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Comparative energy balance in groups of africanized and european honey bees: Ecological implications
Cony. Biochent. Ph.vsiol.
Vol. 97A.
No.
1,pp. 1-7,
0300-9629190 53.00+ 0.00 0 1990Pergamon Press plc
1990
Printed in Great Britain
COMPARATIVE ENERGY BALANCE IN GROUPS OF AFRICANIZED AND EUROPEAN HONEY BEES: ECOLOGICAL IMPLICATIONS E. E. SOUTHWICK,* D. W. ROUBIK~ and J. M. WILLIAMS~ *Department of Biological Sciences, State University of New York, Brockport, NY 14420 USA. Telephone: 716-395-5743, Fax: (716) 395-2416; tsmithsonian Tropical Research Institute, Balboa, Republic of Panama, APO Miami 43002, USA: and fJohn M. Williams Associates, Box 281, Brockport, NY 14420, USA (Received
22
Noaember 1989)
Groups of honey bees (&is me//$m L.) are able to metabolically regulate their central temperature under cold stress. At 2C, Africanized honey bees in 30g groups consumed 46.4% more oxygen per unit time holding their core temperatures at 29.O”C compared to European honey bees. 2. Differences in oxygen consumption increase as group sizes decrease. Regression analysis at freezing temperature showed that the two races attain similar costs of energy balance with the same mass when Africanized colonies contain about 20,000 bees and European colonies contain 16,000 bees (Fig. 1). 3. Africanized honey bees tested in groups at temperatures of 2°C and - 15°C showed metabolic rates that were 13-109% higher than those of the temperate region honey bees, but at 22.5”C, the cost of energy maintenance was 54% lower. We predict that physiological and behavioral characteristics combined with climatic conditions in North America will limit the northern distribution of nesting Africanized honey bees to a 120 consecutive day isoline of temperatures not exceeding 10°C during Winter (Fig. 2). In some southern regions of the USA, the Africanized race will have competitive advantage over the European honey bees now extant. Abstract-l.
INTRODUCTION The Africanized honey bee race currently occupies habitats in all of Central and most of South America. It is a hybrid bee similar to Apis mellifera scutellata (Lepeletier), a honey bee native to the lower middle
elevations of southern and eastern Africa (Boreham and Roubik, 1987; Roubik, 1988a, 1989; Ruttner, 1988). Potential expansion of the geographic range of this insect into cooler regions raises a central question of colony survival at high latitudes and altitudes. Can this honey bee thermoregulate and survive the cold northern winters which would be encountered in the mid- and northern latitudes in the United States? Which features of individual and colony biology are relevant in making such predictions? The future distribution is dependent on a number of factors, one of which is the colonies’ capacity to actively control brood nest temperature during exposure to low ambient temperatures. Without a stable brood nest temperature near 35°C during midwinter, honey bees in the temperate zone could not begin the timely production of brood needed for resource collection in spring and summer. This would probably lead to colony death during the following winter (Seeley, 1985; Seeley and Visscher, 1985). A key factor in survival of the honey bee colony is the use of physical and physiological mechanisms that allow for successful overwintering in north temperate zones (Southwick, 1985a, 1988, 1989, in press). Comparisons between Africanized and European honey bee colonies in this regard have been inconclusive but have suggested no significant differences in nest heat regulation and mass-specific honey con-
sumption under cool conditions (Dietz et al., 1988; Villa, 1985; Villa et al., 1987). However, Southwick (1988) pointed out that no data exist on the metabolic responses of Africanized honey bee colonies or even of the individual workers to exposure to ambient temperatures less than 15°C. Considerable data have been published on the thermal capacities of European honey bees, primarily Apis mellifera carnica in West Germany, and mixed racial hybrids in the United States (Heinrich, 1981; Ritter, 1982; Southwick, 1988, 1987, 1985a, 1983, 1982; Southwick and Heldmaier, 1987). These studies revealed that temperature equilibrium is achieved in the intact colony through mechanisms that balance routes of energy gain and energy loss. Under the low-temperature conditions of primary interest in the present study, thermal control, especially of the central brood area, is achieved by a colony through maintaining large numbers of individuals and large honey stores under winter conditions. In a colony of roughly 20,000 individuals, the bees cluster tightly together, affecting the important pathways of heat flow by effectively reducing convective and radiative heat loss, and increasing metabolic heat production as the colony’s stores of carbohydrate are converted to heat energy. The positioning of individuals within the cluster, particularly at the periphery of the cluster and between and against the cells of insulating empty wax comb, has also been shown to be important (Southwick, 1985b, c). Presumably, any colony of honey bees that could achieve thermal balance under low temperature conditions would do so by utilizing these physiological and behavioral mechanisms (Southwick, 1988).
E. E.
2
3
10
100
1000
Mass
(g
SOUTHWICK
3000
I
Fig. I. The relation of bee cluster mass and minimum maintained oxygen consumption achieved by groups of Africanized honey bees (filled circle, this study) and groups of European honey bees (open circle, from Southwick, 1985a) held at constant air temperature of 2 C overnight. MR = 69.79 M-06’, R’ = 0.95 (n = 17 Africanized bee groups) MR = 22.69 M “48. R’ = 0.96 (n = 16 European
bee groups, after Southwick 1985a) where MR is metabolism in ml 0,;gjhr and M is group mass in g. The six points indicated as triangles are metabolic values maintained just before these small groups of 50 Africanized honey bees fell into cold comatose condition from which they could not recover without an increase in air temperature.
The first invasion of Panama bees in 1982 demonstrated extremely
close
in size and
by Africanized honey that the bees were
behavior
to the original
et al.
African Apis mellifera scutellata brought to Brazil in 1956 (Boreham and Roubik, 1987). We use the term “Africanized” to denote that the bees are a product of hybridization between one African race and five other races of European origin that were maintained in the American tropics and which have interbred, albeit slightly, with Apis mellifera scutellata (Ruttner, 1988; Smith et al., 1989). In this paper, we report comparative measurements of oxidative metabolism at low temperatures by groups of honey bees of the Africanized and European races currently occupying Panama. The study provides the first metabolic measurements of Africanized honey bees during exposure to moderately low ( < 15’C) temperatures. The results help to clarify the temperature/metabolism relationships and thermoregulatory capacities of honey bees and provide data for predicting the geographic distribution population.
of the expanding
Esperimen~al
animuls
Africanized
honey
bee
METHODS
Morphometric analysis of feral honey bees in the American tropics is essential to characterize their origin; Africanized honey bees are, in general, smaller than all varieties of European honey bees (Daly and Balling, 1978; Ruttner, 1988). Two morphometric traits that provide
L Fig. 2. Isolines showing numbers of consecutive days when the normal highest temperature is below 10°C. These isolines were constructed from the climatological history of 250 weather reporting stations throughout the United States for the period of 1951-1980. The contours were constructed using the normal maximum temperatures for each station. The general reduction of temperature with altitude was considered by adjustment along topographical contours. This is seen, for example, near the Sierra Nevada range. near the Front Range of the Rockies, and, to a lesser extent, near the Alleghenies. (Data from National Climatic Data Center, no date.)
Energy
balance
and distribution
maximum discrimination are the length of the worker forewing and the width of the “wax mirrors” on abdominal sternites (Boreham and Roubik, 1987; Daly and Balling, 1978). Samples of at least 10 bees were taken from each colony used and scored for these two characteristics. Numerous hives of Africanized honey bees were established by native beekeepers from feral honey bee swarms in central Panama. There are currently no other varieties of honey bees living in the wild or in apiaries on the mainland. The European honey bee colonies used were taken from San Jose Island in the Pacific Ocean 70 km from the Panamanian mainland (Pearl Island Archipelago, 8 ‘15’ N, 79-8’ W), where European honey bee queens produced commercially in the southern United States have been imported each year for use in apiculture (Roubik, 1988b). Each honey bee group used in the experiments was taken from a single colony and usually consisted of about 300 workers, but some tests were run with several size groups of 50 to about 8000 workers. Metabolic measurements Test groups of worker bees were placed in ventilated air-tight acrylic chambers complete with empty and honeyfilled comb on which to cluster; large groups had their own stored honey supply and small groups were provided ad libirum with a sugar candy (honey mixed with powdered sugar) throughout the experiments. Preliminary test runs revealed no difference in metabolic rates of small groups with or without queens, so all tests were run without queens except where noted. For small group comparisons, each test run utilized three groups (i.e. one Africanized and two European, or vice versa) and a control chamber without bees tested at the same time. Sequential respiratory gas measurements were taken at 5 min intervals, using a microprocessor controlled electronic valve manifold. For each test, the metabolic chamber containing bees was placed within the controlled temperature cabinet at about 1330 hr each day. Following procedures previously described by Southwick (I 982) fresh air was drawn through the chamber by a diaphragm pump at about 500 ml/min (with flow rate controlled by a needle valve). The air stream entering each chamber was dried by passing over columns of Drierite (CaSO,), and carbon dioxide was removed by columns of Ascarite (NaOH coated asbestos). The exit stream was dried and carbon dioxide removed and then routed through an oxygen analyser (Applied Electrochemistry S-3A with a double cell sensor, N-37M, and R-2 flow control, accuracy of +O.OOl vol%). The carbon dioxide was removed and not measured because we assumed that the respiratory quotient (RQ = moles carbon dioxide released/moles oxygen consumed) was equal to one (1 .O). Previous measurements with ad libirum honey-fed European honey bees showed this to be consistently the case, at least under the conditions of test runs up to 24 hr long (Southwick, 1985a). Oxygen contents of the air streams could be determined digitally and were simultaneously recorded on a YSI strip chart recorder for later analysis. Gas flow rates were determined with a Gilmont flowmeter which had been calibrated against a soap film flow meter (+ 1%). Any error in flow rates would have been in a consistent direction (all values too high or too low). This was not the case as born out in our results, so this type of error must be small and is not further considered. Oxygen consumption was determined by comparing the oxygen contents of the air flowing into and exiting the chamber after correction for carbon dioxide removal.
in honey
bees
mate because we were not certain of cluster positioning when placement of the thermocouples was fixed. All tests were under dark conditions (D:D). Sufficient time was allowed to reach minimal metabolic rates to allow for comparisons with data in the literature, usually about 15 hr (Southwick, 1985a). After minimum metabolic rates were determined, the bees were weighed and numbers of individuals were estimated by sampling groups of IO or more bees for individual weights. We did not attempt to measure crop contents. The two temperatures of exposure reported here were f2”C and - 15°C to allow comparisons with existing published data. RESULTS
Morphometry Morphometrics
of
the
Africanized
honey
bee
colonies, all collected near the Pacific coast of central Panama in December and January, showed that the bees were strongly African and were relatively small compared to Africanized honey bees sampled throughout South Africa in the early 1970s (Boreham and Roubik, 1987; Dale and Balling, 1978). These authors found an average forewing length of 8.65 mm (range 8.33 to 9.05mm) and a wax mirror width of 2.17 mm (range 2.01 to 2.38 mm) for Africanized honey bees. Forewing length averages ranged from 8.39 to 8.61 mm among bees sampled from the 10 Africanized honey bee colonies used in this study, and those of wax mirror width were 2.11 to 2.27 mm. All coefficients of variation were between 1% and 3%. The two European honey bee colonies had average forewing lengths of 8.92 and 9.02 mm, and wax mirror widths averaging 2.45 mm. The European honey bees sampled by Daley and Balling (1978) from South American colonies averaged 9.12 and 2.36 mm for these two traits, respectively. Metabolic rates Comparative data on minimum metabolic rates of groups of Africanized and European honey bees were obtained at temperatures of 2°C and - 15°C. At 2°C (Table 1), small groups of African honey bees weighing about 30 g showed significantly greater metabolic rates than groups of European honey bees of similar mass. Under these conditions, the Africanized honey bees consumed 46.4% more oxygen per gram and per unit time in order to maintain their heat balance (with the approximate central cluster temperature maintained at 29.0 + 1.52C, n = 8) than did the European honey bees (cluster temperature of 29.7 k l.O”C, n = 6). Live weight of honey bee test groups was 30 g for both races, but due to the smaller individual mass of Africanized workers (88 mg, on average, vs 111 mg for Europeans), there were more bees in their groups. On average, 301 individuals made up an Africanized Minimum metabolic rates (oxygen consumption, VO,) in groups of about 300 honey bees exposed to 2’C
Table
I.
small
broodless
overnight
in Panama,
Temperarure monitoring Simultaneous measurements of several temperatures inside and outside the chamber, in the central cluster, and the outer region of cluster, were taken utilizing Cu-Con thermocouples connected to a Bailey Instruments thermocouple meter and paper chart recorder (YSI dual channel recorder). Central cluster temperatures are only approxi-
3
C.A.
(data
expressed
as mean k SE)
Africanized Live
mass
Worker
number
Group vo, VO,
30.
per bee
I k 2.61
301 + 18’ 8.64 f
(163400)
I.01 ml O,/g/hr*
864 ~1 O,/hr (n = 15 groups)
*Statistically
significant
European 28.
g
difference
I i 1.38g
232k
II*
(If@-312)
5.90 k 0.53 ml O>/g/hr* 715~1
O,/hr
(n = I3 groups) (P cl 0.01).
E. E.
4
SOUTHWICK et al.
group, with only 232 individuals in a European group. Africanized groups showed 46% higher rates of mass specific metabolism, but at the individual level, an African bee consumed, on average, 21% more oxygen per hour per bee than its larger European counterpart. When exposed to 2 C overnight, groups of different sizes (50 to 8000 individuals) showed great differences in the minimum metabolic rate maintained, which was directly dependent on group size (Fig. 1). At this cool temperature, there is an increase in mass specific metabolic cost as the groups become smaller in numbers of bees or mass (not reduction in size by tighter clustering of the group). Groups of 50 Africanized workers were too small for thermoregulatory control overnight at this temperature (2 ‘C) as indicated by total loss of thermal control. All bees in the 6 groups of 50 bees tested at 2-C fell into “cold coma” after only 226 hr of exposure. Three groups of Africanized honey bees, one of 351, one of 440, and one of 7020 workers, were tested at - 15 ‘C for 15 hr. They maintained central cluster temperatures at 28 to 3 1 C without losing many outer individuals (< 5%) to cold coma. The groups consisting of 351 individuals and 440 individuals (30.9 and 43.4 g, respectively) consumed 15.8 and II.2 ml O?/g/hr. This is about 3.5 times the rate of the groups at exposure to 2-C. The 7020 bee group. which formed an intact colony with queen and brood (total mass 618 g) displayed a metabolic rate of 6.47 ml O2 /g/hr at - 15’C, about 5 times greater than at 2’C (I. 18 ml Oz/g/hr) and 7.5 times higher than at 22.5’C (0.88 ml OJg/hr). DISCCSSION
Throughout the ecological experiment created by uncontrolled spread of Africanized honey bees through the Americas, one of the most frequently asked questions is, how far north will they go? The ability to achieve temperature regulation strongly influences the extent of Africanized honey bee colonization in North America (Roubik, 1987; 1990). One way in which our data are useful is in predicting climatic limits of the colonizing population, which should continue to be feral and therefore not available for manipulation by apiculturists. Clearly, other ecological variables such as the influence of natural enemies and competitors. and the availability of nesting localities and food sources are also important. Additional data is needed on foraging behavior, nesting behavior, colony growth, and other variables as they relate to honey bee distribution (Roubik, 1989; 1988b, 1990). The range expansion of Africanized honey bees will likely be limited by factors such as habitat and competition, and their colony demography in northern habitats will likely be influenced by both the migratory habit of human beekeepers combined with control measures taken by human beings. Our data on metabolic capacities at low temperatures, combined with the known behavioral characteristics of European and Africanized honey bees (summaries by Winston et al., 1983; Rinderer, 1988; Southwick, 1989, in press; Roubik. 1989. 1990) provide some straightforward predictions for the
impending States.
colonization
Thermoregulatory
of
the
southern
United
costs
Even though the small groups of European honey bees we tested were 10% lighter than the groups of Africanized honey bees (28.1 vs 31.2 g), which would be expected to raise their mass dependent metabolic rates, the European honey bees still consumed less oxygen to maintain their normothermic central cluster temperature under the 2°C experimental conditions. The measurements we obtained on cost of thermal control in a full size queenright colony of Africanized honey bees at the cool 2-C environmental temperature yielded values of metabolic rate 13% higher than predicted by data published on European honey bees (full size queenright colonies) at the same temperatures (Southwick, 1985a). In fact, all the mass specific metabolic data we obtained on African honey bee groups were 13% to 109% higher than predicted from European data at environmental temperatures below IO’C (Southwick, 1985a, 1988). We have also an interesting comparison at a thermoneutral temperature, since at 22.5 C the metabolic costs to Africanized bees were 54% lower than the predicted value for temperate European honey bees. The tropical honey bees are obviously better adapted to warm temperature than their northern counterparts. Examination of comparative honey bee colony performance at higher temperatures would be worthwhile. Thermoregulatory activities of honey bee clusters are dynamic and complex (Southwick, 1985a). The cluster geometry of Africanized honey bees under low temperature stress is not yet elucidated adequately to understand if there are patterns (such as cluster “tightness”) that might affect the limits of northern nesting. For all group sizes that were tested, Africanized honey bees had higher mass-specific metabolic rates than those reported for European honey bees. Differences between Africanized and European bees were more pronounced in smaller groups. This might indicate that in such groups the Africanized bees cluster less tightly or are less efficient in preventing heat loss. They were also noticeably more nervous in the experimental setup at moderate temperature, although no differences could be seen at 2-C. When log-transformed, the data fall on straight lines, as plotted in Fig. I. The slopes are significantly different (P < 0.01). with the steeper slope displayed by Africanized groups. The plots for the two honey bee races intersect at 1790.6 g which is about equal to 16,000 European honey bees or 20,000 Africanized honey bees. All the Africanized bees in the smallest groups tested overnight at 2-C each comprised of 50 bees, died of cold exposure after only a few hours. Few European bees (mean of I2 individuals or 24% from 37 groups) in similar size groups tested under the same conditions by Southwick (1985a) entered cold coma even after I5 hr or more at this temperature. Ecological implications of colony size are related to thermoregulatory capacity. As the numbers of individual workers within the colony decrease. the
Energy balance and distribution in honey bees metabolic costs of temperature maintenance increase more rapidly in the Africanized hybrid. This is important in considering limits of expansion of the population of Africanized honey bees for at least three reasons. First, all colonies lose progressively more individuals (which die) as the confinement period is extended. This “winter loss” is substantial, even in European colonies (Farrar, 1963). So as the winter temperatures prevent flight, it becomes more and more costly for the group to continue thermal control, with these costs rising faster for the Africanized clusters. Second, as Africanized honey bees will tend to enter autumn and winter seasons with relatively small colonies (certainly less than the 30,000 bees recommended for success, Furgala, 1975) from poorly established late summer swarms, they will be under increased thermal stress even at the beginning of the low temperature season. Third, the smaller overwintering colonies will be prevented from the early colony growth considered to be critical for success (Seeley and Visscher, 1985). The stresses associated with the smaller winter clusters of Africanized bees can be expected to exacerbate “stress diseases” such as Nosema. Survizlability at low temperature The length of the foraging season in north temperate regions is one of the factors that will determine distributional limits of Africanized honey bees. At high elevations in Colombia, near 2000 to 3000m, colonies nesting in the wild displayed emigration or disappearance after 4 months of rainy or otherwise poor foraging conditions (Villa, 1987). In northern Argentina, Dietz et al. (1988) found that bee colonies purportedly of Africanized stock survived approximately three months in a refrigeration chamber. The honey-hoarding and foraging behavior of Africanized compared to European honey bees has received experimental study by Rinderer et al. (1985) who suggested that the Africanized race forages more consistently than European honey bees, but amasses smaller food stores. This behavior has been interpreted as a reflection of “high efficiency” foraging by European honey bee colonies, which need relatively large honey stores and worker bee populations in order to produce metabolic heat and allow brood production during winter months. In contrast, foraging for “high harvest rate” is shown by African honey bee colonies which reproduce as rapidly as possible, at the expense of forager longevity and total colony efficiency (Winston et al., 1983; Seeley, 1985; Roubik, 1989). No study has determined whether Africanized honey bee colonies initiate brood production in midwinter, seen as an essential factor in colony survival by European honey bees (Seeley and Visscher, 1985). We still do not know what specific changes in social organization are involved in the evolution of cold tolerance. From our data collected in Panama and other limited data available, the length of time that a colony is confined to low temperatures and prevented from foraging seems critical to Africanized honey bee colony survival. When in cool conditions of 10°C or lower, there was no flight or foraging activity by Africanized honey bee colonies (Villa, 1987, personal communication; this study). They may not only run
5
out of stored food faster than European races, but their cluster formation may prevent them from even moving to available food stores within the nest. Villa (1987, personal communication) found that clusters of Africanized honey bees at 4000 m elevation in Venezuela formed tighter and more compact clusters than those formed by European honey bees when the same mass of bees of each group was exposed to an environmental temperature of about 10°C. He also found that some colonies of Africanized bees that died during prolonged confinement at low temperatures still had stores of honey within their nests. We noted that the small experimental clusters in Panama were unable to move for more than an hour after removal from 2°C in test chambers, compared to activity within a few minutes by European honey bees. Within such clusters, the movement of workers may be essential to move to new honey storage areas on the comb, but such dynamics are still inadequately understood for Africanized or European honey bees. Our preliminary observations suggest that they may be important for colony survival at lower temperatures, irrespective of the amount of honey hoarded by the colony. Furthermore, the survival of a colony depends upon increased worker longevity during the winter. The higher metabolic rates observed for Africanized honey bees would tend to reduce their longevity (Winston et al., 1983; Sohal, 1986) such that, irrespective of honey stores, the shorter lifespans of Africanized workers would limit colony survival. A number of investigators have moved African and Africanized honey bees from their native habitats to northern areas for study. None have reported success in maintaining colonies over lengthy cold winters. Woyke (1973) transported Africanized honey bees (Apis mellifera scutellata) from Brazil to Poland and was unsuccessful in overwintering any colonies there. African honey bees kept in Oberursel, near Frankfurt, West Germany, did not maintain their colonies over the winter (unpublished observations). In fact, the standard practice used by the Oberursel Institut fuer Bienenkunde has been to house African queens in large colonies of European honey bees (Apis mellifera carnica or Apis mellifera mellfera) in order to “keep” them over the winter (Koeniger, personal communication). African queens are not maintained through the winter with their own African workers. There is recent evidence (Smith et al., 1989) that Africanized honey bees may not be hybrids after all, but instead may be genetically pure descendants of the original African founder population. Thus, there is probably little dilution of African traits (including those related to thermoregulation) through hybridization as the population spreads into North America. This suggests that there may be a fairly sharp boundary to the African honey bees’ northern range. Predicted distribution Because of nest confinement below IO’C, isolines of lOC, shown in Fig. 2 with numbers of days presented, are likely to indicate the maximum winter survival limits of Africanized honey bee colonies in North America. North of any isoline, air temperatures do not exceed 10°C during the numbered
6
E. E. SOUTHWICKel al
consecutive days. The question remains: how long can the Africanized honey bees be confined and still survive? The evidence from the energetic analysis reported in this study and from the other cited studies on behavior and social organization indicate that survival would be no longer than about 90 to possibly 120 days. The probable maximum survival time of 120 days gives an isoline, labelled 120, north of which all feral Africanized colonies would probably die of confinement and/or depletion of their food stores. South of the 120 day isoline, Africanized bees might be able to survive even through the winter. The use of the 120 day, 1OC isoline as a maximum is supported from the comparative data previously cited from high altitudes in northern South America (Villa, 1987; personal communication) where the racial type of Africanized honey bees is not in question. However, the true limit may be further south, particularly since we do not know whether workers in the colony at the onset of winter could actually survive for an additional 120days. The 120day limit includes most of Long Island, New York, parts of Pennsylvania, central Ohio, Illinois and Indiana. and the southern borders of Iowa and Nebraska, central Colorado, northern Utah, Nevada, western Idaho, and Washington state. Geographic pockets of ameliorating temperature are found to vary with altitude in mountain regions allowing for successful overwintering north of the 120 day isoline and limiting overwintering south of the line as in the Sierra Nevada mountains of California. Of course, some Africanized honey bees at the northern limits of their nesting range will certainly produce highly mobile reproductive swarms as well as absconding swarms throughout the summer season as they do in their tropical environments (Kigatiira. 1988). These would disperse well beyond the predicted winter limit. Feral colony distribution would be expected to show annual fluctuation around this line, if, in fact, the colonies can survive there throughout the winter. Our estimate of 120 days survival time yields a northern nesting limit considerably further north than other predictions based on other temperature data without the metabolic and behavioral backup. For example, Taylor (1985) published a map based soley on low daily temperatures, which is considerably south of our predicted limit. His prediction includes limits of feral nesting Africanized bees only in the very southernmost tips of California, Arizona, Texas, Louisiana, Georgia and Florida. As we have stressed, ecological variables of many kinds are still too poorly understood to predict which, if any, would exert a control of honey bee colony survival of a type superseding that of the thermal environment. For at least portions of the southern United States, it does appear that feral Africanized honey bees are at a thermal advantage over European honey bees now feral in this region (Taylor, 1988). The Africanized honey bee is inferior to European honey bees in cold tolerance, as demonstrated by comparative colony energy balance and behavioral characteristics. The distribution of the feral Africanized honey bee colonies, which have by far the most significant impact on beekeeping and the ecology of local plants and animals, will be strongly
limited by their relatively inefficient attempt to thermoregulate during extended exposure to low temperatures. We are most grateful to G. F. Novey and son for logistic support and permission to work with their honey bee colonies. DWR acknowledges the support of Smithsonian Institution Scholarly Studies grants for research on Africanized honey bees and EES acknowledges a short-term visitor research grant from that institution. REFERENCES
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Energy
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and di stribution
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in honey
bees
7
colonies. In Africanized Honey Bees and Bee Mites (Edited by Needham G. R.. Page R. E. Jr, Delfinado-Baker M. and Bowman C. E.), pp. 223-236. Ellis Horwood Ltd, Chichester, UK. Southwick E. E. (1989) Social temperature control and heat production in honey bees. In Thermal Physiology (Edited by Mercer J. B.), pp. 755-759. Elsevier, Amsterdam. Southwick E. E. (in press) Overwintering in honey bees: implications for apiculture. In Insects at Low Temperature (Edited by Lee R. F. and Denlinger D. L.). John Wiley and Sons, New York. Southwick E. E. and Heldmaier G. (1987) Temperature control in honey bee colonies. Bioscience 37, 395-399. Taylor 0. R. (1988) Ecology and economic impact of African and Africanized honeybees. In Africanized Honey Bees and Bee Mires (Edited by Needham G. R., Pane R. E. Jr, Dehinado-Baker, My and Bowman, C.- E.), PP. 2944. Ellis Horwood Ltd. Chichester. UK. Taylor 0. R. Jr (1985) African bees: potential impact in the United States. Bull. Enromol. Sot. Am. winter, 14-24. Villa J. D. (1985) Comparative behavior and performance of African and European derived honey bees at different elevations in northern South America. 86 pp. MS. Thesis, University of Kansas, Villa J. D. (1987) Africanized and European colony conditions at different elevations in Colombia. Am. Bee. J. 127, 53-57. Villa J. D., Gentry C. and Taylor 0. R. Jr (1987) Preliminary observations on thermoregulation, clustering, and energy utilization in African and European honey bees. J. Kansas Entomol. Sot. 60, 4-14. Winston M. L.. Taylor 0. R. and Otis G. W. (1983) Some differences between temperate European and tropical African and South American honeybees. Bee World 64, 12-21. Woyke J. (1973) Experiences with Apis mell$era adansonii in Brazil and in Poland. Apiacra 8, 115-I 16.
Vol. 97A.
No.
1,pp. 1-7,
0300-9629190 53.00+ 0.00 0 1990Pergamon Press plc
1990
Printed in Great Britain
COMPARATIVE ENERGY BALANCE IN GROUPS OF AFRICANIZED AND EUROPEAN HONEY BEES: ECOLOGICAL IMPLICATIONS E. E. SOUTHWICK,* D. W. ROUBIK~ and J. M. WILLIAMS~ *Department of Biological Sciences, State University of New York, Brockport, NY 14420 USA. Telephone: 716-395-5743, Fax: (716) 395-2416; tsmithsonian Tropical Research Institute, Balboa, Republic of Panama, APO Miami 43002, USA: and fJohn M. Williams Associates, Box 281, Brockport, NY 14420, USA (Received
22
Noaember 1989)
Groups of honey bees (&is me//$m L.) are able to metabolically regulate their central temperature under cold stress. At 2C, Africanized honey bees in 30g groups consumed 46.4% more oxygen per unit time holding their core temperatures at 29.O”C compared to European honey bees. 2. Differences in oxygen consumption increase as group sizes decrease. Regression analysis at freezing temperature showed that the two races attain similar costs of energy balance with the same mass when Africanized colonies contain about 20,000 bees and European colonies contain 16,000 bees (Fig. 1). 3. Africanized honey bees tested in groups at temperatures of 2°C and - 15°C showed metabolic rates that were 13-109% higher than those of the temperate region honey bees, but at 22.5”C, the cost of energy maintenance was 54% lower. We predict that physiological and behavioral characteristics combined with climatic conditions in North America will limit the northern distribution of nesting Africanized honey bees to a 120 consecutive day isoline of temperatures not exceeding 10°C during Winter (Fig. 2). In some southern regions of the USA, the Africanized race will have competitive advantage over the European honey bees now extant. Abstract-l.
INTRODUCTION The Africanized honey bee race currently occupies habitats in all of Central and most of South America. It is a hybrid bee similar to Apis mellifera scutellata (Lepeletier), a honey bee native to the lower middle
elevations of southern and eastern Africa (Boreham and Roubik, 1987; Roubik, 1988a, 1989; Ruttner, 1988). Potential expansion of the geographic range of this insect into cooler regions raises a central question of colony survival at high latitudes and altitudes. Can this honey bee thermoregulate and survive the cold northern winters which would be encountered in the mid- and northern latitudes in the United States? Which features of individual and colony biology are relevant in making such predictions? The future distribution is dependent on a number of factors, one of which is the colonies’ capacity to actively control brood nest temperature during exposure to low ambient temperatures. Without a stable brood nest temperature near 35°C during midwinter, honey bees in the temperate zone could not begin the timely production of brood needed for resource collection in spring and summer. This would probably lead to colony death during the following winter (Seeley, 1985; Seeley and Visscher, 1985). A key factor in survival of the honey bee colony is the use of physical and physiological mechanisms that allow for successful overwintering in north temperate zones (Southwick, 1985a, 1988, 1989, in press). Comparisons between Africanized and European honey bee colonies in this regard have been inconclusive but have suggested no significant differences in nest heat regulation and mass-specific honey con-
sumption under cool conditions (Dietz et al., 1988; Villa, 1985; Villa et al., 1987). However, Southwick (1988) pointed out that no data exist on the metabolic responses of Africanized honey bee colonies or even of the individual workers to exposure to ambient temperatures less than 15°C. Considerable data have been published on the thermal capacities of European honey bees, primarily Apis mellifera carnica in West Germany, and mixed racial hybrids in the United States (Heinrich, 1981; Ritter, 1982; Southwick, 1988, 1987, 1985a, 1983, 1982; Southwick and Heldmaier, 1987). These studies revealed that temperature equilibrium is achieved in the intact colony through mechanisms that balance routes of energy gain and energy loss. Under the low-temperature conditions of primary interest in the present study, thermal control, especially of the central brood area, is achieved by a colony through maintaining large numbers of individuals and large honey stores under winter conditions. In a colony of roughly 20,000 individuals, the bees cluster tightly together, affecting the important pathways of heat flow by effectively reducing convective and radiative heat loss, and increasing metabolic heat production as the colony’s stores of carbohydrate are converted to heat energy. The positioning of individuals within the cluster, particularly at the periphery of the cluster and between and against the cells of insulating empty wax comb, has also been shown to be important (Southwick, 1985b, c). Presumably, any colony of honey bees that could achieve thermal balance under low temperature conditions would do so by utilizing these physiological and behavioral mechanisms (Southwick, 1988).
E. E.
2
3
10
100
1000
Mass
(g
SOUTHWICK
3000
I
Fig. I. The relation of bee cluster mass and minimum maintained oxygen consumption achieved by groups of Africanized honey bees (filled circle, this study) and groups of European honey bees (open circle, from Southwick, 1985a) held at constant air temperature of 2 C overnight. MR = 69.79 M-06’, R’ = 0.95 (n = 17 Africanized bee groups) MR = 22.69 M “48. R’ = 0.96 (n = 16 European
bee groups, after Southwick 1985a) where MR is metabolism in ml 0,;gjhr and M is group mass in g. The six points indicated as triangles are metabolic values maintained just before these small groups of 50 Africanized honey bees fell into cold comatose condition from which they could not recover without an increase in air temperature.
The first invasion of Panama bees in 1982 demonstrated extremely
close
in size and
by Africanized honey that the bees were
behavior
to the original
et al.
African Apis mellifera scutellata brought to Brazil in 1956 (Boreham and Roubik, 1987). We use the term “Africanized” to denote that the bees are a product of hybridization between one African race and five other races of European origin that were maintained in the American tropics and which have interbred, albeit slightly, with Apis mellifera scutellata (Ruttner, 1988; Smith et al., 1989). In this paper, we report comparative measurements of oxidative metabolism at low temperatures by groups of honey bees of the Africanized and European races currently occupying Panama. The study provides the first metabolic measurements of Africanized honey bees during exposure to moderately low ( < 15’C) temperatures. The results help to clarify the temperature/metabolism relationships and thermoregulatory capacities of honey bees and provide data for predicting the geographic distribution population.
of the expanding
Esperimen~al
animuls
Africanized
honey
bee
METHODS
Morphometric analysis of feral honey bees in the American tropics is essential to characterize their origin; Africanized honey bees are, in general, smaller than all varieties of European honey bees (Daly and Balling, 1978; Ruttner, 1988). Two morphometric traits that provide
L Fig. 2. Isolines showing numbers of consecutive days when the normal highest temperature is below 10°C. These isolines were constructed from the climatological history of 250 weather reporting stations throughout the United States for the period of 1951-1980. The contours were constructed using the normal maximum temperatures for each station. The general reduction of temperature with altitude was considered by adjustment along topographical contours. This is seen, for example, near the Sierra Nevada range. near the Front Range of the Rockies, and, to a lesser extent, near the Alleghenies. (Data from National Climatic Data Center, no date.)
Energy
balance
and distribution
maximum discrimination are the length of the worker forewing and the width of the “wax mirrors” on abdominal sternites (Boreham and Roubik, 1987; Daly and Balling, 1978). Samples of at least 10 bees were taken from each colony used and scored for these two characteristics. Numerous hives of Africanized honey bees were established by native beekeepers from feral honey bee swarms in central Panama. There are currently no other varieties of honey bees living in the wild or in apiaries on the mainland. The European honey bee colonies used were taken from San Jose Island in the Pacific Ocean 70 km from the Panamanian mainland (Pearl Island Archipelago, 8 ‘15’ N, 79-8’ W), where European honey bee queens produced commercially in the southern United States have been imported each year for use in apiculture (Roubik, 1988b). Each honey bee group used in the experiments was taken from a single colony and usually consisted of about 300 workers, but some tests were run with several size groups of 50 to about 8000 workers. Metabolic measurements Test groups of worker bees were placed in ventilated air-tight acrylic chambers complete with empty and honeyfilled comb on which to cluster; large groups had their own stored honey supply and small groups were provided ad libirum with a sugar candy (honey mixed with powdered sugar) throughout the experiments. Preliminary test runs revealed no difference in metabolic rates of small groups with or without queens, so all tests were run without queens except where noted. For small group comparisons, each test run utilized three groups (i.e. one Africanized and two European, or vice versa) and a control chamber without bees tested at the same time. Sequential respiratory gas measurements were taken at 5 min intervals, using a microprocessor controlled electronic valve manifold. For each test, the metabolic chamber containing bees was placed within the controlled temperature cabinet at about 1330 hr each day. Following procedures previously described by Southwick (I 982) fresh air was drawn through the chamber by a diaphragm pump at about 500 ml/min (with flow rate controlled by a needle valve). The air stream entering each chamber was dried by passing over columns of Drierite (CaSO,), and carbon dioxide was removed by columns of Ascarite (NaOH coated asbestos). The exit stream was dried and carbon dioxide removed and then routed through an oxygen analyser (Applied Electrochemistry S-3A with a double cell sensor, N-37M, and R-2 flow control, accuracy of +O.OOl vol%). The carbon dioxide was removed and not measured because we assumed that the respiratory quotient (RQ = moles carbon dioxide released/moles oxygen consumed) was equal to one (1 .O). Previous measurements with ad libirum honey-fed European honey bees showed this to be consistently the case, at least under the conditions of test runs up to 24 hr long (Southwick, 1985a). Oxygen contents of the air streams could be determined digitally and were simultaneously recorded on a YSI strip chart recorder for later analysis. Gas flow rates were determined with a Gilmont flowmeter which had been calibrated against a soap film flow meter (+ 1%). Any error in flow rates would have been in a consistent direction (all values too high or too low). This was not the case as born out in our results, so this type of error must be small and is not further considered. Oxygen consumption was determined by comparing the oxygen contents of the air flowing into and exiting the chamber after correction for carbon dioxide removal.
in honey
bees
mate because we were not certain of cluster positioning when placement of the thermocouples was fixed. All tests were under dark conditions (D:D). Sufficient time was allowed to reach minimal metabolic rates to allow for comparisons with data in the literature, usually about 15 hr (Southwick, 1985a). After minimum metabolic rates were determined, the bees were weighed and numbers of individuals were estimated by sampling groups of IO or more bees for individual weights. We did not attempt to measure crop contents. The two temperatures of exposure reported here were f2”C and - 15°C to allow comparisons with existing published data. RESULTS
Morphometry Morphometrics
of
the
Africanized
honey
bee
colonies, all collected near the Pacific coast of central Panama in December and January, showed that the bees were strongly African and were relatively small compared to Africanized honey bees sampled throughout South Africa in the early 1970s (Boreham and Roubik, 1987; Dale and Balling, 1978). These authors found an average forewing length of 8.65 mm (range 8.33 to 9.05mm) and a wax mirror width of 2.17 mm (range 2.01 to 2.38 mm) for Africanized honey bees. Forewing length averages ranged from 8.39 to 8.61 mm among bees sampled from the 10 Africanized honey bee colonies used in this study, and those of wax mirror width were 2.11 to 2.27 mm. All coefficients of variation were between 1% and 3%. The two European honey bee colonies had average forewing lengths of 8.92 and 9.02 mm, and wax mirror widths averaging 2.45 mm. The European honey bees sampled by Daley and Balling (1978) from South American colonies averaged 9.12 and 2.36 mm for these two traits, respectively. Metabolic rates Comparative data on minimum metabolic rates of groups of Africanized and European honey bees were obtained at temperatures of 2°C and - 15°C. At 2°C (Table 1), small groups of African honey bees weighing about 30 g showed significantly greater metabolic rates than groups of European honey bees of similar mass. Under these conditions, the Africanized honey bees consumed 46.4% more oxygen per gram and per unit time in order to maintain their heat balance (with the approximate central cluster temperature maintained at 29.0 + 1.52C, n = 8) than did the European honey bees (cluster temperature of 29.7 k l.O”C, n = 6). Live weight of honey bee test groups was 30 g for both races, but due to the smaller individual mass of Africanized workers (88 mg, on average, vs 111 mg for Europeans), there were more bees in their groups. On average, 301 individuals made up an Africanized Minimum metabolic rates (oxygen consumption, VO,) in groups of about 300 honey bees exposed to 2’C
Table
I.
small
broodless
overnight
in Panama,
Temperarure monitoring Simultaneous measurements of several temperatures inside and outside the chamber, in the central cluster, and the outer region of cluster, were taken utilizing Cu-Con thermocouples connected to a Bailey Instruments thermocouple meter and paper chart recorder (YSI dual channel recorder). Central cluster temperatures are only approxi-
3
C.A.
(data
expressed
as mean k SE)
Africanized Live
mass
Worker
number
Group vo, VO,
30.
per bee
I k 2.61
301 + 18’ 8.64 f
(163400)
I.01 ml O,/g/hr*
864 ~1 O,/hr (n = 15 groups)
*Statistically
significant
European 28.
g
difference
I i 1.38g
232k
II*
(If@-312)
5.90 k 0.53 ml O>/g/hr* 715~1
O,/hr
(n = I3 groups) (P cl 0.01).
E. E.
4
SOUTHWICK et al.
group, with only 232 individuals in a European group. Africanized groups showed 46% higher rates of mass specific metabolism, but at the individual level, an African bee consumed, on average, 21% more oxygen per hour per bee than its larger European counterpart. When exposed to 2 C overnight, groups of different sizes (50 to 8000 individuals) showed great differences in the minimum metabolic rate maintained, which was directly dependent on group size (Fig. 1). At this cool temperature, there is an increase in mass specific metabolic cost as the groups become smaller in numbers of bees or mass (not reduction in size by tighter clustering of the group). Groups of 50 Africanized workers were too small for thermoregulatory control overnight at this temperature (2 ‘C) as indicated by total loss of thermal control. All bees in the 6 groups of 50 bees tested at 2-C fell into “cold coma” after only 226 hr of exposure. Three groups of Africanized honey bees, one of 351, one of 440, and one of 7020 workers, were tested at - 15 ‘C for 15 hr. They maintained central cluster temperatures at 28 to 3 1 C without losing many outer individuals (< 5%) to cold coma. The groups consisting of 351 individuals and 440 individuals (30.9 and 43.4 g, respectively) consumed 15.8 and II.2 ml O?/g/hr. This is about 3.5 times the rate of the groups at exposure to 2-C. The 7020 bee group. which formed an intact colony with queen and brood (total mass 618 g) displayed a metabolic rate of 6.47 ml O2 /g/hr at - 15’C, about 5 times greater than at 2’C (I. 18 ml Oz/g/hr) and 7.5 times higher than at 22.5’C (0.88 ml OJg/hr). DISCCSSION
Throughout the ecological experiment created by uncontrolled spread of Africanized honey bees through the Americas, one of the most frequently asked questions is, how far north will they go? The ability to achieve temperature regulation strongly influences the extent of Africanized honey bee colonization in North America (Roubik, 1987; 1990). One way in which our data are useful is in predicting climatic limits of the colonizing population, which should continue to be feral and therefore not available for manipulation by apiculturists. Clearly, other ecological variables such as the influence of natural enemies and competitors. and the availability of nesting localities and food sources are also important. Additional data is needed on foraging behavior, nesting behavior, colony growth, and other variables as they relate to honey bee distribution (Roubik, 1989; 1988b, 1990). The range expansion of Africanized honey bees will likely be limited by factors such as habitat and competition, and their colony demography in northern habitats will likely be influenced by both the migratory habit of human beekeepers combined with control measures taken by human beings. Our data on metabolic capacities at low temperatures, combined with the known behavioral characteristics of European and Africanized honey bees (summaries by Winston et al., 1983; Rinderer, 1988; Southwick, 1989, in press; Roubik. 1989. 1990) provide some straightforward predictions for the
impending States.
colonization
Thermoregulatory
of
the
southern
United
costs
Even though the small groups of European honey bees we tested were 10% lighter than the groups of Africanized honey bees (28.1 vs 31.2 g), which would be expected to raise their mass dependent metabolic rates, the European honey bees still consumed less oxygen to maintain their normothermic central cluster temperature under the 2°C experimental conditions. The measurements we obtained on cost of thermal control in a full size queenright colony of Africanized honey bees at the cool 2-C environmental temperature yielded values of metabolic rate 13% higher than predicted by data published on European honey bees (full size queenright colonies) at the same temperatures (Southwick, 1985a). In fact, all the mass specific metabolic data we obtained on African honey bee groups were 13% to 109% higher than predicted from European data at environmental temperatures below IO’C (Southwick, 1985a, 1988). We have also an interesting comparison at a thermoneutral temperature, since at 22.5 C the metabolic costs to Africanized bees were 54% lower than the predicted value for temperate European honey bees. The tropical honey bees are obviously better adapted to warm temperature than their northern counterparts. Examination of comparative honey bee colony performance at higher temperatures would be worthwhile. Thermoregulatory activities of honey bee clusters are dynamic and complex (Southwick, 1985a). The cluster geometry of Africanized honey bees under low temperature stress is not yet elucidated adequately to understand if there are patterns (such as cluster “tightness”) that might affect the limits of northern nesting. For all group sizes that were tested, Africanized honey bees had higher mass-specific metabolic rates than those reported for European honey bees. Differences between Africanized and European bees were more pronounced in smaller groups. This might indicate that in such groups the Africanized bees cluster less tightly or are less efficient in preventing heat loss. They were also noticeably more nervous in the experimental setup at moderate temperature, although no differences could be seen at 2-C. When log-transformed, the data fall on straight lines, as plotted in Fig. I. The slopes are significantly different (P < 0.01). with the steeper slope displayed by Africanized groups. The plots for the two honey bee races intersect at 1790.6 g which is about equal to 16,000 European honey bees or 20,000 Africanized honey bees. All the Africanized bees in the smallest groups tested overnight at 2-C each comprised of 50 bees, died of cold exposure after only a few hours. Few European bees (mean of I2 individuals or 24% from 37 groups) in similar size groups tested under the same conditions by Southwick (1985a) entered cold coma even after I5 hr or more at this temperature. Ecological implications of colony size are related to thermoregulatory capacity. As the numbers of individual workers within the colony decrease. the
Energy balance and distribution in honey bees metabolic costs of temperature maintenance increase more rapidly in the Africanized hybrid. This is important in considering limits of expansion of the population of Africanized honey bees for at least three reasons. First, all colonies lose progressively more individuals (which die) as the confinement period is extended. This “winter loss” is substantial, even in European colonies (Farrar, 1963). So as the winter temperatures prevent flight, it becomes more and more costly for the group to continue thermal control, with these costs rising faster for the Africanized clusters. Second, as Africanized honey bees will tend to enter autumn and winter seasons with relatively small colonies (certainly less than the 30,000 bees recommended for success, Furgala, 1975) from poorly established late summer swarms, they will be under increased thermal stress even at the beginning of the low temperature season. Third, the smaller overwintering colonies will be prevented from the early colony growth considered to be critical for success (Seeley and Visscher, 1985). The stresses associated with the smaller winter clusters of Africanized bees can be expected to exacerbate “stress diseases” such as Nosema. Survizlability at low temperature The length of the foraging season in north temperate regions is one of the factors that will determine distributional limits of Africanized honey bees. At high elevations in Colombia, near 2000 to 3000m, colonies nesting in the wild displayed emigration or disappearance after 4 months of rainy or otherwise poor foraging conditions (Villa, 1987). In northern Argentina, Dietz et al. (1988) found that bee colonies purportedly of Africanized stock survived approximately three months in a refrigeration chamber. The honey-hoarding and foraging behavior of Africanized compared to European honey bees has received experimental study by Rinderer et al. (1985) who suggested that the Africanized race forages more consistently than European honey bees, but amasses smaller food stores. This behavior has been interpreted as a reflection of “high efficiency” foraging by European honey bee colonies, which need relatively large honey stores and worker bee populations in order to produce metabolic heat and allow brood production during winter months. In contrast, foraging for “high harvest rate” is shown by African honey bee colonies which reproduce as rapidly as possible, at the expense of forager longevity and total colony efficiency (Winston et al., 1983; Seeley, 1985; Roubik, 1989). No study has determined whether Africanized honey bee colonies initiate brood production in midwinter, seen as an essential factor in colony survival by European honey bees (Seeley and Visscher, 1985). We still do not know what specific changes in social organization are involved in the evolution of cold tolerance. From our data collected in Panama and other limited data available, the length of time that a colony is confined to low temperatures and prevented from foraging seems critical to Africanized honey bee colony survival. When in cool conditions of 10°C or lower, there was no flight or foraging activity by Africanized honey bee colonies (Villa, 1987, personal communication; this study). They may not only run
5
out of stored food faster than European races, but their cluster formation may prevent them from even moving to available food stores within the nest. Villa (1987, personal communication) found that clusters of Africanized honey bees at 4000 m elevation in Venezuela formed tighter and more compact clusters than those formed by European honey bees when the same mass of bees of each group was exposed to an environmental temperature of about 10°C. He also found that some colonies of Africanized bees that died during prolonged confinement at low temperatures still had stores of honey within their nests. We noted that the small experimental clusters in Panama were unable to move for more than an hour after removal from 2°C in test chambers, compared to activity within a few minutes by European honey bees. Within such clusters, the movement of workers may be essential to move to new honey storage areas on the comb, but such dynamics are still inadequately understood for Africanized or European honey bees. Our preliminary observations suggest that they may be important for colony survival at lower temperatures, irrespective of the amount of honey hoarded by the colony. Furthermore, the survival of a colony depends upon increased worker longevity during the winter. The higher metabolic rates observed for Africanized honey bees would tend to reduce their longevity (Winston et al., 1983; Sohal, 1986) such that, irrespective of honey stores, the shorter lifespans of Africanized workers would limit colony survival. A number of investigators have moved African and Africanized honey bees from their native habitats to northern areas for study. None have reported success in maintaining colonies over lengthy cold winters. Woyke (1973) transported Africanized honey bees (Apis mellifera scutellata) from Brazil to Poland and was unsuccessful in overwintering any colonies there. African honey bees kept in Oberursel, near Frankfurt, West Germany, did not maintain their colonies over the winter (unpublished observations). In fact, the standard practice used by the Oberursel Institut fuer Bienenkunde has been to house African queens in large colonies of European honey bees (Apis mellifera carnica or Apis mellifera mellfera) in order to “keep” them over the winter (Koeniger, personal communication). African queens are not maintained through the winter with their own African workers. There is recent evidence (Smith et al., 1989) that Africanized honey bees may not be hybrids after all, but instead may be genetically pure descendants of the original African founder population. Thus, there is probably little dilution of African traits (including those related to thermoregulation) through hybridization as the population spreads into North America. This suggests that there may be a fairly sharp boundary to the African honey bees’ northern range. Predicted distribution Because of nest confinement below IO’C, isolines of lOC, shown in Fig. 2 with numbers of days presented, are likely to indicate the maximum winter survival limits of Africanized honey bee colonies in North America. North of any isoline, air temperatures do not exceed 10°C during the numbered
6
E. E. SOUTHWICKel al
consecutive days. The question remains: how long can the Africanized honey bees be confined and still survive? The evidence from the energetic analysis reported in this study and from the other cited studies on behavior and social organization indicate that survival would be no longer than about 90 to possibly 120 days. The probable maximum survival time of 120 days gives an isoline, labelled 120, north of which all feral Africanized colonies would probably die of confinement and/or depletion of their food stores. South of the 120 day isoline, Africanized bees might be able to survive even through the winter. The use of the 120 day, 1OC isoline as a maximum is supported from the comparative data previously cited from high altitudes in northern South America (Villa, 1987; personal communication) where the racial type of Africanized honey bees is not in question. However, the true limit may be further south, particularly since we do not know whether workers in the colony at the onset of winter could actually survive for an additional 120days. The 120day limit includes most of Long Island, New York, parts of Pennsylvania, central Ohio, Illinois and Indiana. and the southern borders of Iowa and Nebraska, central Colorado, northern Utah, Nevada, western Idaho, and Washington state. Geographic pockets of ameliorating temperature are found to vary with altitude in mountain regions allowing for successful overwintering north of the 120 day isoline and limiting overwintering south of the line as in the Sierra Nevada mountains of California. Of course, some Africanized honey bees at the northern limits of their nesting range will certainly produce highly mobile reproductive swarms as well as absconding swarms throughout the summer season as they do in their tropical environments (Kigatiira. 1988). These would disperse well beyond the predicted winter limit. Feral colony distribution would be expected to show annual fluctuation around this line, if, in fact, the colonies can survive there throughout the winter. Our estimate of 120 days survival time yields a northern nesting limit considerably further north than other predictions based on other temperature data without the metabolic and behavioral backup. For example, Taylor (1985) published a map based soley on low daily temperatures, which is considerably south of our predicted limit. His prediction includes limits of feral nesting Africanized bees only in the very southernmost tips of California, Arizona, Texas, Louisiana, Georgia and Florida. As we have stressed, ecological variables of many kinds are still too poorly understood to predict which, if any, would exert a control of honey bee colony survival of a type superseding that of the thermal environment. For at least portions of the southern United States, it does appear that feral Africanized honey bees are at a thermal advantage over European honey bees now feral in this region (Taylor, 1988). The Africanized honey bee is inferior to European honey bees in cold tolerance, as demonstrated by comparative colony energy balance and behavioral characteristics. The distribution of the feral Africanized honey bee colonies, which have by far the most significant impact on beekeeping and the ecology of local plants and animals, will be strongly
limited by their relatively inefficient attempt to thermoregulate during extended exposure to low temperatures. We are most grateful to G. F. Novey and son for logistic support and permission to work with their honey bee colonies. DWR acknowledges the support of Smithsonian Institution Scholarly Studies grants for research on Africanized honey bees and EES acknowledges a short-term visitor research grant from that institution. REFERENCES
Boreham M. M. and
Roubik D. W. (1987) Population change and control of Africanized honey bees in the Panama canal area. Bull. Enfomol. Sot. Am. 33, 34-39. Daly H. V. and Balling S. S. (1978) Identification of Africanized honey bees in the western hemisphere by discriminant analysis. J. Kansas Entomol. Sot. 51, 8577869. Dietz A., Krell R. and Pettis J. (1988) Survival of Africanized and European honey-bee colonies confined in a refrigation chamber. In Africanized Honey Bees and Bee Mites (Edited by Needham, G. R., Page R. E. Jr, Delfinado-Baker M. and Bowman, C. E.), pp. 2377244. Ellis Horwood Ltd, Chichester, UK. Farrar C. L. (1963) The overwintering of productive colonies. In: The Hire and the Honey Bee. p. 341. Dadant and Sons. Hamilton. IL, USA. Furgala B. (1975) Fall management and the wintering of productive colonies. In The Hior and the Honey Bee, pp. 471490. Dadant and Sons, Hamilton, IL, USA. Heinrich B. (1981) The mechanisms and energetics of honey bee swarm temperature regulation. J. E.xp. Biology 91, 25m55. Kigatiira 1. (1988) Amalgamation in tropical honey bees. In Africanized Honey Bees and Bee Mires (Edited by Needham G. R.. Page R. E. Jr. Delfinado-Baker M. and C. E.), pp. 62-17. Ellis Horwood Ltd. Bowman, Chichester, UK. National Climatic Data Center (no date) Chmatography of the United States, No. 84. Daily normals of temperature, heating, and cooling degree days and precipitation, 195 I 1980. Microfiche, National Oceanographic and Atmospheric Administration, Asheville, TN. USA. Rinderer T. E. (1988) Evolutionary aspects of the Africanization of honey-bee populations in the Americas. In Afiicanked Hone}, Bees and Bee Mites (Edited by Needham G. R.. Page R. E. Jr. Delfinado-Baker M. and Bowman C. E.), -pp. 13-28. Ellis Horwood Ltd. Chichester. UK. Rinderer T. E.. Collins A. M. and Tucker K. W. (1985) Honey production and underlying nectar harvesting activities of Africanized and European honeybees. J. Apiculr.
Res. 23, 161-167.
Ritter W. (1982) Experimenteller Beitrag zur Thermoregulation des Bienenvolks (Apis melliftira L.). Apidologie 13, 169. 195.
Roubik D. W. (1987) Long-term consequences of the African honey bee invasion: implications for the United States. In Proceeding.s of Afiicanked Honey Bee Symposium. pp. 46-54. American Farm Bureau, Park Ridge, IL. USA. Roubik D. W. (1988a) An overview of Africanized honeybee populations: reproduction. diet, and competition. In A,fricanized Honey Bees and Bee Mites (Edited by Needham G. R., Page R. E. Jr, Delfinado-Baker M. and Bowman C. E.). pp. 45554. Ellis Horwood Ltd. Chichester, UK. Roubik D. W. (1989) Ecology und Narurul History qf Tropicul hers, 524 pp. Cambridge University Press, New York.
Energy
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and di stribution
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