**2. A brief presentation of the honeybee**

#### **2.1 A social insect**

The honeybee is a eusocial insect, living in colonies that can be made of up to 50,000 individuals, including a fertile female, the queen, workers which are sterile females, males (drones), and brood (eggs, larvae and pupae). The workers do various tasks in succession during their lifetime depending on their age and the environment, such as maintaining and building combs, feeding larvae, feeding and grooming the queen and other members of the colony, ventilation, reception and storing of collected food, and defending the nest. From about 21-day old on to their death, the main part of their activity is outside the hive, gathering pollen, nectar, water and propolis. By visiting flowers, forager bees provide the colony with nectar and pollen, which are subsequently transformed into honey and "bee bread", respectively. Survival of the colony depends on the reserves made from these supplies in the combs, especially during the winter.

### **2.2 Nectar and pollen gathering**

Nectar and pollen gathering often occur together as the flowers of most plant species are hermaphrodites and provide both resources. But foraging bee can also collect only one resource and be strict nectar or pollen collector. Indeed, some plants produce on one hand little or no nectar, but offer an abundance of pollen (e.g. kiwifruit *Actinidia deliciosa* A. Chev.; Vaissière et al., 1996), while others produce large echinate pollen grains that honeybees cannot pack on their hind legs (e.g. cotton *Gossypium hirsutum* L; Vaissière & Vinson, 1994). In addition it was demonstrated that a tendency to prefer pollen foraging is genetically determined (Page et al., 1995). Despite this, for reasons of adaptability to the environment and to the colony needs, honeybee worker can rapidly change their foraging activities based on mechanisms of communication and learning.

#### **2.3 Foraging efficiency depends on communication and learning**

At the colony level, honeybees are communicating through dances to exchange information about the location of food sources which have been located by scout workers (von Frisch, 1967). Also, the foraging activities vary according to the colony needs communicated by trophallaxis (exchange of food and secretions from mouth to mouth) and exchanges of pheromones inside the colony (Winston, 1987). At the individual level, the foraging worker can remember the configuration of the foraging area and the characteristics of the food sources (Menzel et al., 1993). This last point raises the question of the appreciation of flower attractiveness by the bees. Bees are first attracted by floral odours which can be perceived from far away (Loper & Waller, 1970). But overall it is the association between the reward (quantity and quality of pollen or nectar supplied) and the characteristics of the flower such as odour, colour, and shape, that enables the learning and subsequent recognition of a flower. A flower type providing little resources will be quickly abandoned to the expense of a more profitable type of flower, if the food supply in the environment allows it (Winston, 1987).

Under experimental conditions, honeybees prefer nectar containing saccharose (Waller, 1972) and are able to assess differences in sugar concentrations in the order of 5% (Jamieson & Austin, 1956). They prefer concentrated nectars that range in sugar content between 15% to 50% (Jamieson & Austin, 1956; Sigurdson, 1981a, 1981b; Waddington & Kirchner, 1992; Waller, 1972), but they avoid nectars which are too viscous and thus make their collection difficult. Nectar accessibility also influences floral choice by nectar foragers as nectar has to be within reach given their proboscis length. Honeybees have an average tongue length of 6 mm and can often gather little nectar from flowers with deep corolla such as those of red clover (*Trifolium pratense* L.) and several other Fabaceae (Jablonski, 2001).

For pollen, the protein content does not seem to be detected by the foragers (Maurizio, 1954). Pollens which have the highest protein content are not necessarily those which are the most sought after or the most appetizing. Thus, the fact that a pollen is collected by honeybee foragers does not provide information about its nutritive value. Indeed, pollen from female kiwifruit vines is readily collected by honeybees while its nutritive value is very low (Jay & Jay, 1993). It is not easy to establish a link between the protein content and the nutritive value of a given pollen, because pollen grains contain many other elements besides proteins, and also because their proteins are more or less digestible. Digestibility essentially depends on the thickness and ornementation of the pollen wall. Moreover, a lack of rich pollen in the environment can result result in workers collecting pollen completely deficient of any nutritive value (Louveaux, 1959; Maurizio, 1954; Wille et al., 1985). Also accessibility is an important factor for pollen collection since honeybees cannot harvest large pollen grains which are echinate with long spines such as those of cotton and several other Malvaceae (Vaissière & Vinson, 1994). And the overall appetence of pollen is also influenced by the presence or absence of phago-stimulants or repulsive compounds (Pernal & Currie, 2000).

#### **2.4 Flower loyalty and foraging areas**

372 Ecosystems Biodiversity

it is essential to understand the relationship between this insect and the melliferous or polleniferous flora in their environment. This is the main goal of this review and we also describe some available data on the effects of diet on some biological functions of bees so as to build a scientific background for agro-environmental measures protecting floral

The honeybee is a eusocial insect, living in colonies that can be made of up to 50,000 individuals, including a fertile female, the queen, workers which are sterile females, males (drones), and brood (eggs, larvae and pupae). The workers do various tasks in succession during their lifetime depending on their age and the environment, such as maintaining and building combs, feeding larvae, feeding and grooming the queen and other members of the colony, ventilation, reception and storing of collected food, and defending the nest. From about 21-day old on to their death, the main part of their activity is outside the hive, gathering pollen, nectar, water and propolis. By visiting flowers, forager bees provide the colony with nectar and pollen, which are subsequently transformed into honey and "bee bread", respectively. Survival of the colony depends on the reserves made from these

Nectar and pollen gathering often occur together as the flowers of most plant species are hermaphrodites and provide both resources. But foraging bee can also collect only one resource and be strict nectar or pollen collector. Indeed, some plants produce on one hand little or no nectar, but offer an abundance of pollen (e.g. kiwifruit *Actinidia deliciosa* A. Chev.; Vaissière et al., 1996), while others produce large echinate pollen grains that honeybees cannot pack on their hind legs (e.g. cotton *Gossypium hirsutum* L; Vaissière & Vinson, 1994). In addition it was demonstrated that a tendency to prefer pollen foraging is genetically determined (Page et al., 1995). Despite this, for reasons of adaptability to the environment and to the colony needs, honeybee worker can rapidly change their foraging activities based

At the colony level, honeybees are communicating through dances to exchange information about the location of food sources which have been located by scout workers (von Frisch, 1967). Also, the foraging activities vary according to the colony needs communicated by trophallaxis (exchange of food and secretions from mouth to mouth) and exchanges of pheromones inside the colony (Winston, 1987). At the individual level, the foraging worker can remember the configuration of the foraging area and the characteristics of the food sources (Menzel et al., 1993). This last point raises the question of the appreciation of flower attractiveness by the bees. Bees are first attracted by floral odours which can be perceived from far away (Loper & Waller, 1970). But overall it is the association between the reward (quantity and quality of pollen or nectar supplied) and the characteristics of the flower such as odour, colour, and shape, that enables the learning and subsequent recognition of a flower. A flower type providing little resources

resources and benefiting the beekeeping industry.

supplies in the combs, especially during the winter.

on mechanisms of communication and learning.

**2.3 Foraging efficiency depends on communication and learning** 

**2.2 Nectar and pollen gathering** 

**2. A brief presentation of the honeybee** 

**2.1 A social insect** 

Honeybees respond to groups of stimuli and rewards that are characteristic of each floral type. Both pollen and nectar gathering by a forager are made more efficient by the fact that the bee learns the handling of a floral type that it finds profitable and then remains loyal to this type for as long as it is available. Indeed, one can observe specialized foraging positions on most flower types (Robinson, 1989) and a strong area loyalty. Indeed, the individual foraging area of honeybee foragers is limited to an area of ca. 100 m2 (Singh, 1950).

Yet one must not confuse the foraging area of an individual forager with that of the colony as a whole. Within the colony, different foraging groups target different sites. In an environment where nectar is abundant, the foraging area of a colony is on average ca. 2 km radius around the hive. And 90% of bees dancing gather pollen in a radius of less than 5 km from the hive (Beekman & Ratnieks, 2000; Steffan-Dewenter & Kuhn, 2003), that is a survey area of about 80 km2. When needed, a colony can expand considerably its foraging area. Beekman & Ratnieks (2000) noted that 50% of the foraging bees foraged at > 6 km, and 10% at > 9 km. Based on these results, the flowering areas targeted at the honeybees could be safely created and protected within a 1 km radius around the hive. But in intensively farmed landscapes that are flower-poor, the foraging activity can take place

Why Enhancement of Floral Resources in Agro-Ecosystems Benefit Honeybees and Beekeepers? 375

Pollen is produced and released by the anthers and it can be more or less accessible to the floral visitors depending on floral morphology. Honeybees rarely eat it in its natural state. Rather, it is first aggregated with nectar or diluted honey to form pellets (Vaissière & Vinson, 1994). Pellets are then placed in the cells, packed and covered with honey and it is

Fresh pollen contains proteins and amino acids, but also carbohydrates and lipids, including sterols. Each type of pollen can be characterised by its global caloric value, its protein content as % of dry matter, its nitrogen content, amino acid composition (classified as essential or non essential), and starch, sugar and lipid content as well as its vitamin and mineral elements. Specific techniques are needed for each of these measurements and results often differ between different authors. It is therefore difficult to obtain the complete biochemical profile for the pollen of a given plant species (Stanley & Linskens, 1974). For example, dandelion pollen (*Taraxacum campylodes* G.E. Haglund), has a protein content that ranges from 9.2 to 19.2% of its dry weight, depending on the authors, its main lipids are made up linoleic and palmitic acid, and its mineral element composition is known as well. We also know that it is deficient in arginine and is missing essential amino acids such as tryptophane and phenol-alanine (Loper & Cohen, 1987). A few other complete data exists on pollen of gymnosperms and corn *Zea mays* L., but generally such complete data sets are rare

Large quantities of food are required by a honeybee colony. Food gathering at the height of the season must be enough to feed 50,000 workers and 9,000 larvae. Such colony may have an annual nectar budget of about 120 kg and a pollen budget of 20 kg (Seeley, 1995). It may stock from 60 to 80 kg of honey per year (Erber, 1992; Rosov, 1944; Seeley, 1995; Weipple, 1928. The larva of a worker honey bee consumes about 140 mg of honey during its

An active foraging worker uses 0.5 mg of honey per km flown, and it can fly as much as 800 km during its lifetime (Gould & Gould, 1988). Others authors estimated that a forager consumed 11.5 mg of sugars per hour in flight, and only 0.7 mg per hour when inside the hive (Heinrich, 1979; Olaerts, 1956). During winter, bee activity is reduced, but the cluster must maintain a constant temperature in the centre of the nest of 34°C to 36°C, which requires a large energy expenditure. Thus, an average sized colony needs to stock ca. 25 kg of honey for winter consumption. Overall, the annual needs of a colony are estimated at about 80 kg of honey and 20 kg to 40 kg of pollen depending upon the authors (Crailsheim

A colony gathers from 15 to 55 kg of pollen per year (Eckert, 1942; Hirschfelder, 1951; Louveaux, 1958; Ribbands, 1953; Seeley, 1985). Nursing bees are the ones that consume the most pollen as they eat ca. 60 mg of pollen over 10 days (Pain & Maugenet, 1966), to develop their hypopharyngeal glands which produce the 42 mg of food consumed by larvae during the first 5 days of larval development (Haydak, 1968). This food given by nursing bees constitutes a major part of the protein supply consumed by larvae since pollen is processed into brood food and only 5% of the protein derived from pollen are directly fed to larvae

transformed by lactic fermentation to make « bee bread ».

and does not allow a multi-criteria classification of pollen types.

development (Rosov, 1944; Seeley, 1985; Weipple, 1928; Winston, 1987).

**3.3 Nectar and pollen budget of the colony** 

et al., 1992; Louveaux, 1954; Winston, 1987).

(Babendreier et al., 2004).

**3.2 Pollen** 

readily over several kilometres around the hive (Decourtye et al., 2008; Steffan-Dewenter & Kuhn, 2003).
