Spatial foraging patterns and colony energy status in ... - Springer Link

Journal of lnsect Behavior, Vol. 6, No. 2, 1993

Spatial Foraging Patterns and Colony Energy Status in the African Honey Bee, Apis mellifera scutellata Stanley S. Schneider I and Linda C. McNally 1 Accepted May 12, 1992; revised June 2, 1992

The relationship between changes in foraging patterns 6nferred from waggle dance activity) and colony energy status (inferred from brood rearing activity, food storage, and colony weight) was examined for the African honey bee during a period of relative resource abundance and resource dearth. When resources were more abundant mean foraging distances (about 400 m) and foraging areas (4-5 km 2) were small, and colonies recruited to 12-19 different sites per day. Colony foraging ranges and sites visited increased slightly during the dearth period, yet foraging continued to be concentrated within less than 10 km 2. The degree to which fluctuations in foraging patterns were correlated with colony energy status varied with the availability of floral resources. During periods of relative forage abundance, increases in foraging range and number of sites visited were significantly correlated with increases in brood rearing and colony weight. In contrast, colonies examined during periods of resource dearth exhibited no correlations between foraging areas, foraging distances, and fluctuations in brood rearing, food storage, or colony weight. Thus, during dearth periods colonies may not be able to coordinate foraging patterns with changes in colony energy status. KEY WORDS: Apis mellifera scutellata; foraging; waggle dance; recruitment; brood rearing.

INTRODUCTION

Animals frequently adjust their foraging behavior in response to changing energy needs. As an animal's energy budget fluctuates, it may alter its foraging range and sampling activity, modify its selectivity of dietary items, and adjust its Department of Biology, University of North Carolina, Charlotte, North Carolina 28223. 195

0892-7553/93/0300-0195507.00/0 9 1993PlenumPublishingCorporation

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sensitivity to the variance in the rate of foraging reward (Stephens and Krebs, 1986; Caraco and Lima, 1987; Tamm, 1987; Shettleworth et al., 1988). The influence of energy needs on foraging behavior is of particular interest in the highly social insects (ants, bees, termites), because foraging activity is geared to the energetic needs of the entire colony rather than those of the individual workers (Wilson, 1971; Oster and Wilson, 1978; Winston, 1987). The relationship between colony food needs and foraging behavior has been extensively studied for the honey bee, Apis mellifera. At the heart of honey bee social foraging is the waggle dance, which directs recruits to profitable food sources (von Frisch, 1967). A forager's decision to dance is determined by a combination of factors associated with the flower patch she is visiting (such as distance from the nest, nectar sweetness, and nectar abundance) and colony nutritional status, which is communicated by the food processing workers that unload nectar from incoming foragers (Seeley, 1986; Seeley and Levien, 1987). When colonies have little stored food or large amounts of empty comb, foragers are quickly unloaded, which stimulates waggle dance activity and thus recruitment behavior. Conversely, when colonies have large food reserves or little empty comb for nectar storage food processing, bees are slow to unload foragers, which reduces waggle dance and recruitment activity (Seeley, 1989). The net result is a fine-tuned adjusting of colony foraging effort to energy needs, by continually redistributing recruits throughout the environment (Seeley and Levien, 1987; Seeley, 1989; Seeley et al., 1991). Much of what is currently known about the regulation of honey bee foraging is based upon studies in which colonies have had access to only one or a few artificial feeding stations, usually located within 1 km of the hive (von Frisch, 1967; Seeley, 1986, 1989; Seeley et al., 1991). However, under natural conditions honey bee colonies gather food over a large area (10-100 km 2) and distribute recruits among 12-15 sites per day (Visscher and Seeley, 1982; Schneider, 1989a; Schneider and McNally, 1992b). Yet little is known about how changing energy requirements influence the allocation of a colony's entire foraging force among the multiple food sources normally available in the honey bee's environment. This study examined the associations between colony foraging patterns and energy needs in the African honey bee, Apis mellifera scutellata (hereafter referred to as scutellata). This was accomplished by using waggle dance activity to infer day-to-day fluctuations in foraging patterns and then examining the correlations between such fluctuations and changes in colony growth and development. The study was conducted in the Okavango River Delta, Botswana. The Okavango is sparsely inhabited by humans, and there is little or no agricultural or beekeeping activity. The scutellata colonies in the Delta are abundant (8/km2), experience a prolonged foraging season, and exhibit distinct seasonal fluctuations in food storage, brood rearing, and recruitment activity (McNally

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and Schneider, 1992; Schneider and McNally, 1992a, b; Schneider and Blyther, 1988). The scutellata colonies of the Okavango therefore offer a unique opportunity to study the relationship between foraging patterns and colony needs in a naturally occurring population of honey bees in their native environment. MATERIALS AND METHODS

Study Colony Maintenance The study was conducted using four two-frame, glass-walled observation colonies. Each colony was originally excavated in the field and the combs and bees transferred into 45-liter hive boxes. Once a colony began raising brood, it was transferred into an observation hive which provided comb space (4050 cm 2) similar to the mean comb area (3231 cm 2) of honey bee nests in the Okavango (Schneider and Blyther, 1988). The glass walls of each hive were marked off in a grid of 5 x 5-cm squares to facilitate monitoring worker activity. Colony population sizes were estimated once each week by counting the number of bees in 10 randomly selected grid squares, calculating the mean number of bees per square, and then multiplying this figure by the total number of squares of comb in the colony. All population estimates were conducted in the early morning hours before flight activity began. The observation colonies were maintained inside high-walled canvas tents (two colonies/tent), located in the shade and lined internally with heavy brown paper to reduce heat and light levels. Under such conditions scutellata colonies can be maintained for extended periods and exhibit normal patterns of brood rearing and foraging activity (Schneider, 1989a, b; Schneider and McNally, 1992a). Further descriptions of observation colony maintenance are given by Schneider (1989a, b, 1990) and Schneider and McNally (1992a, b).

Estimating Colony Energy Requirements We used two methods to examine colony energy needs. First, once each week we used the grids drawn onto the observation hive walls to measure the proportion of total comb area that contained brood (eggs, larvae, and pupae) and food (boney, nectar, and pollen) and that was empty. These data provided a direct estimate of the level of brood rearing and food storage activity within the colonies. Second, each colony was maintained on a battery-powered, Kubota KA-10 digital platform scale graduated in 5-g increments and was weighed at the end of each day after foraging activity had ceased. The weight of the empty hive was then subtracted from each day's weighing, resulting in a value for the combined weight of all workers, brood, food, and comb in the colony. These data provided an indirect estimate of fluctuations in colony energetic condition

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due to the combined interactions of brood rearing, food storage, and worker metabolism and death. Throughout the remainder of the paper we refer to a colony's brood rearing activity, food storage, and weight collectively as its "energy status."

Determining the Relationship Between Spatial Foraging Patterns and Colony Energy Status Colony foraging patterns were examined by monitoring waggle dance activity, translating the location of the site communicated by each dancer, and then constructing a map of the different food sources indicated. Each observation colony was monitored for 2-3 days each week throughout the time it occupied an observation hive. Whenever possible, different colonies were monitored on the same days. On each day of observation a colony was observed for 30 rain each hour from sunrise to sunset. Throughout these time periods, waggle dancers were selected at random and the direction and distance components of their dances were recorded. Honey bees communicate the direction to a food source through the orientation of the waggle-ran portion of the dance with respect to vertical (von Frisch, 1967). We measured the angle of the waggle runs in this study relative to vertical using a protractor and subsequently converted the dance angles into a direction with respect to north by (1) calculating the sun azimuth for the time of observation, using an Astrosoft program for an IBM personal computer, and (2) adding the azimuth value to the recorded dance angle. The distance to a food source is communicated by the duration of the waggle run (yon Frisch, 1967). The distance communicated by each dancer examined in this study was estimated by (1) recording the time of 5-10 different waggle runs (5.92 _+ 4.92) using a digital stopwatch, (2) calculating a mean waggle run time (obviously inconsistent times were ignored), and (3) converting this time into a distance estimate in meters. The conversion of dance times was accomplished using a curve expressing the relationship between waggle run duration and distance. This curve was established by training marked foragers to feeding stations at known distances up to 1 km from the hives, then timing their waggle runs once they returned to the colony. The translation of dance times greater than those covered by the waggle run duration-distance curve was accomplished by extrapolation. Round dances were assigned a distance of 17 m (see Schneider, 1989a). If a dancer carried pollen, pollen color was noted. Dancers not carrying pollen were assumed to be nectar foragers, although a small proportion of nonpollen dancers may also have been associated with water collection (Schneider and McNally, 1992b). Further details of recording waggle dance activity are given by Schneider (1989a) and Schneider and McNally (1992a, b). For each day of observation in a given colony, a foraging map was con-

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structed by plotting the location communicated by each dancer using symbols denoting the different pollen colors and nectar (for examples of such maps, see Schneider, 1989a; Visscher and Seeley, 1982). We used the maps to determine, for each day of observation, (1) the mean foraging distance (m) communicated by all dancers; (2) the foraging area (km2), defined as the circular area encompassing 95% of all indicated sites; and (3) the number of different food sites visited. Blooming plants visited by honey bees in the tropics often occur as widely distributed, individual trees or shrubs (Winston, 1987; Smith, 1958; Schneider, unpublished data). Thus, in this study locations indicated by waggle dancers on a given day were considered to occur within the same foraging site if (1) the dances were for the same food type (e.g., same color of pollen or nectar) and (2) the indicated locations were less than 100 m apart. Dance locations separated by more than 100 m were considered to constitute separate foraging sites. Additionally, we determined for each colony the mean daily foraging distance, mean foraging area, and mean number of sites visited per day for all days of observation during each week of the study. Two components of the relationship between spatial foraging patterns and colony energy status were examined. First, for each week of observation we determined the correlations between the weekly means for daily foraging distance, foraging area, and number of sites utilized and the proportions of brood, food, and empty comb present in the colonies at the end of each weekly period. Additionally, we examined the relationship between the weekly means for the foraging parameters and colony population size. Second, for each day of observation we examined the correlations between mean foraging distance, foraging area, and sites visited and (1) colony weight on the preceding day and (2) mean colony weight over the preceding three days. This second aspect was examined to determine if foraging patterns were more closely associated with immediate or more long-term trends in colony mass. Unless otherwise stated, all mean values are reported _+1 SD. All proportional data were arcsine transformed prior to analysis. RESULTS The observation colonies were monitored at different times of the year, experienced different fates, and exhibited different patterns of brood rearing, weight gain, and population growth. Colonies 1 and 2 were observed from November through January, and each migrated from the study area in January. Forage availability in the study area began to decline during the NovemberJanuary period (McNally and Schneider, 1992). Nevertheless, colonies 1 and 2 had fairly high and consistent levels of brood production, gained weight throughout much of the observation period, and exhibited steadily increasing population sizes (Figs. 1 and 3). In contrast, colony 3 was monitored from February to

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Fig. l . The percentage of total comb area devoted to brood rearing and mean colony weight during each week of observation in colonies 1 and 2.

May and colony 4 from March to June, and neither migrated during these months. Both colonies were observed during a resource dearth in which the availability of forage was low (McNally and Schneider, 1992). Colonies 3 and 4 ceased brood rearing in May (Fig. 2), at which time food stores declined to near-zero and virtually no blooming plants were available in the study area (McNally and Schneider, 1992). Colony 3 died in May, presumably of starvation. The weights and population sizes of colonies 3 and 4 remained fairy constant or declined throughout the study period (Figs. 2 and 3). When viewed over all weeks of observation, the mean proportions of brood comb in colonies 1 and 2 (53.5 -t- 9.4 and 49.0 ___ 10.1%, respectively) were significantly greater than those of colonies 3 and 4 (26.6 _+ 15.6 and 16.4 + 21.1%, respectively; F = 13.36, df = 3,38, P < 0.01). Likewise, the mean weights for colonies 1 and 2 (1993 ___ 780 and 2185 -t- 473 g, respectively) were significantly greater

African Honey Bee Foraging

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Fig. 2. The percentage of total comb area devoted to brood rearing and mean colony weight during each week of observation in colonies 3 and 4. The arrow indicates the death of colony 3.

than those of colonies 3 and 4 (1224 _ 473 and 1224 + 325 g, respectively; F = 11.64, df = 3,38, P < 0.01). Based on these observations, w e divided the colonies into two groups: those observed during a period of greater forage abundance (colonies 1 and 2) and those observed during a period of dearth (colonies 3 and 4). All colonies had similar mean population sizes during the study period (colony 1, 4883 _ 1636 bees; colony 2, 4429 + 1414; colony 3, 4922 + 578; colony 4, 4520 + 376; F = 0.54, df = 3,40, P = 0.66). The spatial foraging patterns for colonies 1-4 are summarized in Table I and Figs. 4 and 5. When viewed over all days of observation, mean daily foraging distances for the four colonies varied between 400 and 620 m and foraging areas between 3.9 and 7.6 km 2 (Table I; colony 1 was observed for a total of 27 days; however, analysis was restricted to the 24 days for which

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Fig. 3. The population sizes of the study colonies during each week of observation. The arrow indicates the death of colony 3.

Table I. The Mean Jr SD Daily Foraging Distances (m), Foraging Areas (km2), Number of Sites Recruited for, and Number of Waggle Dancers Observed per Day over All Days of Observation in Colonies 1-4 ~

Colony 1 2 3 4

Foraging distance (range) 424 -I- 257 (17--4542) 428 -I- 353 (17-4994) 619 + 226 (17-8533) 578 -I- 116 (17-14,864)

Foraging area

Sites visted

Dancers

N

5.0 _+ 5.5

16.7 + 7.7

101.8 ___ 57.5

24

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12.5 + 6.5

92.0 + 50.2

24

7.6 + 10.2

19.1 + 6.9

125.4 -I- 78.8

27

4.9 ___ 3.4

18.5 + 11.1

104.9 + 72.0

25

a Sample sizes refer to the total days of observation.

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weight data were also available). The foraging distances for colonies 1 and 2 were significantly smaller than those of colonies 3 and 4 (F = 3.15, df -- 3,96, P = 0.028). However, the mean daily foraging areas did not differ among the four colonies (F = 1.42, df -- 3,96, P -- 0.242). In colonies 1 and 2 mean foraging areas and distances were small and relatively constant from one week to the next during the first 4 to 6 weeks of the study. However, these foraging parameters became increasingly large and variable in the final 6 to 7 weeks preceding migration (Fig. 4), during which time resource abundance was declining (McNally and Schneider, 1992). In contrast, foraging areas and distances

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in colonies 3 and 4 remained relatively large and variable throughout much of the study period (Fig. 5). There was no difference among the four colonies in the mean number of sites visited per day (F = 1.86, df = 3,96, P = 0.151; Table I). Weekly fluctuations in mean number of sites visited per day were also similar in the four colonies, although those of colony 4 tended to be more variable (Figs. 4 and 5). The four colonies also did not differ with respect to the mean number of waggle dancers observed per day (F = 1.16, df = 3,96, P = 0.026; Table I). Thus, the data provided by the daily foraging maps suggested that, despite the different foraging conditions experienced by the two colony groups, all four colonies were similar with respect to the area of the environment exploited, number of sites visited per day, and level of foraging effort. However, foragers from colonies 1 and 2 tended to travel shorter distances to food sources. Furthermore, the temporal patterns of the fluctuations in foraging areas and distances differed between the two colony groups. In colonies 1 and 2 foraging areas and distances became larger and variable only during the latter half of the observation period as resources began declining. Those of colonies 3 and 4 remained larger and somewhat erratic throughout the study period, and forage availability remained low throughout the months in which these two colonies were observed. The two colony groups differed with respect to the relationship between foraging patterns and the estimates of colony energy status. For the colonies examined during the period of greater floral abundance, weekly means for daily foraging distances, foraging areas, and number of sites visited per day were significantly and positively correlated with the proportion of total comb area containing brood (Table II, Figs. 1 and 4). These same aspects of colony foraging behavior were significantly and negatively correlated with the proportion of empty comb but exhibited no correlation with the proportion of comb containing food reserves (food comb; Table II). Foraging pattern fluctuations in colonies 1 and 2 may have been influenced by changes in population size. In both colonies there was a significant, positive correlation between population size and weekly means for foraging distances (Table II, Figs. 3 and 4). Colony 1 also had a significant correlation between population size, mean daily foraging area, and number of sites visited. However, it is unlikely that population size alone was sufficient to account for all observed foraging pattern fluctuations. For example, population size was not correlated with weekly mean foraging areas and number of sites visited for colony 2 (Table II). Likewise, partial correlation analysis revealed that when the effects of population size were held constant in colony 1, there continued to be a significant correlation between brood comb area, weekly mean foraging distance, and mean foraging area (for both correlations r > 0.650, df = 8, P < 0.05). The correlation between brood comb area and weekly mean foraging distance in colony

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Table II. Correlation Coefficients for the Relationships Between Mean Daily Foraging Distances, Areas and Sites Visited per Day over Weekly Periods, and the Proportions of Brood, Food, and Empty Comb and Population Size Measured Weekly in the Colonies" Mean daily foraging distance (m) % brood comb Colony 1 Colony 2 Colony 3 Colony 4 % food comb Colony 1 Colony 2 Colony 3 Colony 4 % empty comb Colony 1 Colony 2 Colony 3 Colony 4 Population size Colony 1 Colony 2 Colony 3 Colony 4

Mean daily foraging area (km2)

Foraging sites per day

0.907*** 0.753** -0.417 -0.365

0.953*** 0.689* -0.320 -0.371

0.845*** 0.713" 0.645* 0.816"*

0.450 0.039 0.366 -0.230

0.385 0.018 0.595 -0.079

0.288 0.260 -0.37t 0.893**

-0.872*** -0.673* -0.021 0.365

-0.854*** -0.604* -0.172 0.279

-0.792** -0.752** -0.159 -0.872***

0.844** 0.716" -0.165 0.196

0.927*** 0.597 -0.343 0.122

0.765** 0.519 0.381 0.004

aData were available for 11 weeks of observation for each colony. *P < 0.05. **P < 0.01. ***P < 0.001. 2 was nonsignificant when the effects o f population size were held constant (r = 0.386, P > 0.05), although it continued to be positive. Thus, while the increasing population sizes o f colonies 1 and 2 strongly affected foraging patterns, other factors such as brood rearing activity and the amount of empty comb may also have influenced fluctuations in colony foraging behavior. Colonies 1 and 2 also exhibited significant, positive correlations between each of the foraging pattern parameters measured and (1) colony weight on the day preceding observation and (2) mean colony weight over the 3 days preceding observation (Table III, Figs. 1 and 4). Thus, increases in colony weight over both a 1- and a 3-day period were associated with increases in the foraging areas and sites utilized on the following day o f observation. Taken together, these data suggest that during the period o f greater resource abundance, decreases in empty comb and increases in brood rearing activity, colony weight, and, to some extent, colony population size occurred in conjunction with an expansion o f the foraging range and the allocation o f foragers among a larger number o f food sources.

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Table III. Correlation Coefficients for the Associations Between Mean Foraging Distance, Foraging Area, and Number of Sites Visited on a Given Day and (1) Colony Weight on the Preceding Day and (2) Mean Colony Weight over the Preceding 3 Daysa

Mean foraging distance (m)

Foraging area (km2)

Sites visited

Weight on preceding day Colony 1 Colony 2 Colony 3 Colony 4

0.687** 0.615"* -0.404* -0.193

0.699** 0.556** -0.165 -0.053

0.622** 0.469* 0.354 0.672**

Mean weight on preceding 3 days Colony 1 Colony 2 Colony 3 Colony 4

0.676** 0.579** -0.375 -0.195

0.694** 0.526** -0.197 -0.058

0.609** 0.426* 0.303 0.645**

~Data were available for 24, 24, 27, and 25 days of observation for colonies 1-4 respectively. *P < 0.05. **P < 0.01.

T h e colonies observed during the dearth period exhibited less distinct associations between foraging patterns and the estimates of colony energy status. For both colony 3 and colony 4 the correlations between weekly means for foraging distance and area, the proportions of brood, food, and empty comb, and population size were nonsignificant and tended to be negative (Table II, Figs. 2, 3, and 5). Likewise, colonies 3 and 4 exhibited mostly negative, nonsignificant correlations between mean foraging distance, foraging area, and colony weights (Table III). Fluctuations in the number of food sites recruited for per day in colonies 3 and 4 were more strongly correlated with the estimates of colony energy status and followed the same basic patterns observed for colonies 1 and 2. Colonies 3 and 4 had a significant, positive correlation between the mean number of sites visited per day and the proportion of comb area devoted to brood rearing (Table II). Colony 4 also exhibited (1) positive correlations between mean number of sites visited, proportion of food comb, and colony weight over the preceding 1 and 3 days and (2) a negative correlation between the mean number of sites visited and the proportion of empty comb (Tables II and III). These same correlations were nonsignificant for colony 3. Taken together, these data suggest that during the dearth period, changes in colony foraging range occurred largely independently of fluctuations in brood rearing activity, colony population, and colony weight. However, the number of food sites visited per day tended to increase with increasing brood rearing and colony weight and decreasing empty comb area.

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DISCUSSION The results of this study revealed three main aspects of the association between foraging patterns and energy status for scutellata colonies in the Okavango Delta. First, while foraging distances and areas could fluctuate on a daily basis, under most conditions colonies met their food needs by exploiting relatively small regions of the environment. During periods of greater resource abundance, mean foraging distances were about 400 m and mean daily foraging areas were 4-5 km 2. During periods of resource dearth, mean foraging distances increased to 600 m and mean foraging areas to 5-8 km 2. Thus, while foraging areas may have changed as the abundance of resources fluctuated, food collection tended to remain concentrated within a few square kilometers around the nest, even when food availability was reduced and colonies faced potential starvation. A previous study of scutellata foraging patterns in the Okavango (at a site about 3 km from the present study site) revealed mean foraging distances of 1200 m and foraging areas of 30-40 km 2 (Schneider, 1989a). However, this earlier study was conducted just prior to the onset of reproductive swarming. Since scutellata swarms may travel long distances (Otis, 1991) and workers perform waggle dances for new nest sites prior to departing from the original nest (Schneider, unpublished data), the larger foraging distances and areas reported by Schneider (1989a) may have resulted in part from the accidental inclusion of recruitment dances for new nest sites in the mapping of colony foraging activity. Second, the results of the present study suggest that, in addition to fluctuating with food availability, foraging pattern changes were also correlated with colony energy needs. However, the degree to which these correlations occurred was dependent upon the overall availability of blooming plants. Colonies 1 and 2 were observed during a period of relative forage abundance, and their high levels of brood rearing activity and steady increases in colony population size and weight suggested that each had an overall positive energy status. During this period, decreases in empty comb area and increases in brood rearing activity, colony weight, and, to some extent, population size occurred in conjunction with larger foraging areas, recruitment for a larger number of food sites, and (by inference) a broader distribution of foragers among available food sources. Thus, even though foraging areas tended to be relatively small during periods of resource abundance, increases in a colony's energy status at these times may have been associated with gathering food from a larger number of sources within an expanded area of the environment. The energy required to coordinate spatial foraging patterns with energy needs in colonies 1 and 2 may have varied during the study period. During the final 6 to 7 weeks preceding migration, mean foraging areas and distances became increasingly large and variable on a day-to-day basis. While colonies 1

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and 2 continued to coordinate their foraging patterns and energy needs during this time, the data suggest that they were having to expend increasing amounts of foraging effort to maintain their positive energy status. The increasing energy expenditures may have reflected deteriorating foraging conditions. Thus, as floral resources became scarcer and perhaps more patchily distributed, it may have become increasingly difficult for scutellata colonies to synchronize foraging patterns with energy needs. Eventually, deteriorating foraging conditions may have resulted in foraging pattern fluctuations and changes in colony energy status becoming more or less uncoupled. Colonies 3 and 4 were monitored during a dearth period and each experienced an overall negative energy status, which may have contributed to the cessation of brood rearing and the death of colony 3. During this period, colony survival may have required the harvesting of any and all floral resources discovered, regardless of day-today fluctuations in colony weight, brood rearing activity, population size, or amount of empty comb. Daily fluctuations in mean foraging areas and distances may therefore have occurred more in association with chance discoveries of resources, rather than colony energy needs. However, increases in the number of food sites visited per day continued to occur in conjunction with increases in brood rearing and colony weight, suggesting that even during severe dearth periods colonies may still have been able to coordinate foraging patterns and energy status to some extent. The interactions of colony energy status and foraging patterns may have influenced migration behavior in the present study. Colonies 1 and 2 migrated, while colonies 3 and 4 did not, suggesting that only colonies that have maintained a positive energy status for an extended period have sufficient energy reserves for emigration. However, migration may occur only if appropriate levels of brood production, food storage, and colony population and weight occur in conjunction with changing foraging patterns. Thus, the increasingly large and variable foraging distances and areas of colonies 1 and 2 during the final 6 to 7 weeks of observation may have triggered migration, provided that colony energy status was conducive (see also Schneider and McNally, 1992b). Colonies 3 and 4 also exhibited large and variable foraging distances, suggesting that they too experienced deteriorating foraging conditions. However, the lower energy status of these two colonies may have hindered or prevented migration from the study area. The third aspect of the relationship between foraging and energy needs suggested by this study was that fluctuations in colony foraging patterns during the period of greater resource abundance were associated more with brood rearing activity than with food storage. This is in contrast to temperate climate colonies, in which foraging activity is strongly influenced by the amount of stored food (Seeley, 1986; Rinderer and Collins, 1991). This difference may result from the contrasting survival strategies of tropical and temperate climate

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honey bees. Tropical colonies experience an extended foraging season and high predation rates, factors which favor high rates of swarming and an emphasis on brood production versus food storage (Winston et al., 1983; Schneider and Blyther, 1988; McNally and Schneider, 1992). Thus, colony foraging may be more geared toward the energetic and nutritional needs of brood rearing (see also Danka et al., 1987; Schneider, 1989a; Schneider and McNally, 1992a). In contrast, temperate climate races must amass large food reserves for winter survival and devote a greater proportion of comb area to food storage than brood production (Seeley and Morse, 1976; Winston et al., 1981). Colony foraging may therefore be more strongly synchronized with fluctuations in food storage activity. In summary, the spatial distribution of scutellata foragers throughout the environment varied in conjunction with changes in brood rearing activity, colony weight, and population size. These fluctuations in foraging patterns may have adjusted colony foraging effort such that available resources were exploited in a manner most conducive to colony growth and development. However, such adjustments may be feasible only during periods in which there is the potential for a positive colony energy status. A clearer understanding of the relationship between foraging patterns and colony energy needs will require experimental manipulations. To this end we are currently conducting studies in which waggle dance activity is monitored before and after colonies are given extra brood or empty comb.

ACKNOWLEDGMENTS We thank M. Spivak and two anonymous reviewers for commenting on the manuscript. We thank Koro Safaris of Mann, Botswana, for help in locating and establishing the study site. C. and G. Blomstrand of Thamalakane Lodge provided much appreciated hospitality and moral support during our supply runs into Mann. The Office of the President, the Department of Wildlife and Tourism, and the National Museum and Art Gallery of Botswana provided valuable assistance throughout the study. We give special thanks to our local assistants, Longwan and James. The research was supported by U.S. National Science Foundation Grant BSR8906997.

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