Environmental determinants of bumblebee activity patterns

Am bient temperature, am bient relative humidity, levels of insolation and air movement are recognised as the most important parameters determining the activity patterns of bees. Prys-Jones & Corbet (1991) provide an overview of the activity patterns of British species of bumblebees. Seasonal temperatures affect the timing of bumblebee colony cycles and may be important in defining the limits of a species' range (Williams 1986).

Bees of the family Apidae are facultative heterotherms, possessing the capacity for physiological as well as behavioural thermoregulation. Bumblebees have more pronounced therm oregulatory abilities than honeybees, and share common physiological mechanisms which have undergone intensive study. The physiology of flight and thermoregulation are fairly well understood (Heinrich 1979; Corbet et al 1993). Facultatively endothermie bees are able to raise their body temperature by shivering the thoracic flight muscles: this procedure is known as 'warm-up'. Bumblebees are able to initiate warm-up at lower ambient temperatures than honeybees, so that they have a wider thermal window for foraging activity. Ambient temperature is critical in determining the point at which foraging may begin, as bumblebees will only forage in very low ambient temperatures if the quality of the resource is sufficiently high. Different climatic factors may influence foraging in different ways. For example, nectar-robbing is less temperature-dependent than pollen gathering in B. terrestris on red clover in New Zealand (Wratt 1968).

Under certain conditions bumblebees may show a bimodal activity pattern which peaks in the morning and evening and drops in the middle part of the day due to the danger of overheating and/or in response to increased competition from honeybees (Prys-Jones & Corbet 1991). Bumblebees are large, dark-coloured, well-insulated.

Introduction part I: a review o f the literature

highly active and thus capable of reaching high thoracic temperatures. Overheating is avoided by means of behavioural temperature regulation (such as resting in shade, or evaporating the moisture from a drop of nectar extruded from the crop) or by physiological changes, such as the redirection of blood-flow from the thorax, containing the highly active flight muscle, towards the abdomen (Heinrich 1979).

As well as by shivering the flight muscles, bumblebees are able to raise their body temperature without warm-up, by means of the substrate cycle enzymes fructose diphosphatase (FDPase) and phosphofructokinase (PFKase) in the flight muscle. Substrate cycling maintains thoracic temperatures in non-flying bumblebees and bears an inverse relation to ambient temperature (Clark et al 1976). Non-shivering thermogenesis is energetically cheap compared to standard shivering endothermy, and may even be the most important mechanism for endothermy in bumblebees (Prys- Jones 1986).

Temperature may affect bumblebee activity patterns indirectly, through the nectar secretion patterns of flowers, making them more or less attractive as energy sources. An understanding of foraging patterns therefore needs to consider the influence of temperature, humidity and insolation on nectar characteristics, patterns of nectar secretion, and the attractiveness of flowers through the release of flower volatiles, as well as the direct influences of climate and microclimate on bee activity. Ambient conditions may also affect bumblebee activity through competitive interactions with other organisms: for example the number of B. ruderatus foraging for pollen on red clover and lucerne in New Zealand decreases as ambient temperature rises because of increasing competition from honeybees (Wratt 1968).

The indirect effects of environmental factors on nectar availability may explain why Poulsen (1973), studying bees on field beans in Denmark, obtained lower foraging rates from his study than those obtained by Free (1962) on the same crop in southern England. Poulsen attributed this difference to the lower temperatures prevailing in Denmark, but Free (1968) found that honeybees and bumblebees, once active, work at fairly constant speeds regardless of the direct effects of temperature. Heinrich (1979) stated that "in order to forage optimally, bees must make physiological adjustments that affect foraging rate and energy expenditure".

Because of the energy expenditure and loss of body fluids inevitably consequent upon active flight, bumblebees must ingest sufficient water during the day to replenish their body fluids. Ambient temperature, relative humidity and air movement all influence how much moisture is lost, while the concentration and volume of nectar determine how much water can be regained. Unlike honeybees, bumblebees do not drink and must obtain all fluids from nectar. If the sugar concentration of nectar is very low, as after a fall of rain, it may contain insufficient sugar to meet their metabolic needs (Kauffield et al 1969). On still, hot days, ambient relative humidity may be very low and nectar may become highly concentrated. Viscous or crystalline nectar does not provide sufficient moisture in hot, dry weather conditions, and it is mechanically impossible for a bee to extract it. The increasing viscosity of nectar may contribute to the decrease in bumblebee activity sometimes observed during the middle of the day. Willmer (1982) provides detailed discussion of the importance of insect water balance in diurnal activity patterns.

Interspecific differences in thermogenic abilities and temperature thresholds for activity may account for specific differences in diurnal activity patterns and foraging ecology, particularly between bumblebees and solitary bees (Heinrich 1976). Prys- Jones (1986) hypothesises that, for bumblebees, "interspecific differences in foraging behaviour may be related to the activity o f substrate cycle enzymes", and that the activity of FDPase and PFKase may be of equal or greater importance than proboscis length differences in resource partitioning among sympatric bumblebee species. Studies of warm-up rates suggest that all British Bombus species have similar capacities for standard endothermie shivering (Stone & Willmer 1989). However, there is significant interspecific variation in levels of activity of the substrate cycle enzymes (Newsholme et al 1972). For example, B. lapidarius has a higher threshold temperature for activity on flowers than other species (Corbet et al 1993; Bataw & Willmer 1994 unpublished) than other species, and an unusually high level of FDPase in the thoracic flight muscle (see Sections 1.12 and 5.3). Bumblebee distributions are defined by physiological temperature optima (Williams 1986).

The activity patterns of bees are strongly influenced by light intensity (Corbet et al 1993), although some workers consider that the effect is only pronounced at high levels of insolation (Williams 1986). Bumblebees may be less dependent on clear skies for foraging than honeybees because of their greater capacity for endothermie

Introduction part I: a review o f the literature

warm-up and thermoregulation. In one study of honeybees and bumblebees foraging on runner bean, the number of foragers was greatly dependent on the maximum ambient temperature and the number of hours of sunshine (Free 1968). Insolation may act directly on the body temperatures of the bee and/or via the secretion of floral nectar to influence foraging (Free 1960, for honeybees on fruit trees). Measurements of insolation were omitted from the present study.

Despite their endothermie abilities, bumblebee activity levels are subject to short-term changes in weather. Strong winds discourage foraging (Stoddard & Bond 1987; Simon Potts, personal communication), and foraging generally ceases during rain. Honeybees and bumblebees both prefer to forage in sheltered areas (Smith et al 1972). Bumblebees are less temperature dependent than honeybees (Stoddard & Bond 1987), but like them they are ultimately dependent on the climate.