**5. What are the benefits of diet diversity?**

376 Ecosystems Biodiversity

Clearly, the survival and development of honeybee colonies are influenced by the regularity, quality and quantity of the nectar and pollen supply. Within intensively farmed agricultural landscapes, nectar- and pollen-producing crops may provide a narrow window with mass flowering followed by a dearth of pollen and nectar resources. A typical example occurs with oilseed crops such as rape and sunflower (*Helianthus annuus* L.) for which nectar and pollen resources are usually abundant during the blooming, but only for a short period. The subsequent temporal dearth of resources could be partially filled simply by the creation and protection of additional non-cropped areas such as field margins (strips bordering crop fields), hedgerows (linear scrub along field boundaries), woodlands, ponds,

But, for both pollen or nectar , it is long and difficult to assess precisely their production in quantity and quality. Indeed, one must not only take into account the effects from the environment but also the effects of the genetic make-up of the plants at the species and variety levels. This last point is important to objectively assess the best flowering plant for

The majority of the protein intake of larvae comes from the hypopharyngeal gland secretions of nurse bees, and the development of these glands depends on their pollen diet. The development of hypopharyngeal glands is not dependant upon the essential amino acids present in the pollen consumed, but on the total quantity of protein ingested (Pernal & Currie, 2000). Therefore, a situation of pollen deficiency may have detrimental effects on the nurse bees' tasks and brood care, resulting in undernourished larvae (Blaschon et al., 1999). When such deficiencies occur, the nurse bees may also reduce the number of larvae to feed and cannibilize the eggs (Schmickl & Crailsheim, 2001). The young larvae are eliminated for the benefit of the older larvae which need more pollen input. In the case of extended pollen deficiency, another strategy is to reduce overall larval care (Blaschon & Crailsheim, 2001). Finally, pollen feeding during the larval stage has an important impact on the traits of the adults as it may determine the size of the future adult (Roulson & Cane, 2000) and its life

Ovary development is another major process influenced by pollen intake. Experiments have been carried out on worker bees kept in isolation without queen, in order to evaluate their capacity to develop ovaries, a physiological process highly dependent protein utilization and pollen quality. This method has shown that pollen from apple (*Malus domestica* Borkh.) or sweet clover (*Melilotus* spp.) is favourable to ovary development whereas pollen from pine (*Pinus* spp.) is not and that of sunflower is below average (Pernal & Currie, 2000). Also, a diet consisting of several pollens of different nutritive value is not equivalent to their average nutritive value ( Taséi & Aupinel, 2008; Alaux et al., 2011). We can also assume that a pollen of low nutritional value, like that of dandelion, can be compensated by mixing it with another pollen that has a higher nutritional value for reproductive needs (Genissel et al., 2002). This highlights the importance of avoiding putting bees in a situation where they do not have sufficient floral

Finally, it has recently been shown that a high concentration of pollen lipids (mainly linoleic, myristic and dodecanoic acids) protects the brood nest from certain bacteria such as *Paenibacillus larvae* and *Melissococcus pluton* which are the pathogenic agents responsible for

variety, as is often the case amidst large intensive agricultural landscapes.

ditches and fallow farm fields (Decourtye et al., 2010).

**4. Impact of pollen supply on the life of the colony** 

bees, though it is rarely known.

expectancy (Schmidt et al., 1987).

Within complex landscapes, honeybee colonies normally collect and consume pollen from a large array of plant species (Dimou & Thrasyvoulou, 2009; Louveaux, 1959; Severson & Parry, 1981). This generalist behavior for pollen collection (polylecty), as opposed to oligolecty or monolecty in other bee species, is further supported by experimental evidence that honeybees feed preferentially on plurispecific pollen mixtures rather than pollen from a single species (Schmidt, 1984). These results support the postulate that honeybees select a mixed diet when given a choice. However, today intensive agricultural landscapes most often provide colonies with a low variety of plant species. Indeed, honeybees used for the pollination service of large areas may even be forced to feed mainly on a single flowering crop, like sunflower that has pollen with a poor nutritional value and sesame that has pollen which contains only low levels of phagostimulants (Schmidt et al., 1995). Such practices may be stressful for colony health. In those cases, the presence of additional floral or food sources could to reduce these potential problems.

The protein content of pollen (2.5 to 61%), its amino acid composition, its lipid content (1 to 20%), and that of starch, sterols, vitamins and minerals vary tremendously among plant species (Roulston & Buchmann, 2000; Roulston & Cane, 2000; Stanley & Linskens, 1974). Therefore, regardless how much monospecific pollen is consumed, it might miss nutrients essential to the health of honeybee colonies. The deficiency of a given pollen in essential nutrients could be compensated for by a more diverse pollen diet. Indeed, a mixed pollen diet increases the lifespan of honeybees as compared to a monospecific pollen diet (Schmidt, 1984; Schmidt et al., 1987). In addition, a diversified pollen diet might help the bees to fight against pathogens. Alaux et al. (2010) found that a diverse pollen diet can actually enhance some immune functions in worker honeybees. For example, their production of glucose oxidase, an enzyme involved in the synthesis of the antiseptic hydrogenperoxide in honey and brood food, was 40% higher in honeybees fed with pollen from a variety of plants compared to those fed with pollen from a single plant species – even if this monofloral diet had a higher protein content. However, whether polyfloral diets might increase the actual resistance to diseases and pathogens remain to be tested. In bumblebees *Bombus terrestris*, larvae fed with a mixed pollen diet were heavier than larvae fed with monofloral pollen of equivalent or higher protein content (Taséi & Aupinel, 2008), and so we might also expect a similar beneficial effect of a diverse pollen diet on the health of honeybee larvae.

As stated previously, increasing the number of pollen species in the diet probably provides a buffer against deficiencies of specific nutrients (Schmidt, 1984) as well as the presence of toxic compounds in some pollen (Mesquita et al., 2010). Indeed, several studies have demonstrated the importance of some specific nutrients in bee health. For example, de Groot (1953) found that 10 essential amino acids in specific proportions are required for optimal honeybee health: arginine, histidine, lysine, tryptophan, phenylalanine, methionine, threonine, leucine, isoleucine, and valine. Those essential amino acids cannot be synthesized *de novo* by honeybees and therefore need to be supplied directly in the diet. Some fatty acids, found at different levels in pollens ( Manning, 2001; Singh et al., 1999), can also be beneficial

Why Enhancement of Floral Resources in Agro-Ecosystems Benefit Honeybees and Beekeepers? 379

demography. The pollen of some other grasses usually grown for fodder (e.g. *Setaria italica* L.P.Beauv.) are also actively foraged by honeybees during periods of pollen dearth, but this pollen does not appear satisfactory based on its nutrient content. In this regard, wild plant species such as wild cherries (*Prunus avium* L.*)* or wild poppies offer proteinand lipid-rich pollens, and enable a stable development of colonies in the spring, when

In intensive agricultural landscapes where semi-natural habitats and weeds are sparse, floral schemes, i.e. management of flowering areas, might provide ecological compensation features for honeybees (Decourtye et al., 2010). They are intended foremost to ensure population sustainability during the periods of food shortage rather than to foster honey production. Such floral schemes might also contribute to the conservation of some wild bee species. Indeed Fabaceae, which are also visited extensively by wild bees, are often preferred in the agri-environmental schemes of farmers, since their management is wellknown and their seeds are generally fairly cheap. The efficiency of floral schemes to provide pollen resources to colonies can be assessed by analyzing the pollen pellets obtained for example with pollen traps. And the benefits for beekeepers are clear as colonies that have had access to more regular resources during a given season produced more brood and

**7. Consideration of the landscape factors in agro-environmental actions** 

Some authors have questioned the effectiveness of agro-environmental schemes because their beneficial effects on target species do vary from one study to another (Kleijn et al., 2006). The same holds true for floral landscape enhancements dedicated specifically to bees (Dicks et al., 2010). Yet there is a growing body of evidence that the seemingly unpredictable effectiveness of floral schemes is actually dependent on the landscape context in which it is established (Decourtye et al., 2010). Landscape context typically refers to the degree of land use by humans. Intensive, simplified, agricultural landscapes are distinguished from complex landscapes with greater amounts of semi-natural habitats or habitat diversity. A handful of studies have specifically measured the influence of landscape context on the efficiency of experimental flower patches in attracting bees (Heard et al., 2007; Kohler et al. 2008; Steffan-Dewenter et al., 2002). However, to date, no consistent conclusion can be drawn on such floral schemes because different field protocols have been used with

Only one of these studies (Steffan-Dewenter et al., 2002) focused on honeybees and it reported a weak pattern of context-dependent floral scheme effectiveness. Authors have implanted experimental flower patches in a variety of landscape contexts, and have monitored honeybee foraging activity at those patches. Flower patches tended to attract fewer honeybees when implanted in landscapes characterized by a higher amount of seminatural habitats (field and forest margins, hedgerows, fallows and extensive grasslands) within a 3-km radius. Conversely, foraging activity at flower patches located in more intensive agricultural landscapes was greater, indicating that honeybees compensated for

the lack of natural resources by making a disproportionate use of the floral schemes.

Yet, theoretical evidence suggests that honeybees would rather respond positively to the presence of semi-natural habitats. In particular, hedgerows, forest margins and other linear landscape elements may be used as visual landmarks by honeybees to direct their flight

the blooming of the oilseed rape is over.

**promoting flowering areas** 

larger populations in the following year (Decourtye et al., 2008).

different study species and at different spatial scales.

to honeybees due to their antimicrobial properties (Hornitzky, 2003). Pollen and nectar, beside being the primary food source for bees, also contain phytochemicals and are often rich in carotenoids, flavonoids, alkaloids and phenolic compounds that have antioxidant properties and antimicrobial activity (Adler, 2000; Balch & Balch, 1990; Basim et al., 2006; Campos et al., 2003; Leblanc et al., 2009; Morais et al., 2011). Sustaining the diversity of flower resources in the landscape might increase the chances for bees to find all those beneficial nutrients, and also to avoid or provide an alternative to toxic nectar and pollen. Indeed, some plant components are non-nutritive but toxic to honey bees (Barker, 1990), like the sugars galactose, arabinose, xylose, melibiose, raffinose, stachyose and lactose that can be found in pollen and nectars of some plants (Barker, 1977).

#### **6. Availability of food resources in the environment: a question of temporal and spatial scales**

Currently, there is no temporal continuity in floral resource availability within intensively farmed agricultural landscapes. In Europe, mass flowering crops providing bees with nectar or pollen are often limited to maize, sunflower and oilseed rape at large landscape scales in cereal farmland systems (Decourtye et al., 2010). Among these three, maize provides the greatest quantities of pollen collected by honeybees, due to its long-lasting availability and good accessibility to foragers (Charrière et al., 2010; Odoux et al., 2004; Vaissière & Vinson 1994). On the other hand, oilseed rape and sunflower can be important nectar sources and provide substantial honey crops. This abundance of resource often has a strong impact on colony dynamics as the high intake of food during the flowering of the oilseed rape induces a rapid demographic increase in the colonies. Unfortunately, these young and populous bee cohorts are likely to suffer from food resource scarcity after the mass flowering ends.

Beekeeping takes place in a great variety of agrosystems and is therefore exposed to a wide range of colony management issues. The foraging ecology of honeybees has to be considered within temporal and spatial scales as well. Cereal plains often include also seminatural habitats, which are able to supply food resources for honeybees during periods of food shortage. Therefore, bees shift foraging habitats on a seasonal basis. The capacity of these agricultural environments to sustain honeybee colonies between crop mass-flowering periods depends on the presence of wild plants in hedgerows, grasslands and woody habitats. In other words, the carrying capacity of the landscapes is expected to increase with its structural complexity (Steffan-Dewenter & Kuhn, 2003). During periods of food shortage, bees can cover larger distances to fetch food, e.g. beyond 5 km away from the colony (Beekman & Ratnieks, 2000; Odoux et al., 2009). In addition, some weeds in cereal fields probably become keystone resources at this time. For instance, bees may collect on a daily basis more pollen on poppy flowers *(Papaver rhoeas* L.*)*, than they would on maize (Odoux, 2010). The presence of this adventicious species is clearly dependant on agricultural practices such as crop rotation, soil preparation, and herbicide use.

The nutritional carrying capacity of farming landscapes for honeybees varies a lot, as food resources vary in quantity and quality. The cultivated lavender hybrid (*Lavandula x intermedia* Emeric ex Loisel) is an attractive melliferous crop for beekeeping, but it is malesterile so that it does not provide any pollen at all. On the contrary, apple orchards produce an abundant pollen that is rich in proteins (Louveaux, 1959). Abundant intakes of sunflower and maize pollens, which are particularly poor in protein and lipid content (Feuillet et al., 2008; Roulston & Cane, 2000), are expected to exert stresses on colony

to honeybees due to their antimicrobial properties (Hornitzky, 2003). Pollen and nectar, beside being the primary food source for bees, also contain phytochemicals and are often rich in carotenoids, flavonoids, alkaloids and phenolic compounds that have antioxidant properties and antimicrobial activity (Adler, 2000; Balch & Balch, 1990; Basim et al., 2006; Campos et al., 2003; Leblanc et al., 2009; Morais et al., 2011). Sustaining the diversity of flower resources in the landscape might increase the chances for bees to find all those beneficial nutrients, and also to avoid or provide an alternative to toxic nectar and pollen. Indeed, some plant components are non-nutritive but toxic to honey bees (Barker, 1990), like the sugars galactose, arabinose, xylose, melibiose, raffinose, stachyose and lactose that can

**6. Availability of food resources in the environment: a question of temporal** 

Currently, there is no temporal continuity in floral resource availability within intensively farmed agricultural landscapes. In Europe, mass flowering crops providing bees with nectar or pollen are often limited to maize, sunflower and oilseed rape at large landscape scales in cereal farmland systems (Decourtye et al., 2010). Among these three, maize provides the greatest quantities of pollen collected by honeybees, due to its long-lasting availability and good accessibility to foragers (Charrière et al., 2010; Odoux et al., 2004; Vaissière & Vinson 1994). On the other hand, oilseed rape and sunflower can be important nectar sources and provide substantial honey crops. This abundance of resource often has a strong impact on colony dynamics as the high intake of food during the flowering of the oilseed rape induces a rapid demographic increase in the colonies. Unfortunately, these young and populous bee

cohorts are likely to suffer from food resource scarcity after the mass flowering ends.

practices such as crop rotation, soil preparation, and herbicide use.

Beekeeping takes place in a great variety of agrosystems and is therefore exposed to a wide range of colony management issues. The foraging ecology of honeybees has to be considered within temporal and spatial scales as well. Cereal plains often include also seminatural habitats, which are able to supply food resources for honeybees during periods of food shortage. Therefore, bees shift foraging habitats on a seasonal basis. The capacity of these agricultural environments to sustain honeybee colonies between crop mass-flowering periods depends on the presence of wild plants in hedgerows, grasslands and woody habitats. In other words, the carrying capacity of the landscapes is expected to increase with its structural complexity (Steffan-Dewenter & Kuhn, 2003). During periods of food shortage, bees can cover larger distances to fetch food, e.g. beyond 5 km away from the colony (Beekman & Ratnieks, 2000; Odoux et al., 2009). In addition, some weeds in cereal fields probably become keystone resources at this time. For instance, bees may collect on a daily basis more pollen on poppy flowers *(Papaver rhoeas* L.*)*, than they would on maize (Odoux, 2010). The presence of this adventicious species is clearly dependant on agricultural

The nutritional carrying capacity of farming landscapes for honeybees varies a lot, as food resources vary in quantity and quality. The cultivated lavender hybrid (*Lavandula x intermedia* Emeric ex Loisel) is an attractive melliferous crop for beekeeping, but it is malesterile so that it does not provide any pollen at all. On the contrary, apple orchards produce an abundant pollen that is rich in proteins (Louveaux, 1959). Abundant intakes of sunflower and maize pollens, which are particularly poor in protein and lipid content (Feuillet et al., 2008; Roulston & Cane, 2000), are expected to exert stresses on colony

be found in pollen and nectars of some plants (Barker, 1977).

**and spatial scales** 

demography. The pollen of some other grasses usually grown for fodder (e.g. *Setaria italica* L.P.Beauv.) are also actively foraged by honeybees during periods of pollen dearth, but this pollen does not appear satisfactory based on its nutrient content. In this regard, wild plant species such as wild cherries (*Prunus avium* L.*)* or wild poppies offer proteinand lipid-rich pollens, and enable a stable development of colonies in the spring, when the blooming of the oilseed rape is over.

In intensive agricultural landscapes where semi-natural habitats and weeds are sparse, floral schemes, i.e. management of flowering areas, might provide ecological compensation features for honeybees (Decourtye et al., 2010). They are intended foremost to ensure population sustainability during the periods of food shortage rather than to foster honey production. Such floral schemes might also contribute to the conservation of some wild bee species. Indeed Fabaceae, which are also visited extensively by wild bees, are often preferred in the agri-environmental schemes of farmers, since their management is wellknown and their seeds are generally fairly cheap. The efficiency of floral schemes to provide pollen resources to colonies can be assessed by analyzing the pollen pellets obtained for example with pollen traps. And the benefits for beekeepers are clear as colonies that have had access to more regular resources during a given season produced more brood and larger populations in the following year (Decourtye et al., 2008).
