaining and managing honey bee colonies for pollination Obtaining and managing honey bee colonies for pollination 23 It has been suggested that feeding sugar syrup scented Where hives are fed sugar syrup by the growers or with flowers of the target crop can be beneficial. their staff, it is important that they are protected from However, there is insufficient evidence that this practice bee stings with appropriate clothing and show no is any better than feeding unscented syrup to be able major allergic reaction to being stung. This should be to recommend it. arranged with the beekeeper.

Although dramatic increases in pollen collection have been observed, the effect of syrup feeding on Wear protective clothing when feeding sugar syrup pollination is unknown because of the difficulty in to avoid being stung. collecting this type of data. It has been assumed that in order to collect more pollen, the bees from a colony The sugar syrup must be fed inside the hive rather than must either visit more flowers, or visit them to collect outside. The method is unlikely to work if the syrup is pollen instead of nectar, both of which should increase fed outside and it may provoke robbing (see below). pollination for most plants.

3.7.1 Feeding colonies Only feed sugar syrup to bees inside their hive. The feeding of honey bee colonies needs to be organised with the beekeeper, usually well before 3.7.2 Types of feeders the hives are introduced as the beekeeper will need to ensure that the colonies have sugar Both division board feeders (Figure 30) and top feeders feeders fitted (see below). The beekeeper will also (Figure 31) work equally well. Top feeders sit on top of need to ensure that the colonies have sufficient empty a hive while a division board feeder sits inside a hive comb to store the sugar that is being fed. If there is not replacing one or two frames. Top feeders have the enough room, the bees will fill with sugar the combs advantage that there is less disturbance of the colonies that the queen needs for egg laying. This will cause when the feeders are filled so there is less chance of the colony to stop growing, which may reduce their being stung. pollination efficiency. With both division board feeders and top feeders, large numbers of bees can feed on the syrup at the The beekeeper should be involved in any decision same time. Feeders that work on a drip feed principle, to feed sugar syrup to honey bee colonies. delivering small quantities of syrup over a long period, may not be effective or in some instances may not work

Figure 30. Division board feeder positioned to the far Figure 31. Hive with lid removed to show a top feeder. left of a box.

24 Obtaining and managing honey bee colonies for pollination at all and are therefore not recommended. Feeders the syrup given on the first few days but will do so later generally need pieces of wood or other items floating as they learn to take the syrup from the feeder. on or in the syrup to stop bees drowning. Feeding 1, 2 and 3 litres per hive every three days has been tested in colonies with about 30,000 bees (12 Only use feeders that permit a large number of frames covered with bees) in kiwifruit . The bees to access the syrup at the same time. amount of kiwifruit pollen collected increased with increasing volume of syrup fed. In New Zealand they are usually fed 1 litre every day or 2 litres every second 3.7.3 Concentration of the sugar syrup day. It may be necessary to feed less than this if the In many countries, beekeepers feed sugar syrup to colonies have less than 30,000 bees. colonies to keep them alive (usually 60 - 65% sugar) or lower concentrations to encourage the colonies to Feed 1 L of syrup daily or 2 L every second day. increase in size.

Both 30% sugar syrup (30 g of sugar in 70 ml of water) and 60% (60 g in 40 ml) have been tested on kiwifruit 3.7.6 Adverse weather and were both found to be equally effective. The choice It is often assumed that it is not worth feeding colonies of concentration may therefore depend on other while it is raining. This has not been researched but it factors other than pollination. Lower concentrations is probably worth continuing with feeding programmes have the advantage that they are cheaper and easier irrespective of the weather, unless bad weather is likely to make up, but they ferment much faster. Bees will to stop all honey bee activity for three or more days. not consume syrup if fermentation is too advanced. Concentrated syrup is very slow to ferment but is more expensive. Feeding dry sugar does not appear to have 3.8 Robbing any effect on pollen collection. Robbing is where a honey bee colony attempts to steal honey from another colony (Figure 32). Many of the Feed sugar syrup that is between 30% and 65% flowers honey bees visit are present only for a short sugar. period so they have evolved to take the maximum advantage of any available food sources. They are quick to find new food sources, and because they are Feeding sugar syrup can be beneficial for beekeepers able to communicate the distance, direction and taste as well. Because hives are often introduced to crops of the food to other bees, they can very quickly recruit at high densities, there may be little nectar and pollen large numbers of their hive mates to visit a food source. available for each hive. Feeding sugar syrup may It may take several hours for the first bee to find a new encourage the colonies to expand in size so they food source, but very quickly there will be hundreds are more able to collect a honey crop after they are or thousands of bees. Although this is fascinating to removed from the crop. watch, the results can be drastic.

While sucrose solutions have been tested and shown Honey bees from one colony usually leave other to work, it is not reported whether other sugars like colonies alone. Foragers can, however, become glucose and fructose will be equally effective. For this confused when returning from a foraging trip and enter reason only sucrose is recommended. the wrong hive when these are placed in straight rows and painted the same colour. When this happens by 3.7.4 Timing of feeding accident, the bees are usually accepted by the new Honey bee colonies can become aggressive when they colony. However, a bee that decides that taking honey are first moved to a new location so it is best to avoid from a neighbouring colony is much easier than visiting doing anything with them on the first morning they are flowers, gets a very different reception. The bees in a crop. A syrup feeding programme should start on whose job it is to guard the hive appear to be able to the second day the hives are in the crop and continue differentiate between those bees entering by mistake till the end of flowering. and those robber bees that attempt to steal honey. The robbers are usually set upon by the guard bees and Trials with kiwifruit have demonstrated that feeding at either ejected from the hive, or killed. Because of this, any time between 9 am and 5 pm will increase pollen usually few bees attempt to steal honey. collection. It is probably best to feed sugar syrup about the same time as the crop of interest is starting to Feeding sugar syrup or honey can change all this. As produce pollen. long as the syrup is placed inside the hive it seldom causes problems. The house bees consume the 3.7.5 Amount and frequency of feeding syrup and its presence is treated in the same way that The amount of syrup required depends in part on the the colony treats its own food reserves. Other than number of bees in the colony. All the syrup fed should increasing pollen collection and stimulating the queen have been consumed by the bees before the feeder is to lay, it seldom has any side effects. However, feeding refilled. Quite often the bees will not have consumed all sugar syrup outside a hive, either on purpose or

Obtaining and managing honey bee colonies for pollination Obtaining and managing honey bee colonies for pollination 25 accidentally, can cause large problems. In this case it By following a few simple rules it is possible to eliminate is the experienced foragers that take the syrup instead robbing problems. The most important things to of the house bees. The foragers, and the thousands remember are not to feed bees outside the hive, and of other bees that they recruit to the food, become to avoid spilling syrup while feeding without cleaning it conditioned to collecting large volumes of high quality up. This includes not letting it run down the outside of food outside their hive. When the food is finished they the hives or through the frames and out through the start to search elsewhere for it. The only other source hive entrance. Also, always store the syrup in closed of this type of food is usually the honey reserves of the containers, even if it is inside a garage or packing shed. neighbouring colonies. When the containers are empty, wash them out or seal them again rather than letting the bees clean them A single robber bee causes few problems, but out. As long as care is taken, robbing should not be thousands of them can cause major problems. If the a problem. robbers are in sufficient numbers they can kill other colonies and remove all the honey, which is detrimental to pollination. Robbing causes the colonies under Be careful not to cause robbing. attack to become very defensive. While hives can usually be approached safely if care is taken, you Summary: are liable to receive a very hot reception if robbing • Only feed syrup if more pollen foragers are needed. is occurring, even if you happen to be the innocent party. This defensive behaviour may also extend for • Feed 1 L /day or 2 L of syrup every second day if the quite large distances around the hive, causing all colonies can consume this amount. sorts of other problems. The robbing bees usually concentrate on the weaker colonies. If these colonies • Feed at the time the crop is producing pollen. are weak because of disease, robbing can result in the spread of disease to healthy colonies. Colonies • The syrup should have between 30 and 65% sugar that are spending their time attacking other colonies by weight. or defending themselves from attack are usually not • Use a top or division board feeder. interested in visiting flowers. • Don’t feed dry sugar, fructose or glucose.

• Don’t feed bees outside their hive.

• Be careful not to initiate robbing. 3.9 Pollen trapping and feeding It is possible to influence the amount of pollen a colony collects by removing pollen from a hive or by feeding pollen. Pollen can be removed using one of two methods, either pollen trapping or stripping frames of pollen. 3.9.1 Pollen trapping A pollen trap is a device with a grid that fits across the entrance of a hive. The devices are either fitted underneath a colony, replacing the floorboard, or fitted at the entrance of the colony. The entrance traps are usually faster and easier to fit to beehives.

The pollen traps work by scraping some of the pollen pellets off the legs of the bees as they enter the trap (Figure 33). Once dislodged, the pollen pellets fall through another screen and are collected in a tray. Bees do not seem to notice when their pollen pellets have been removed and still do everything they would normally do in the hive if they still had their pellets.

Beekeepers in some countries use pollen traps to collect pollen for human consumption or to feed back to bees. The proportion of pollen pellets removed from incoming bees depends on the size of the pollen pellets, Figure 32. A colony being robbed by other bees. which can vary considerably amongst crops. Their

26 Obtaining and managing honey bee colonies for pollination 3.9.2 Stripping frames of pollen When bees bring pollen into a hive, they store it in specific areas of cells in the honey comb until the colony needs to use it. It is sometimes possible to remove full frames of pollen. Removing frames of stored pollen from beehives has been shown to stimulate pollen collection. The size of the increases that could be expected is unknown. If frames of pollen are going to be removed, this will need to be done by a beekeeper.

Many beekeepers feed pollen or pollen substitutes to beehives to cause them to increase in size. Feeding pollen has, however, been reported to decrease the amount of pollen a colony collects. This may be worthwhile doing in crops in which only nectar Figure 33. Honey bees walking through the wire collectors are important pollinators e.g. hybrid radishes screen of a pollen trap which scrapes some of the and avocados, as it may decrease the number of pollen pollen pellets off their legs. foragers, allowing the colony to concentrate on nectar foraging.

3.10 Attracting honey bees to flowers Growers have long been sold compounds to spray on flowers to attract honey bees. The earliest attempt involved sugar syrup. More recently, a number of other materials have been tested, including a range of products using honey bee pheromones. Several commercial products claim to attract bees to flowers. 3.10.1 Sugar syrup Spraying sugar syrup onto flowers has been shown to increase the number of bees visiting plums5, European Figure 34. Pollen pellets in the drawer of a pollen trap. pears6, apples and nashi 7. Increases in fruit set have also been recorded after spraying sugar syrup8. However, other studies have reported increases in the number efficiency also varies with the size and the shape of of bees visiting leaves and branches but fewer bees the holes in the grid. Star shaped grids usually remove visiting flowers9. The reduction in the number of bees more pollen pellets than grids with square holes. visiting flowers may be due to their being insufficient honey bees in the area. If high efficiency pollen traps are used for a long time (months), they can have a negative effect on the When it was tested on nashi, it increased the number colonies as they become starved of pollen. of bees visiting leaves and branches. However, it also increased the number of bees visiting flowers (Figure If a pollen trap is to be used, care should be taken to 35). The effect lasted into the second day. On apples, ensure that the pollen trap grid is large enough not to the number of bees visiting flowers increased with the slow down the movement of bees into and out of the concentration of syrup applied (Figure 36). hive. The traps should also be checked frequently to ensure they do not become blocked with dead bees. The evidence is sufficient to indicate that spraying crops with sugar syrup will probably increase the number of It has been demonstrated that pollen trapping can bees visiting the flowers and increase pollination. If result in an increase in pollen collection. The effects syrup is being applied, concentrations between 30 and are, however, usually smaller than those achieved with 40% are probably the most appropriate. It needs to be sugar syrup feeding. noted, however, that there are still many unknowns with Pollen traps are also a very useful way of determining this method and its effects. The best recommendation how much pollen a colony is collecting from a crop as we can give is to try it on a small area of the crop before pollen pellets from different flowers often are uniquely treating everything. coloured (Figure 34).

Ensure the pollen traps are not restricting the movement of bees into and out of their hives.

Obtaining and managing honey bee colonies for pollination Obtaining and managing honey bee colonies for pollination 27 120 3.10.2 Commercial bee attractants BeeScent® 100 BeeScent® is a liquid formulation containing 9% pheromone and 40% other natural attractants. There are published data on this product that demonstrate 80 that it is effective at attracting bees to crops. In one trial it increased the number of bees visiting pear flowers for between 48 and 96 hours. It increased fruit set Leaves etc 60 by 27% on Bartlett pear, 44% on Anjou pear, 12% on cherries and 22% on Red Delicious apples. Whether

Bees per tree the increases in fruit set were statistically significant 40 Flowers increases was not stated10. Fruit boost® 20 The active ingredient of Fruit boost® is queen mandibular Control pheromone. The pheromone is produced by honey 0 bee queens and can be manufactured artificially. The pheromone is very attractive to honey bee workers. It

pre has been demonstrated that the pheromone sprayed 1130 1100 1230 1440 1200 1400 1330 1500 1030 1300 1000 onto apple, pear, cherry, cranberry and blueberry Time of day flowers can increase the number of honey bees visiting the flowers and increase production. The economics Figure 35. Average number of bees per tree visiting of using the product varies, however, depending on nashi flowers (flowers), leaves or branches (leaves the crop. etc.) on trees sprayed with 33% sugar syrup or visiting flowers on unsprayed trees (control) on the day the treatment was applied (0900 h). The vertical lines are 3.11 Honey bee stocking rates standard error bars9. Providing recommendations for how many honey bee colonies should be introduced to a crop is probably 45 one of the most important things to do but it is usually impossible to do reliably. For most crops there are 40 published recommendations on the number of colonies that should be introduced for pollination. However, the 35 recommendations vary considerably even for the same crop. For example recommendations for hives required 30 per ha for blueberries range between 1 and 10 hives per ha. 25 Various factors can affect the number of colonies that are required to be present to pollinate a particular crop. 20 3.11.1 Colony strengths Bees per flowers 1000 15 Colony stocking rates cannot be discussed without also discussing the number of bees in a colony. One 10 very populous honey bee colony may have as many foragers as 10 or 20 small colonies. Unfortunately most 5 published recommendations for stocking rates do not 0 10 20 30 40 50 60 indicate how large the colonies should be and are Percent sugar syrup therefore of little value. Figure 36. Relationship between the number of bees 3.11.2 Competing flowers visiting apple flowers and the concentration of sugar Probably the largest complicating factor when syrup applied. discussing colony stocking rates is the number of competing flowers around a crop and how attractive these other flowers are relative to the crop of interest. For example in a crop that had the same number of colonies, all prepared to the same strength on two consecutive years. In the first year there were few competing flowers outside the crop to draw bees away. However in the second year, white clover in the fields surrounding the crop flowered earlier than usual and caused the bees to desert the crop in favour

28 Obtaining and managing honey bee colonies for pollination of the white clover. In hindsight, the grower should have might suffer. If pollination was insufficient, it would be used four hives per ha the first season and possibly worth increasing hive numbers. more than 20 hives per ha the second season. Likewise if there appears to be more or less competing It is usually not possible to assess with any degree of flowers nearby than in previous years, then consideration accuracy the importance of competing flowers and how should be given to changing hive numbers. far colony numbers should be adjusted to compensate for them. This is because honey bees have such a Others’ experience large potential foraging area that it is very difficult to If it is a new crop it is worth discussing the number assess the area of competing flowers that are within of hives used by others in the area growing the same the bees’ foraging range. Even if the size of the area of crop. The beekeeper supplying the hives may be able competing flowers was known, the amount of nectar to provide information on how many hives other people and pollen produced by these flowers will likely vary are using. The further away these other crops are the between years and depend on the temperature and less reliable the information will be. soil moisture. Trial and error 3.11.3 Attractiveness of the crop This may consist of introducing hives and monitoring the results by assessing the number of bees on the If a crop is very attractive to bees, e.g. white clover crop and assessing pollination. and citrus, it may not be necessary to introduce many hives as most of the bees in the colonies introduced As a general principle, the cost of hives is small will forage from the crop. We have recorded bees compared with the value of a crop, so it is better to flying 5 km to reach a white clover field. If a crop is overestimate the number of hives than underestimate. less attractive, many hives may need to be introduced to ensure that at least some of the bees visit the crop. It is better to overestimate hive numbers than 3.11.4 Area of the crop underestimate them. The larger the area of the crop, the fewer the number of colonies that will be needed per ha. If there is a large area of the crop there will be a relatively large number of hives introduced at a standard stocking rate. The effect of any competing flowers outside the cropping area will be much less. An example of this is kiwifruit where, in some parts of New Zealand, it is almost a . At 8 hives per ha, there may be more than 700 hives per km2. In those cases there are so many bees that the effect of competition around the edges will always be minimal compared with a single hectare of a crop surrounded by competing flowers. 3.11.5 Number of flowers in the crop The number of flowers affects the number of bees needed and hence the number of hives. If there were no competing flowers, there would be a simple relationship in which doubling the number of flowers per hectare would require doubling the number of bees required. However, often many of the hives are introduced to ensure that at least some of the bees visit the crop because others are visiting the flowers outside the crop. In such cases doubling the number of flowers in the crop will usually require a smaller increase in the number of hives required. 3.11.6 Deciding on hive numbers Past experience If you have grown the crop previously you will have a good indication of how many hives to use next year, assuming the strength of the hives is the same size. If the level of pollination the crop received last year was adequate, consideration should be given to using the same number of hives next season. You could reduce hive numbers although it would be risky as pollination

Obtaining and managing honey bee colonies for pollination Obtaining and managing honey bee colonies for pollination 29 4. Orchard/crop management

4.1 Conditions within the orchard 4.2 Pesticides 4.3 Surfactants 4.4 Removing beehives before spraying 4.5 Mowing grass 4.6 Beekeeper/grower co-operation in and around crops. Although it is still unclear to what 4.1 Conditions within the degree pesticides are the cause of the bee losses, orchard honey bee poisonings due to pest control chemicals do occur in most countries including New Zealand. 4.1.1 Landmarks Bee poisonings firstly affect the beekeepers who Bees use landmarks for their orientation when flying, are trying to derive their income from the bees. This which can result in problems in some crops. The bees may either reduce their willingness to supply hives can become confused when blocks look similar. In for pollination or increase the fees that they charge. such situations, groups of bees can often be seen If the poisoning occurs when the crop is flowering, flying in circles looking for their hives that may be in it may also reduce the level of pollination, as foraging the next block. It has been suggested that coloured bees will be killed. markers, flags or any other things to break up the monotony of blocks may assist bee orientation but Bee poisonings have several common symptoms. The this has not been tested. The disorientation usually most common are large numbers of dead bees at the looks worse than it actually is. Many of the confused entrance of the hive (Figure 37). It is common to see a bees are probably house bees going on orientation few dead bees at the hive entrance but thousands of flights, or bees visiting other flowers outside the crop dead bees suggest they have been poisoned. Another and hence of little importance for pollination. The symptom is live bees outside the entrance that have a disorientation appears to be short lived as the number very jerky motion. of disorientated bees does not appear to continue to increase during the flowering season. Disorientation is, Dead bees do not pollinate. therefore, a problem that can usually be safely ignored.

4.1.2 Water Pest control has changed over time. Historically most Like other animals, bees need water. If there is not water pest control chemicals were ‘broad spectrum’ so that easily available to bees it may be useful to provide it. they would kill a wide range of invertebrates. However, A dripping tap or a sack hanging over the edge of a with advances in chemistry, there has been a move bucket of water will usually be sufficient. This will help to pesticides that are increasingly species specific. to reduce the number of bees visiting the neighbour’s Although this has resulted in many chemicals being swimming pool. safer for honey bees, it has made the issue more complicated as some pest control chemicals can In arid conditions, larger amounts of water may need to be provided and this should be discussed with a beekeeper. 4.1.3 Wind Bees do not like flying in strong winds. Wind in excess of 15 km/h will reduce bee activity, and few bees will leave their hives when wind velocities are in excess of 24 km/h. It is therefore important to place colonies in a location that is protected from strong winds. 4.1.4 Mowing orchards It has been suggested that the weeds in or under a crop should be left to encourage bees to stay in the crop. This is, however, unlikely to improve pollination as the bees visiting the weeds will not generally also visit the flowers of the crop. It is therefore, useful to keep the weeds mown while the crop is flowering. As a general practice, it is useful to remove as many competing flowering plants as possible.

It is good practice to remove as many competing flowers growing around or under a crop but don’t mow flowering weeds when bees are present.

4.2 Pesticides In many northern hemisphere countries there are reports of large numbers of colonies dying. One of the popular theories blames the pesticides that are used Figure 37. Dead bees outside their hive.

Orchard/crop management 31 safely be applied to flowers without killing bees while be eliminated by mowing underneath the canopy of others cannot. Even with these safer chemicals being horticultural crops before spraying. It is much more available, many of the older broad spectrum chemicals difficult with flowering weeds growing amongst a crop. are still being used. In this case only non bee toxic chemicals should be used. Poisoning of hives introduced to a crop can occur because the grower has applied a bee-toxic chemical 4.2.2 to flowers in the crop. However, even if growers are It had been shown that most fungicides are not toxic very careful about the pest control chemicals they use, to adult honey bees. Although this is probably correct, poisoning can still occur. Honey bee colonies have large a recent study has demonstrated that the pollen flight ranges so the bees from the colonies introduced collected by bees from flowers sprayed with fungicides to a crop may be foraging on flowers up to 5 km away becomes contaminated with fungicides, and that and get poisoned there. It can therefore be useful to when some fungicides are fed to honey bee larvae at remind neighbours that hives are being brought in for similar concentration to that found in pollen that it can pollination and not to put toxic sprays on flowers. kill them11. In some crops where sprays can cause significant The effect of fungicides on honey bee larvae has bee deaths, growers, beekeeper organisations and not been extensively researched so that a complete chemical companies work together to put in place list of fungicides that are likely to be toxic to larvae is education programmes designed to prevent bee not reported. Also, warning labels do not poisonings. These programmes may include seminars, normally include warnings about honey bee larvae. mail drops, published articles and even erection of road side signs. It is therefore good practice not to apply fungicides to flowers unless it is essential for disease control. For a grower, the simplest way not to poison bees is that If the safety of the fungicide to honey bee larvae is if a chemical is toxic to bees it should not be applied not known, the issue should be discussed with the to flowers. In New Zealand, the pest control chemicals beekeeper before it is applied to flowers. come with instructions that will describe whether they can be safely applied to flowers. Some fungicides can also affect pollination by affecting the pollen grains’ ability to germinate on the stigma12, Tell your neighbours you are introducing hives so which may adversely affect pollination. Unfortunately, they do not poison them. there has been few investigations on how frequently this will be a problem.

The wording on warning labels on pesticide might say Where possible avoid spraying fungicides on something like: flowers. • D o n’ t a p p l y t o fl o w e r s t h a t a r e , o r a r e l i k e l y t o b evistd by bees.

• Don’t apply to flowers that are, or are likely to be, 4.3 Surfactants visited by bees except in the evening. Surfactants are used to improve the effectiveness of chemicals, to decrease the droplet size or to increase • The spray must be dry before it is contacted by the penetration of chemicals on a plant or insect. Some bees. surfactants used with insecticide and fungicide sprays • Do not spray on flowers that are being visited by are toxic to bees. When water is sprayed onto bees bees. it usually forms discrete droplets on the surface and does not damage the bees (Figure 38 a). However, • Can be applied while bees are foraging. surfactants allow the water to penetrate the body hairs, which will kill bees (Figure 38 b)13. Unfortunately, the • Sprays that are non toxic to bees can be used during toxicity of most surfactants has not been tested and the flowering season. It is, however, important to they do not carry bee warning labels. Unless it has wash the tank out first. been demonstrated that a surfactant will not kill bees it should not be applied to bees even if the pesticide it is If applying bee-safe chemicals to flowers ensure mixed with is non-toxic to bees. the spray tank is washed thoroughly beforehand. Don’t spray surfactants onto honey bees unless 4.2.1 Spray drift they have been shown to be bee safe. One of the most common causes of bee poisoning is spray drift. This is where a pesticide has been applied Water itself can be a problem if it is cold or if it is applied to a crop that is not in flower but has drifted onto at high pressure or high volume (Figure 39). The effect flowers of other plant species. This problem can often is similar to when surfactants are used (Figure 40).

32 Orchard/crop management To avoid killing bees and adversely affecting pollination, it is good practice to avoid applying even bee-safe chemicals while bees are visiting the crop. Care should also be taken to avoid applying sprays directly onto beehives.

Do not apply sprays or water directly on bees or bee hives.

a 4.4 Removing beehives before spraying Growers sometimes have their beehives removed if they have to apply an insecticide and the crop is still flowering. This eliminates bee deaths but great care is needed to ensure that there are not other colonies in the area. It is important to remember that the bees may be flying up to 5 km to visit the crop if it is particularly attractive. 4.5 Mowing grass b Although it is important to mow the grass sward before spraying bee-toxic pest control chemicals to avoid Figure 38. A honey bee sprayed with (a) water and (b) killing bees, the mowing itself may kill bees; some water and a surfactant. mowers are reported to kill over 60% of the bees visiting flowers in the sward when it is mown14. The best way to avoid killing bees is to mow early in the morning or late in the evening when the bees are no longer foraging on flowers in the sward.

Mow grass in the evening or morning when bees are not forging to avoid killing them.

4.6 Beekeeper/grower co-operation

An essential practice when supplying or hiring hives for Figure 39. A clover field being irrigated. pollination is for the beekeeper and grower to discuss the spray programme that will occur when the hives are in the crop. This will allow a plan to be developed to minimise any negative effects on honey bees or pollination.

Figure 40. A bee affected by irrigation.

Orchard/crop management Orchard/crop management 33 5. Crops

5.1 Buckwheat 5.2 Carrots 5.3 Field beans and Broad beans (Vicia Faba) 5.4 Linseed 5.5 Lotus, Birdsfoot - trefoil 5.6 Lucerne (alfalfa) 5.7 Oil Seed Rape 5.8 Radishes 5.9 Red clover 5.10 White clover 5.1 Buckwheat Buckwheat flowers occur in clusters, mostly at the top of the plant. The flowers have eight stamens surrounding a central style which has three stigmas. The stigmas are only receptive for one day.

There are two forms of flowers. One form has long stamens and a short style and the other form short stamens and a long style that projects above the anthers. A single plant usually only has one form of flowers. Although a small level of self pollination is possible (i.e. pollen from the same flower type), pollination is most effective with pollen from the opposite type15. Self pollination is reported to only give 0.5% seed set Figure 41. A male fertile carrot umbel. compared with 44% set with insect visitation16. Varieties with higher levels of self fertility have been developed.

The flowers have eight nectaries spread around the base of the ovary. These secrete large amounts of nectar in the morning17. The amount of nectar produced and its concentration varies with and the year18. A plant may have up to 2000 flowers and flowering may take up to 30 days.

The flowers are visited by insects to collect both pollen and nectar. Honey bees are the most common visitors of buckwheat and can be most easily managed. In sufficient densities each flower will receive more than 40 visits, however, seed set is usually not improved with 19 more than two visits . Figure 42. A male sterile carrot floret. It has been recommended that between five and eight honey bee hives per ha should be introduced for 18 buckwheat pollination . 5.2 Carrots Carrot flowers are in the form of an umbel. There is usually a primary umbel, which is produced first and then a series of increasingly smaller lower order umbels. The primary umbel is the most important for seed production. The plants will flower for between four and six weeks.

The umbel is made up of groups of individual florets. The florets are presented in a number of discrete groups of flowers (Figure 41). The flowers around the outside of the group open first and those in the centre last. It takes about seven days for all the florets on an umbel to open. The stigma remains viable for about a week. Figure 43. A carrot umbel with three species of insects

Although carrot flowers have both male and female visiting it. parts, much seed production has shifted to hybrid seed production. To achieve this, lines that are male sterile (Figure 42) or male fertile are produced. The male Hybrid carrot crops are usually planted with three male sterile line produces the seed and has non functional fertile lines and five or six male sterile lines. male parts. The pollen must be moved from a male fertile line, producing hybrid seed. As only the male Some lines appear to be very attractive to insects. fertile lines produce pollen, pollen-foraging insects The hybrid line in the photo (Figure 43) had a number will not normally visit both male fertile and male sterile of insects visiting each umbel at the same time. The lines unless they do so by accident. Usually only nectar difference in attractiveness was likely due to the foragers visit both lines and pollinate the crop amount of nectar being produced.

Crops 35 Although a number of insects visit carrot flowers and pollinate them, and some species of flies may be better pollinators than honey bees, honey bees are currently the only insect that can be managed in sufficient numbers to provide the necessary pollination services.

Honey bees are introduced to pollinate carrots. They need to have large numbers of bees so they have a high demand for nectar. As the crop flowers for six weeks it is worthwhile considering introducing further hives as flowering progresses to replace any foragers that have deserted the crop. Because some hybrids appear not to be particularly attractive to bees it is important there are sufficient bees visiting the crop. We do not currently have enough information to be able to recommend a particular density of honey bees that should be observed, it is possible to check for differences in the number of bees visiting flowers throughout the season. With this approach the counts Figure 44. A honey bee visiting a broad bean flower. should be done at the time there is the peak honey bee activity for the day. This may necessitate carrying out several counts during a day. If the number of bees flowers but not nectar. Short tongued bumble bees counted starts to decline through the flowering season will, however chew holes in the base of the flower to more colonies should be introduced. reach the nectar, without pollinating the flowers. Honey As nectar foragers are the most important pollinators in bees will then use the holes to reach the nectar. It is this crop, colonies should have large numbers of bees. possible, therefore, that short tongued bumble bees Sugar syrup should not be fed and pollen traps should may be detrimental for pollination. not be used as both of these increase the number of pollen foragers. 5.4 Linseed Linseed flowers have five petals, five stigma, five 5.3 Field beans and Broad anthers, and an ovary with five locules. Each locule beans (Vicia faba) contains two ovules. Under good conditions, the flowers open in the early morning followed closely by Field beans anther dehiscence. As the flowers open the anthers Field bean flowers have a standard petal, two wing touch the stigma and deposit pollen. petals and two lower petals joined along one edge to form a keel. There are ten stamens, nine of which The flowers are visited by insects including honey bees are enclosed along most of their length in a sheath. but trials (cv. Antares) were unable to find any evidence The tenth (upper) stamen is usually exposed along its that these visits increased seed production21. Linseed complete length. There is a single ovary with two to therefore appears to be completely self fertile and four ovules. The flowers reopen each day for about will not benefit from the introduction of honey bees a week. or other efforts to increase pollination. Other may, however, be developed in the future that are not When the flower is tripped, the style, which has long completely self fertile. hairs, brushes the pollen out of the keel and places it on the visiting insect. The levels of self fertility often vary Despite the reported self sterility22, when growing between plants in a crop. Some may set seed without linseed it is probably good practice to check with the being visited by an insect, while others need an insect supplier of the seed to determine whether the variety is visit to set seed19. completely self fertile.

Trials with plants in cages with or without honey bees have demonstrated field bean pollination benefits from honey 5.5 Lotus, Birdsfoot - trefoil bee pollination20. Birdsfoot trefoil (Lotus corriculatus) flowers have wing Broad beans petals and keel petals. The flowers are mostly self Broad bean flowers are similar to field bean flowers incompatible although some self compatible clones 23 (Figure 44). Honey bee pollination does, however, exist . In a trial, untouched flowers produced two appear to be more important. seeds per flower, tripped flowers produced 340 seeds per flower and cross pollinated flowers produced The main insects visiting bean flowers are honey bees 481 seeds24. The main pollinators are honey bees and bumble bees. Honey bees and short tongued and bumble bees, which are large enough to trip bumble bees can usually collect only pollen from the the flowers.

36 Crops Bees visit lotus flowers to collect both pollen and Pollen gatherers normally trip the flowers when nectar. Twelve to 25 honey bee visits per flower are collecting pollen. Inexperienced nectar gatherers needed for full pollination25. Pollen foragers produce usually trip flowers while foraging as well, but soon more seeds per visit than nectar foragers26. learn to collect nectar from the side of the flower, which does not usually trip it. In 16 studies18, an average of Managing bees to promote pollen collection may only about 1% of nectar foragers tripped the flower therefore be of value. Five to six hives per ha have been they visited. recommended for pollination27. There are numerous methods that can possibly be used to increase the percentage of flowers that are 5.6 Lucerne (alfalfa) tripped. The lucerne flower is made up of five petals: the large standard petal, two smaller wing petals, and two petals 5.6.1 Increasing the number of that are fused and called the keel. The keel encloses pollen foragers the stigma and ten anthers. Nectar is produced at the Because of their high rate of tripping flowers, increasing base of the petals (Figure 45). the number of pollen foragers visiting lucerne is likely to have the largest effect on pollination rates. Using The stigma and anthers are under tension. When this colonies with a high demand for pollen, stripping pollen tension is released, the ‘tripped’ stigma and anthers from colonies or feeding sugar syrup should increase snap against the standard petal and remain in that the number of bees collecting pollen and may increase 18 position . A flower must be tripped to produce seed. the number collecting pollen from lucerne and hence Some flowers self trip under a range of environmental the number of flowers tripped. These methods have condition but self tripping results in self pollination. not been adequately investigated in lucerne to know Because there is a range of self sterility in lucerne how effective they will be. plants, only 17–46% of self pollinated flowers produce seeds18. Cross pollination is required for good seed 5.6.2 Increasing the number of yields from lucerne crops. nectar foragers Cross pollination occurs when the flower is tripped If only 1% of nectar foragers trip flowers, increasing by a bee looking for pollen or nectar. The force of the total number of nectar foragers visiting the crop by the tripping usually traps the head of the bee that is introducing more colonies should increased the number visiting the flower. It must struggle to free itself and so of flowers tripped. There are limits, however, on how becomes coated with pollen and deposits pollen it may far the number of nectar foragers can be increased. have carried from another flower. When there are enough nectar foragers to deplete the nectar available in the lucerne flowers, any additional Because of the forces required to trip the flowers, nectar foragers introduced may forage elsewhere. only heavier insects like bees can usually trip lucerne The number of nectar foragers can be increased by flowers. These are usually honey bees, bumble bees, increasing the number of hives, and perhaps more and in some countries leafcutter and alkali bees. In importantly the number of bees in each hive. New Zealand, most lucerne pollination is carried out by honey bees because they are the easiest to manage 5.6.3 Naive foragers and can be introduced to crops in large numbers. When colonies are first introduced, a relatively high percentage of nectar foragers trip flowers before they learn that there are easier ways to collect nectar from lucerne flowers. Thus increasing the number of naive foragers should increase the percentage of lucerne flowers tripped. It has been reported that bringing in new colonies at frequent intervals almost doubled the percentage of tripped flowers28. 5.6.3 Other bees Although honey bees are the most important pollinators of lucerne, because of the numbers introduced to crops, there are other bee species that are more efficient at tripping flowers and pollinating lucerne.

Long tongued bumble bees are reported to trip more flowers than short tongued bumble bees, which feed from the side of the flowers28,29. Bumble bees can be hired, but they are likely to be too expensive to use for lucerne pollination. It may be possible to increase the number of feral bumble bee colonies in the vicinity of a Figure 45. Lucerne flowers. crop (see section 1.4.2).

Crops Crops 37 Leaf cutter bees are reported to be better pollinators of lucerne than honey bees. They are an option if they can be acquired in sufficient numbers for a suitable price. 5.6.4 Assessing pollination Because of the difficulties associated with lucerne pollination, it is recommended that the level of pollination be assessed. This can be done my by measuring the weight of seed per ha but more accurately by picking seed heads and counting the number of seeds produced. It is probably good practice to assess seed set in areas close to and distant from any introduced hives. 5.7 Oil Seed Rape The flowers are in racemes at the top of the plants. They usually have four petals, six stamens and a style. Four of the stamens are longer than the style and two shorter. The flowers have nectaries at the base of the stamens. Although the flowers are self fertile, seed set is Figure 46. A radish flower. improved with cross pollination. This can occur through wind pollination but seed set is generally accepted to be improved with insect pollination. The importance of honey bee pollination does, however, appear to vary with variety. There are trials on a particular variety e.g. cv. Midas where caging plants to exclude bees did not decrease seed set30. On cv. Karoo at a stocking rate of 1.28 hives/ha it was demonstrated that seed set decreased with distance from hives31, indicating that honey bee pollination was important for that variety and too few honey bee colonies had been introduced.

It is probably best practice to introduce honey bees for the pollination of all oil seed rape varieties unless it has been shown that the variety does not benefit from honey bee pollination.

5.8 Radish Figure 47. A honey bee coated in pollen collecting nectar from a radish flower. There is relatively little published on radish pollination, particularly on hybrid radish pollination.

Radishes have small white flowers with four petals 0.8 (Figures 46 and 47), anthers and a single stigma and style. They have a pod that when fully pollinated may produce six seeds. The flowers produce pollen and 0.6 Male fertile nectar. In hybrid radishes, male sterile plants produce Male sterile only nectar, while male fertile flowers produce both pollen and nectar. The flowers open only for a single day and then usually wither. 0.4

Hybrid radishes are usually planted with three rows of male fertile flowers and six to eight rows of male 0.2 sterile flowers. Bees are reported, however, to be able to differentiate between some male fertile and male sterile lines, and this restricts their movement between them. Only 1.3% of bees were as recorded changing 0.0 between the two types of flower they visited when 11 Dec 19 Dec 8 Jan 14 Jan moving between flowers. Date

Radishes are visited by a range of insects but honey Figure 48. Number of bees counted on male-fertile bees are the main pollinators because they can be and male-sterile radish flowers on four dates.

38 Crops managed and introduced in sufficient numbers. In were introduced into New Zealand for the purpose of a study carried out at four sites in New Zealand, all pollinating red clover. sites had less than 50% of the potential seed crop, indicating that there was insufficient pollination. It Long-tongued bumble bee species in New Zealand has been estimated that 6.5 bees per 1000 flowers are reported to be better pollinators of red clover than are needed for full pollination32. The number of bees honey bees and short tongued bumble bees because recorded per flower decreased during the flowering the florets are longer than white clover so short season, suggesting that the bees were moving onto tongued bumble bees and honey bees have difficulty more attractive food sources (Figure 48). in reaching the nectar. The short tongued bumble bee B. terrestris bites holes in the base of the flower to In hybrid radishes, only nectar foragers visit both male access the nectar and therefore are less efficient sterile and male fertile flowers. For this reason, colonies pollinators than the other bumble bee species. Honey introduced for pollination should have large numbers bees will occasionally use these holes as well. of bees and a high demand for nectar. It has been recommended that more than four strong hives should Although not as efficient as bumble bees, honey bees be introduced per hectare. can pollinate red clover. They visit flowers to collect nectar and pollen. They will collect pollen from red It is worthwhile assessing the number of bees on the clover flowers even if they cannot collect nectar33. crop at the timing of peak activity to determine if there are enough hives present. It is generally too expensive to hire bumble bee colonies for red clover pollination in New Zealand and the only species of bumble bee that is commercially available is 5.9 Red clover the short tongued B. terrestris, which is less efficient than the long tongued bumble bees. Bumble bees can Tetraploid Red clover is grown for seed production be encouraged to establish nests in the area of a crop in New Zealand and (Figure 49). The red by placing bumble bee nest boxes. clover flower head has up to 200 florets. The florets open starting at the base of the flower head and fold Most red clover is pollinated by honey bees so they downwards afterwards. In the middle of flowering, a should be introduced to optimise pollination. Feeding flower head will typically have a ring of flowers that honey bee colonies sugar syrup has been shown to have been open and have folded down, a ring of open increase the amount of red clover pollen colonies flowers in the middle and a ring of unopened florets at collect and presumably the number of flowers visited the top of the flower head. It takes about a week for all and pollination, and hence probably worth while. of the florets on a flower head to open. Ensuring colonies have a high brood to bee ratio will also be worthwhile as these colonies will have a high Red clover florets are self sterile so pollen needs to be demand for pollen. transported from another plant. Because of the need to pull down part of the flower (keel) to gain access to the As the pollination of red clover is difficult, it is worth pollen and nectar, only heavier insects can pollinate red assessing seed set. This can be easily done by clover. For this reason, honey bees and bumble bees removing seed pods and rubbing them between the are the main pollinators of red clover. Bumble bees thumb and forefinger to determine the number of seeds. If fully pollinated there should be six seeds per seed pod. 5.10 White clover White clover (Trifolium repens L.) is a species of clover native to , West Asia, and North . It has been introduced throughout the world as a pasture crop. It is also grown as a seed crop in New Zealand (Figure 50).

White clover is a low-growing, herbaceous that bears white flower heads, ‘inflorescences’, made up of small florets. There are a large number of different varieties. The varieties are classified by the size of their leaf: large, medium-large, medium, and small leaved.

White clover flowers have between 21 and 104 florets per flower head (Figure 51). The florets on a flower head open successively over a week, beginning with those at the base and ending with those at the crown Figure 49. Red clover field. of the flower head. Once the florets are open, if they

Crops Crops 39 are not pollinated they will stay open for five to eight days. However, seed set can be reduced by 60% after five days. Based on the number of ovules present, each floret should be able to produce six seeds. In commercial seed crops in New Zealand florets produce between zero and seven seeds, with an average of approximately three seeds.

The florets on a flower head are hermaphroditic (have both male and female organs) but all varieties are self incompatible. A floret cannot produce seeds with pollen from the same florets, from other florets on the same flower head or pollen from other flower heads on the same plant. The pollen has to come from other plants.

For pollination to occur, an insect vector is needed. The anthers liberate pollen before the florets open. The anthers deposit the pollen onto the stigma. Insect visitors pick up this pollen and replace it with pollen Figure 50. A white clover seed crop in Canterbury, from other plants. New Zealand. To be able to gain entrance to a white clover flower, the insect must have sufficient weight to pull the flower downwards (Figure 52). For this reason only larger insects can gain access to white clover florets and pollinate them.

Honey bees are the most important pollinators of white clover. Honey bees visit clover flowers to collect nectar and/or pollen. Both types of foragers are thought to be equally efficient at pollinating clover, for they both contact the stigma. White clover flowers can be very attractive to honey bees, which have been recorded to fly 5 km to reach a clover crop. Good levels of pollination can be achieved by feral bees or managed bees in other crops within flight range.

But to optimise the reliability and effectiveness of pollination it is best to introduce bees.

Based on the average number of seeds produced by a single bee visit to a clover floret (1.24); the length of a bee’s foraging trip and foraging day; and the number Figure 51. A white clover flower head. of open florets at any particular time, 19,420 bees are required per hectare for the maximum number seeds to be set per floret.

Although some growers rely on managed colonies that are already in the vicinity of the crop, the best results will be achieved by introducing colonies a rate of 8 per ha.

Figure 52. A honey bee visiting a white clover flower.

40 Crops

6. Towards diversifying pollinators in crop fields

6.1 Value of pollinator diversity 6.2 Towards increasing pollinator diversity within crops

Crops 6.1 Value of pollinator diversity

Honey bees are used to pollinate crops because • More efficient pollinating species contribute to the they are managed and abundant, however, for many pollination of crops that are poorly pollinated by cropping plants, pollination by honey bees is a recent honey bees35. That is, crops that honey bees are development caused by human introductions and reluctant to forage on or where bees are ineffective intervention. These plants e.g. crops originating from at transferring pollen to stigmas. the Americas in the absence of honey bees (such as avocado, tomato, pumpkin, squash and sunflower18) • Non-honey bee pollinators pollinate crops under have evolved to be pollinated by a wide range of non- climatic conditions that are less suitable for honey honey bee pollinators. In these circumstances, honey bee pollination36. bees may be less effective pollinators than other insect A variety of currently unmanaged bee and fly species. Maximising pollinator diversity is important for pollinators contribute significantly to crop pollination in increasing crop yield because: New Zealand (Figures 53 and 54). The most common • Different pollinating species distribute pollen on species are widespread across both North and South flowers differently. Therefore, a combination of Islands and have been observed visiting the flowers pollinating species increases the pollen distribution of a diverse array of crops including pak choi, onion37 within crop flowers compared with a single species kiwifruit38 radish39 and white clover40. alone34.

Lasioglossum spp.: Small native bee, 6 mm long, Leioproctus fulvescens: Large native bee, slightly very common, black. smaller than honey bees, orange hairs.

Leioproctus spp.: Large native bee, ½ to ¾ size of : Very large introduced bee, black, yellow honey bees, black. and white.

Figure 53. Common unmanaged bees that pollinate crops in New Zealand.

42 Towards diversifying pollinators in crop fields NZ black hover fly Blue hover fly NZ orange hover fly Drone fly

Hover flies (Syrphids) New Zealand black hover flies are very common long thin flies about 12 mm in length. New Zealand orange hover flies are similar but much smaller than New Zealand black hover flies with larger orange body markings. Blue hover flies are slightly smaller than honey bees and have a shiny blue abdomen with an orange segment at the top. Drone flies look similar to honey bees but are often larger. They often have two distinct orange patches near the top of the abdomen with the darker colouring making an ‘H’ shape.

Euro. blue blow fly NZ blue blow fly Brown blow fly Euro. green blow fly

Blow flies (Calliphorids) Usually large rounded metallic coloured flies. The European blue blow fly has a grey-blue abdomen, the New Zealand blue blow fly is very large with a shiny dark blue abdomen and orange spots on its side, the brown blow fly has a golden brown abdomen, and the European green blow fly is shiny green or bronze.

Ginger blister fly, Green soldier fly, Striped thorax fly, March fly, large (15 mm long) about 12 mm long about 12 mm long 12 mm long Tachinidae Stratiomyidae Sarcophagidae Bibionidae

Figure 54. Common unmanaged flies that pollinate crops in New Zealand.

6.1.1 Non-hybrid pak choi seed crops lines to sterile lines for hybrid seed production. In In non-hybrid pak choi crops, honey bees, native these crops, honey bees are often less efficient bees and similarly sized flies are equally efficient pollinators because they make fewer movements pollinators41, 42. Non-honey bee pollinators contributed between the parent lines35. In hybrid carrot seed similar levels of pollination as honey bees over four crops, unmanaged pollinators contributed more consecutive seasons43. There is currently no biodiversity pollination than honey bees, despite fields being management strategy aimed at maximising or securing stocked with hives (Figure 55). In carrot, syrphids the contribution of non-honey bee species. (Drone flies and New Zealand black hoverflies) were the most efficient pollinators because they deposited 6.1.2 Hybrid seed crops pollen from male fertile to male sterile flowers most Hybrid seed crops are commonly grown in New frequently35. Blow flies are also key pollinators in Zealand and require pollen to move from male fertile hybrid carrot fields (Figure 55)44.

Towards diversifying pollinators in crop fields Towards diversifying pollinators in crop fields 43 6.1.3 Other crops There is a lack of information on the effectiveness of non-honey bee pollinators for most crops grown in New Zealand; however, native bees and are effective pollinators of kiwifruit38 and white clover (unpublished research). Research from overseas indicates that non-honey bee pollinators contribute to the pollination of a large variety of crops such as sunflower, strawberry, watermelon, tomato, pumpkin, squash, various types of beans, peas, and apples and stone fruits45. A similar situation is therefore likely in New Zealand.

Field 1 Field 2 Pollen deposition rate = 135.5 pollen/min Pollen deposition rate = 53.6 pollen/min

Field 3 Field 4 Pollen deposition rate = 549.5 pollen/min Pollen deposition rate = 70.5 pollen/min

Honey bee Brown blow fly European blue blow fly

Drone fly Black hover fly Other flies

Figure 55. Estimated pollen deposited per minute by pollinators in four hybrid carrot fields. Rate is for an area of 200 m2. Non-honey bee pollinators distributed the bulk of pollen to male sterile flowers in all fields examined.

44 Towards diversifying pollinators in crop fields 6.2 Towards increasing pollinator diversity within crops

6.2.1 Semi management techniques explore this potential in conjunction with promoting The abundance and distribution of non-honey bee crop populations of natural enemies and suppressing pest pollinators is influenced by a variety of variables including species. climate, lifecycle needs, the spatial and temporal distribution of flowering plants, on-farm landscape Further research, being conducted in Canterbury, features, and regional land uses. Even pine hedgerows NZ, by Plant & Food Research (CAP 10-71), is also (not utilised as a foraging nectar resource by most examining the influence of the wider landscape pollinators) can influence the distribution of species (land uses and features such as watercourses and (Figure 56) that may be using them for shelter46. permanent vegetation) on pollinator abundance and distribution. Many pollinating species readily move Given that pine hedgerows and farm gardens can distances of at least several hundred metres within the influence the abundance and diversity of pollinators, landscape47. Therefore, populations may be influenced there is likely to be significant scope to design hedgerows by the concentration and distribution of land uses and on-farm tree plantings aimed at building pollinator and features beyond farm boundaries. This research diversity and populations. A three-year study, Building has potential to develop tools to predict the spatial Better Biodiversity on Cropping Farms (SFF 12-015), will distribution of pollinators at a regional level.

a. C. stygia b. C. vicina c. L. sericata

50 5 25 10 1 5 1

Mean count 1

0 0 0 Pine Pine Pine Water Water Water Gorse Gorse Gorse Garden Garden Garden Pasture Pasture Pasture

d. Tachinidae e. M. novae-zealandiae f. A. mellifera

25 5 10 10 5 5 1

Mean count 1 1

0 0 0 Pine Pine Pine Water Water Water Gorse Gorse Gorse Garden Garden Garden Pasture Pasture Pasture

Figure 56. The abundance of crop pollinating species blow flies (Calliphora stygia, C. vicina, Lucilia sericata), bristle flies (Tachinidae), New Zealand black hover fly (Melangyna novae-zelandiae), honey bee (A. mellifera). caught in window traps placed five metres from on-farm landscape features (treatments: open pasture near fence lines, watercourses. pine hedgerow, farm garden, gorse hedgerow; n = 6).

Towards diversifying pollinators in crop fields Towards diversifying pollinators in crop fields 45 6.2.2 Some pollinators with management Blow flies potential Blow flies, particularly the European blue blow fly Calliphora ( vicina), are species with potential Leioproctus bees for development as crop pollinators. They occur A number of Leioproctus species visit the flowers of worldwide and are generally easy to rear. Blow flies commercial crops. Leioproctus huakiwi, in particular, is forage on the flowers of a wide range of plants and are a common and widespread species that is an efficient a likely pollinator of many species. They also forage 48 pollinator of crops including kiwifruit , brassica and under climatic conditions less suitable for honey bee onion (Brad Howlett unpublished data). They can also foraging50. To date, research shows they are effective form dense aggregations containing several thousand pollinators of brassica42 hybrid carrot35 and onion 2 bees in an area of less than 10 m (Barry Donovan (Howlett et al. unpublished). personal observations). These characteristics make it a good potential candidate for managing. Research by Calliphora vicina larvae require protein for Plant & Food Research shows that the species nests development51. They are mostly associated with in a wide variety of soil types (clay to sand) and is carcasses, and large numbers can be easily cultured generalist in its foraging (will visit the flowers of several using meat products (e.g. meat, offal, canned meats). different species in a single foraging trip). A number of other species including the native New Zealand blue blow fly C. ( quadrimaculata) can be Overwintering prepupae of Leioproctus huakiwi have reared on similar diets52. been successfully transferred from an overwintering site at Akaroa to Lincoln where a new population has In New Zealand, C. vicina was found to be a very been established49. Two methods of relocating the effective pollinator of hybrid carrot when enclosed prepupae were tested. These were via: inside mesh tents covering several male fertile and sterile plants44. In a further experiment, C. vicina were • Soil cores containing intact nest cells (prepupae left reared and released as adults in two carrot hybrid in the soil undisturbed). fields. On release, flies immediately foraged on male • Artificial cells (prepupae removed from the soil and fertile and sterile umbels within a few metres of the 52 placed in the cells) (Figure 57). release point .

Both methods have successfully led to prepupae To develop C. vicina as a managed pollinator, further developing through to adults and emerging successfully assessments are required to determine the length at the new Lincoln site. Since the establishment, the of time adults remain foraging in crops and whether population of L. huakiwi has grown rapidly49. Attempts this can be manipulated to maximise retention within to transfer populations to arable farms (more exposed the required area. Consideration must also be given sites) have resulted in bee emergence but populations to neighbouring land uses where flies could be a were not successfully established beyond one season. problem, e.g. urban areas. Further research on native bee ecology, particularly Drone flies the mechanisms of nest site aggregation, is required The drone fly (Eristalis tenax) is a hover fly that is an to develop a reliable technique to establish managed efficient pollinator of a range of crops including pak populations. choi41, carrot35 and onion (Brad Howlett unpublished data). It is a more efficient pollinator than honey bees in hybrid carrot35 and onion crops (Howlett et al. unpublished data) because it transfers pollen from male fertile to sterile umbels more frequently.

The larvae of drone flies and a number of other hover fly species (known as rat tailed maggots) develop in watery environments containing high organic contents. They are particularly common in dairy sheds and may be trapped there53.

Techniques for mass rearing larvae need to be developed before this species can be managed. As with other fly species, further information is required on fly movement and whether they remain in fields during the entire flowering period. Methods for manipulating their distribution within fields are important for developing management strategies. These include controlling Figure 57. Pupation box containing Leioproctus pupae their spread from target crops to land uses where they showing drinking straw pupations cells (the pictured may be considered a nuisance (e.g. dairy farms)53 and pupation box is smaller but similar to those used in for maintaining even distribution throughout crops. this trial).

46 Towards diversifying pollinators in crop fields Appendix

Towards diversifying pollinators in crop fields Draft pollination contract

This agreement is made on the (date)

BETWEEN

(grower’s name) hereinafter called the “grower”

and (beekeeper’s name) hereinafter called the “beekeeper”

TERM OF AGREEMENT The term of this agreement shall be for the 20 growing season, covering flowering until 48 hours after the grower requests hive removal, but not beyond of that year. (Other agreed provisions should be added or deleted if required at the time of signing, and initialled by both parties).

SECTION A: RESPONSIBILITIES OF THE BEEKEEPER

Beekeeper Agrees:

1. To supply the grower with hives of honey bees as stipulated in the following table:

HIVE DELIVERY TABLE

Description of the delivery Hive number Timing of introduction location

At % flowering

At % flowering

At % flowering

(Grower to advise beekeeper of delivery dates as per clause 3)

2. To supply hives each containing a minimum of (higher standards may be negotiated, especially on isolated or problem orchards):

a) four full standard frames of brood in all stages (7000 cm2 of brood, seven frames 60% full). b) twelve standard frames well covered with bees (approximately 30,000 bees) c) at least three full-depth frames of honey d) a high quality laying queen e) sufficient room for colony expansion

such hives to

48 Appendix f) be free of American Foul Brood disease (Bacillus larvae), and g) have been treated for Varroa for at least four weeks prior to being introduced to the property.

3. To deliver each instalment of hives to the property within 24 hours of final notice from the grower under Section B, clause 10.

4. To place hives in positions decided in previous consultation with the grower in group sizes of no more than hives.

5. To feed each colony litres of % sugar syrup solution every second morning starting on the second day colonies are in the orchard.

6. To not place/spill sugar syrup outside the hives where it can be collected by foraging bees.

7. a) Within 24 hours of notice from the grower to open and demonstrate bee colony strength of any hives specified by the grower. b) To lend grower and/or auditor effective protective clothing if requested where they wish to accompany the beekeeper under 7a), or under 7c). c) To allow an auditor nominated by the grower to audit the strength of the colonies if requested by the grower (such request not to be made unreasonably).

8. To supply within 24 hours an additional hive(s) to compensate for any hive found to be below the minimum standard, at no extra cost to the grower.

9. To remove the hives within 48 hours of being notified by the grower that they are no longer required.

10. To take all reasonable measures to reduce the number of field bees left behind in the grower’s property(s) when hives are removed.

11. To collect any bee swarms in the property during the flowering period within 48 hours of request by the grower.

12. Replace any hives that swarm within 24 hours.

13. To carry public liability insurance.

14. To inspect the property and any hazards identified by the grower under Section B, clause 8, such inspection to be in daylight before delivery of hives.

SECTION B: GROWER RESPONSIBILITIES

Grower Agrees:

1. To pay a rental sum of $ per hive for a total of hives. GST is to be added to all payments.

2. The total rental is $ . This is payable as to $ on or by (date) and a final payment of $ by the 20th of the month following removal of hives from the property.

3. To pay 1.5% per month (or part thereof) interest on amounts unpaid after due dates.

4. To liaise with the beekeeper well in advance of hive delivery and allow beekeeper prior inspection of the property in daylight.

5. To provide a suitable place to locate hives. This site must be readily accessible to a truck and other vehicles used in handling and servicing the colonies and be in a sheltered, sunny position.

6. To provide the beekeeper with a map of the property well before delivery of hives showing the positions in which hives are to be placed, and the number of hives to be placed at each location. The positions will be as agreed under Section A, clause 4.

7. To be present, or nominate an appropriate person to be present, when the beekeeper inspects under Section A, clause 13, and when hives are delivered and removed (to assist with locating sites).

Appendix Appendix 49 8. To advise the beekeeper in writing of any property hazards including drains, orchard wires, ditches, irrigation pipes, and any other hazard, and to clearly identify the location and nature of such hazards.

9. To allow the beekeeper entry onto the property at a reasonable time whenever necessary to service the bees.

10. To give the beekeeper at least 48 hours first notice and 24 hours final notice that hives are required to be placed in the property.

11. Not to shift, examine, or disrupt bee access to or from hives without the beekeeper’s approval.

12. To give beekeeper at least 48 hours notice to remove hives from property.

13. To abide by Section 49 of the 1996 Hazardous Substances and New Organisms Act and Section 14 of the Pesticide Regulations 1983 of the Pesticides Act 1979.

14. To comply with bee toxicity warnings on agrichemical labels.

15. Not to spray any bee-toxic chemical while the hives are or the property, and in so far as is reasonably practicable, to avoid spraying any insecticide in the ten days prior to hives being shifted into the property.

16. To avoid spraying any agrichemicals between 08:00 and 17:00 hours when large numbers of bees are foraging, in so far as is reasonably practicable.

17. To provide the beekeeper with at least 24 hours notice if anything is to be sprayed on the property while hives are present and to flush any insecticide or other bee-toxic chemical from tanks and spraying equipment before spraying while hives are on the property.

18. To dispose of any insecticide-contaminated liquid or other bee-toxic material so that bees cannot contact or drink it.

19. To give adjoining land owners notice of intent to bring in hives at least ten days before the hives are moved into the property and notice of the full period that the hives may be present.

20. To advise beekeeper within 12 hours if a significant number (one cup or more) of dead bees are seen near the entrance of any hive.

21. To avoid irrigating flowering crops while bees are foraging and to ensure irrigators will not overrun and drench hives.

PERFORMANCE

Neither party shall be responsible for failure to comply with the terms of this agreement where such failure to comply results from causes beyond the reasonable control of that party, provided however that this shall not relieve the grower from liability to make payment for services performed.

ARBITRATION

a) If the grower is dissatisfied with the quality of hives supplied his first recourse shall be to the beekeeper. Such complaints shall be lodged as soon as possible and in no case after the hives are removed from the property.

b) In the event of any unsettled dispute between the beekeeper and grower both parties agree to abide by the decision of a mutually agreed upon independent arbitrator.

ASSIGNMENT OR TRANSFER

This agreement is not assignable or transferable by either party, except that the terms hereof shall be binding upon a successor by operation of law to the interest of either party.

50 Appendix IN WITNESS THEREOF, the parties hereto have executed this agreement the day and year above.

Grower:

Address:

Contact details: (Home) (Mobile)

Beekeeper:

Address:

Contact details: (Home) (Mobile)

(One signed copy each to be retained by the grower and by the beekeeper).

Appendix Appendix 51 References 1. Howlett BG, Donovan BJ 2010. A review of 16. Pausheva ZP 1976. comparative efficiency of New Zealand’s deliberately introduced bee fauna: different methods of hybridization of Buckwheat. current status and potential impacts. New Zealand Pollination of Entomophilus Agricultural Crops by Bees: Entomologist 33: 92-101. 334-338.

2. Donovan BJ 2007. Apoidea (Insecta: Hymenoptera). 17. Phillips EF, Demuth GS 1922. Beekeeping in the Fauna of New Zealand (57). Buckwheat region. U.S. Department of Farmers Bulletin 1216: 22pp. 3. Wolfenbarger DO 1962. Honey bees increase squash yields. Fla. Agr. Expt. Sta. Sunshine State Agr. 18. Free JB 1993. Insect Pollination of crops. San Res. Rpt. 7(1): 15,19. 310. Diego, ACADEMIC PRESS INC.

4. Goodwin RMTH, A. 1991. Feeding sugar syrup 19. Bjorkman T 1995. Role of honey bees (Hymenoptera: to honey bee (Apis mellifera L.) colonies to increase Apidae) in the pollination of Buckwheat in Eastern North kiwifruit pollen collection: Effect of frequency, quantity America. Journal of Economic Entomology 88(6): 1739- and time of day. Journal of Apicultural Reserach 30: 1745. 41-48. 20. Free JB 1966. The pollination requirements of 5. Roberts D 1956. Sugar sprays aid fertilization of broad beans and field beans. Agric. Sci. 66: 395-397. plums by bees. New Zealand Journal of Agriculture 93 (206-207). 21. Wilson R 1991. A noisy spring without pests - balancing conflicting claims of society. Pesticides in the 6. Zyl HL, van Strydom DK 1968. The problem of poof Next Decade: The Challenges Ahead: 1-6. fruit set of Packham’s Triumph pear trees. The Decious Fruit Grower 18: 121-123. 22. Williams IH, Martin AP, Clarke SJ 1990. Pollination requirements of linseed (Linum usitatissimum). The 7. Goodwin RMH, H 1998. Attracting bees by spraying Journal of Agricultural Science 115: 347-352. crop with sugar syrup. New Zealand Beekeeper 11: 10- 11. 23. Spiss L, Hittle CN 1979. Effect of geitonogamic pollinations on self-incompatibility in birdsfoot trefoil 8. Free JB 1965. Attempts to increase pollination by (Lotus corniculatus L.). Acta Agraria et Silvestria, Agraria spraying crops with sugar syrup. Journal of Apicultural 18(2): 257-265. Research 1: 61-64. 24. Silow RA 1931. Self fertility of Lotus spp. Bulletin of 9. Goodwin RMH, H. 1998. Attracting bees by the Welsh Plant Breeding Station 12: 234-240. spraying crop with sugar syrup. The New Zealand Beekeeper December 11: 10-11. 25. Morse RS 1958. The pollination of Birds-foot trefoil. Proceedings of the 10th international Congress of 10. Mayer DF, Britt RL, Lunden JD 1989. An evaluation Entomology 4: 951-953. of BeeScent as a honeybee attractant. Good Fruit Grower 40(6): 40. 26. Badger KL, Anderson SR 1962. Effect of pollen and nectar collecting honey bees on the seed yield of 11. Mussen EC, Julio, L.; Lopez, E.; Peng, C.V. S birdsfoot trefoil, Lotus corniculatus. Crop Science 2: 2004. Effects of selected fungicides on growth and 148-149. development of larval Honey bees, Apis mellifera l. (Hymenoptera: Apidae). Environmental Entomology 27. Kubisova-Kropacova S, Nedbalova V 1975. A study 33(1152-1154). of the relationship between the honeybee and birdsfoot trefoil. Pol’nohospodarstvo 21(7): 560-567. 12. Manandhar DNL, G S 1980. Blossom sprays and their effect on fruit set. The Orchardist of New Zealand. 28. Palmer-Jones T, Forster IW 1972. Measures to 53: 269, 271-272. increase the pollination of lucerne (Medicago sativa Linn.). New Zealand Journal of Agricultural Research 13. Goodwin RM, McBrydie H 1999. Effect of 15: 186-193. surfactants on honey bees. New Zealand Kiwifruit Journal 135: (28-29). 29. Gurr L 1974. The role of bumblebees as pollinators of red clover and lucerne in New Zealand: a review and 14. Fluri P.; Frick R 2002. Honey bee losses during prospect. Proceedings of the New Zealand Grassland mowing of flowering fields. Bee World 83: 109-118. Association 36(1): 111-122.

15. Darwin C 1876. the effects of cross and self fertilisation in the vegetable kingdom. London, Murray.

52 Appendix 30. Langridge DF, Goodman RD 1982. Honeybee 42. Howlett, B.G., M.K. Walker, R. Rader, R.C. Butler, pollination of oilseed rape, cultivar Midas. Australian L.E. Newstrom-Lloyd and D.A.J. Teulon 2011. Can Journal of Experimental Agriculture and Animal insect body pollen counts be used to estimate pollen Husbandry 22: 124-126. deposition on pak choi stigmas? New Zealand Plant Protection, 64: 25-31. 31. Manning R, Boland J 2000. A preliminary investigation into honey bee (Apis mellifera) pollination of 43. Rader, R., B.G. Howlett, S.A. Cunningham, D.A. canola (Brassica napus cv. Karoo) in Western Australia. Westcott and W. Edwards 2012. Spatial and temporal Australian Journal of Experimental Agriculture 40(3): variation in pollinator effectiveness: do unmanaged 439-442. insects provide consistent pollination services to mass flowering crops? Journal of Applied Ecology, 49: 126- 32. Page-Weir NEM, Goodwin RM, McBrydie HM, Cox 134. HM 2008. Honey bee pollination efficiency of carrot and radish seed crops. Ruakura, HortResearch Client 44. Howlett, B.G. 2012. Hybrid carrot seed crop Report No. 25933. pollination by the fly Calliphora vicina (Diptera: Calliphoridae). Journal of Applied Entomology. 136: 33. Free JB 1965. The ability of bumble bees and 421-430. honeybees to pollinate red clover. Journal of Applied Ecology 2: 289-294. 45. Klein, A.M., B.E. Vaissiere, J.H. Cane, I. Steffan- Dewenter, S.A. Cunningham, C. Kremen and T. 34. Holzschuh, A., J.H. Dudenhoffer, and T. Tscharntke 2007. Importance of pollinators in changing Tscharntke. 2012. Landscapes with wild bee habitats landscapes for world crops. Proceedings of the Royal enhance pollination, fruit set and yield of sweet cherry. Society of London. Series B, Biological Sciences, 274: Biological Conservation, 153: 101-107. 303-313.

35. Howlett, B.G., L.J. Evans, M.K. Walker, R.C. Butler 46. Walker, M.K., B.G. Howlett, and R.C. Butler and A. Deverall, 2010. The effectiveness of honey 2008. The effect of landscape features on pollinator bees and other insects as pollinators of hybrid carrot distribution in a Canterbury agroecosystem. Crop & seed fields. Plant & Food confidential report for the Food Confidential Report No 2102 for the Foundation Foundation for Arable Research No, 4284. 47 p. for Arable Research. 25 p.

36. Howlett, B.G., R.C. Butler, W.R. Nelson and B.J. 47. Rader, R., W. Edwards D.A. Westcott, S.A. Donovan 2012. Impact of climate change on crop Cunningham and B.G. Howlett 2011. Pollen transport pollinator activity in New Zealand – DRAFT, Confidential differs among bees and flies in a human-modified report for the Ministry for Primary Industries. 45 p. landscape. Diversity and Distributions. 17: 519-529.

37. Howlett, B.G., M. K. Walker, L.E. Newstrom-Lloyd, 48. Donovan, B.J. and R.P. Macfarlane, 1984. Bees B.J. Donovan and D.A.J. Teulon 2009. Window traps and Pollination., in New Zealand pest and beneficial and direct observations record similar arthropod flower insects, R.R. Scott, Editor. Lincoln University College visitor assemblages in two mass flowering crops. of Agriculture: Christchurch. p. 247-270. Journal of Applied Entomology, 133: 553-564. 49. Donovan, B.J., B.G. Howlett, and M.K. Walker, 38. Macfarlane, R.P. and A.M. Ferguson, 1984. 2010 Relocation and establishment of nesting Kiwifruit pollination: a survey of the insect pollinators populations of the native bee Leioproctus huakiwi in New Zealand. V Symposium International sur la Donovan (Hymenoptera: Colletidae). New Zealand Pollination., 367-373. Entomologist. 33: 109-113.

39. Walker, M.K., B.G. Howlett, and R.C. Butler, 2007. 50. Howlett, B.G. 2009. Pollination performance Abundance and efficiency of pollinators of pakchoi of Calliphora vicina on a carrot Seed Crop. Plant & and radish seed in a New Zealand trial. Crop & Food Research, Confidential Report No. 2382 for the Food Research Confidential Report No. 1948 for the Foundation for Arable Research. 21 p. Foundation for Arable Research. 61 p. 51. Singh, P. 1985. Rearing Calliphoridae, in 40. Howlett, B.G. and G.O. Lankin, 2005. A survey of Calliphoridae (Insecta: Diptera). Fauna of New Zaeland white clover flower visitors in Central Canterbury: the J.P. Dear, Editor. p. 19-20. range of potential pollinators. Crop & Food Confidential Report No. 1486 for the Foundation for Arable 52. Howlett, B.G. and W.R. Nelson 2009. The potential Research. 33 p. of Calliphorids as managed pollinators: a pilot study. 2009, Plant and Food Research Confidential report No 41. Rader, R., B.G. Howlett, S.A. Cunningham, D.A.J. 2344: 19 p. Teulon, L.E. Newstrom-Lloyd, M.K. Walker and W. Edwards, 2009. Alternative pollinator taxa are equally 53. Wilson, D.J., P.J. Gerard, and J.E.de Villiers 2009. efficient, but not as effective as the honeybee in a mass Preventing rat-tailed maggot incursion into dairy sheds. flowering crop. Journal of Applied Ecology, 46: 1080- New Zealand Plant Protection. 62: 99-102. 10 87. ®

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