The Brazilian bee problem.

ANNUAL REVIEWS

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Annu. Rev. Entomol. 1975.20:399-416. Downloaded from www.annualreviews.org Access provided by North Dakota INBRE on 12/21/14. For personal use only.

THE BRAZILIAN BEE

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PROBLEM1 Charles D. Michener Department of Entomology and Department of Systematics and Ecology. The University ofKansas. Lawrence. Kansas 66045

There have been repeated and sometimes lurid references to the introduction of African honey bees into South America, to the spread of such bees or their hybrid descendants (Africanized bees, i.e. the Brazilian honey bee), and to the influence of such bees on apiculture, pollination, animal husbandry, and public health in South America and, prospectively, in North America. Much of what is known about these bees in South America appears in the Final Report of the Committee on the African Honey Bee (27) and in two subsequently annotated versions of the same report (31). One function of the present review is to place some of the content of these reports in more accessible form. Another is to review the numerous more recent contribu tions on the subject, largely from Brazilian sources (including references 13, and 14; proof sheets of only a few articles in reference 13 were available when reference 27 was prepared). Emphasis is placed on the history, present status, and principal attributes of these bees. An account of their possible impact in North America is given in the first report mentioned (27). Some of the questions about these bees have so far been answered from reports of beekeepers, rather than by controlled experiments or observations. Because of variability of the population over a vast area, the results of experiments even where they have been carried out may not be applicable everywhere. Sources of informa tion are therefore documented below. The code B indicates information from bee keepers, including anecdotal information from scientists. SP refers to observations or experiments made on the population of bees of the central part of the state of Sao Paulo (Piricicaba, Rio Claro, Ribeirao Preto, etc), where most of the experimen tal work has been done; in effect, it means under the conditions of central Sao Paulo. 'Contribution number 1551 from the Department of Entomology. The University ofKan sas. Lawrence. Kansas. 66045. 399

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HISTORY AND CURRENT STATUS


Origin and Spread

Before its spread by man, Apis mellifera ranged from northern Europe to the Cape of Good Hope and eastward into western Asia. It varies geographically, as indicated by the recognition of various subspecies (41, 52, 70), some of them regarded as species by Maa (57). European subspecies were long ago carried to many parts of the New World; the history of their introduction into Brazil is given by Nogueira Neto (63). In tropical American countries they were not especially successful. The widespread subspecies of subsaharan Africa, Apis melli/era adansonii. however, is very abundant both in equatorial and warm temperate southern Africa and is an excellent honey producer (52, 72, 73). It is often aggressive and appears to quickly eliminate all colonies of European bees taken into its range. Writing in Tanzania before the Brazilian bee problem was recognized, Smith (72) said: "Viciousness is the first characteristic which beekeepers and others encounter. .. . The colonies always appear to be alerted, ever ready to defend the hive, and on occasion the whole colony goes berserk and stings every living thing in sight. A beekeeper can usually smoke a colony and get it under control while he collects the crop. But if he appears near the hive a second time within several weeks the bees are on him. " Portugal Araujo (66, 68) indicates similar problems in Angola on the opposite side of Africa. Other authors (I) speak of it as gentle; obviously there is great variation among colonies and populations of African bees and indeed other subspecific names have been given to certain high montane and coastal populations (74), as well as to the form occupying a limited area around the Cape of Good Hope. A. m. adansonii was introduced into Brazil in 1956 in order to develop a tropical or subtropical-adapted strain having improved honey productivity. Queens that reached Brazil were mostly from near Pretoria, South Africa (over 1500 m altitude, 26° S; therefore, an area with cool winters), although one was from Tabora, Tan zania. Colonies showing desirable characteristics were to be selected from among hybrids resulting from crosses of European and African bees. However, in 1957, 26 queens mated in Africa escaped with swarms. T,bus A. m. adansonii was introduced into South America near Rio Claro, Sao Paulo, Brazil. (For details of introduction see 27, 31, 40, 43, 44, 67, 77.) The progeny of 26 queens and the perhaps 200 males with which they had mated introduced genetic materials that rapidly spread over an area already approaching that of the contiguous states of the United States, a biologically remarkable performance. The spread is shown in Figure 1. It is impossible to know how much of the dispersal has been natural and how much due to movement of queens or colonies by beekeepers. No doubt both factors have been involved. The African bee is regularly migratory in certain areas (72) and it is not surprising that Brazilian bees show signs of similar abilities and have spread rapidly by swarming and by abscond ing of colonies. At least for a time the rate of spread was in the vicinity of 320 km per year (27, 31). The name Brazilian honey bee has been applied to the strain


BRAZILIAN BEE PROBLEM

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"'"----- Mexico City

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Cities of equivalent

latitude in the north

Figure 1

Spread of the Brazilian honey bee (27). ?

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area of a possible introduction into

Roraima Territory, Brazil. Southward and westward distribution appears to have been slight since

1971.

Further northward spread is unverified.

spreading in South America (27), the attributes of which are in many ways similar to those of A. m. adansonii in spite of interbreeding with the European bees. European bees have largely vanished from the area where Brazilian bees have been for several years (27, 31). There are two ways in which such an introduced race might spread. One is by either aggression against the established race or by winning in the competition for environmental resources, such as food or nest sites. This could happen with little interbreeding. The other is by gene flow into the established popplation.Both have probably occurred in this instance. There are reports of colonies entering apiaries, clustering on or under a hive, and ultimately invading, replacing the queen of the hive. Such aggressive replacement appears to have been common in some areas (8;


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coastal Sao Paulo), rare in others (only one hive in a thousand invaded, SP, 31). It is verified by the finding of dead Brazilian queens in front of Italian hives protected by queen excluders at their entrances (16); these queens were not able to get in when their workers did and died outside. Some of the spread of African genes, however, has doubtless been by means of gene flow. Most European queens returned to their colonies after mating flights and produced workers having at least some African attributes, indicating that they had mated with drones of the Brazilian population (B; 27, 3 1). Individual colonies of Brazilian bees (SP) may have a higher life expectancy than do those of Italian bees. A probability of survival of Brazilian colonies four times longer than for Italian colonies has been indicated, and attributed to characteristics of the workers, not of queens (3 1). The basis for this statement is not clear, but for 10 colonies of Italians and 10 colonies of Brazilians (SP), survival was as follows: Italians-after 6 months seven colonies survived but after 12 and 15 months, only one (which had a hybrid queen) survived; Africans-after 6 months six colonies survived, after 12 months five survived, and after 15 months four survived (51). These 20 colonies were initially of about equal strength, 1500-2000 bees, and were left in boxes essentially undisturbed, subject to periods of food shortage, attacks of ants, and the other vicissitudes experienced by wild small colonies. If verified by more data, these findings may explain part of the success of the Brazilian bee. The longer survival of Brazilian colonies suggests that they may be better at replacing queens than are European colonies under Brazilian conditions. Queen replacement (SP) is apparently more frequently necessary than in temper ate climates; significant racial differences were not noted. Five normally mated Brazilian queens in hive colonies survived a mean of 8.4 months; 6 normally mated Italian X Brazilian queens survived for a mean of 7.4 months. Eighty artificially inseminated queens, half of them Italians and half Brazilians, survived an average of only 4.2 months (51). The reproductive behavior of males seems similar to that of European males in such matters as time of day and durations and numbers of flights (28). An experi ment appears to show partial reproductive isolation that diminishes intersubspecific matings when equal numbers of reproductives of both Italian and Brazilian (SP) races are present (48, 49). (It must be noted that if there were Brazilian drones of unknown origin in the mating area, so that their number exceeded that of Italian drones, interpretations of this experiment would be in some ways different.) Twenty virgin Brazilian queens were inseminated by Brazilian drones in 58.5% of the inseminations, and 21 virgin Italian queens by Italian drones in 64.8% of the" matings. These results are based on identification of the race (or hybridity) of 200 worker progeny of each young queen. Recognition must have been based on mor phology or color and is therefore questionable but in this limited context as distin guished from variable populations from wide areas, the recognition of the races and their hybrids was presumably accurate. In this experiment the Brazilian queens mated, on the average, with about 7.5 males while Italian queens mated with about 5.3 males each. The latter number is little over half-that reported for temperate regions. It would be interesting to know if Italian queens, under SP conditions, mate



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relatively few times even when undisturbed or if Brazilian drones somehow interfere with mating by the Italian bees. The number of sperm cells produced by males of Italians is somewhat less (mean 5,463,000; N = 14) than by Brazilians (mean 7,123,000; N = 14) (SP, 48). FI hybrids contain a mean of only 3,205,750 (N = l2)-a distinctly reduced number further suggesting slight reproductive isolation-and F2 hybrids showed great variability, as might be expected (see reference 48 for statistical details). An outstanding feature of both African and Brazilian bees is the large number of colonies found per unit area. The high frequency of interracial matings that was partially responsible for the demise of European bees in Brazil must be largely due to the enormous feral populations attained by Brazilian bees. There are no data on abundance of feral European bees in Brazil prior to 1957. However, my general observations (1955-1956) indicate that in southern Brazil (Parana, Sao Paulo) they were about as scarce as they are in woods in the United States. This means that although workers were common on flowers, it was difficult to find nests or to attract a swarm to an empty box. In tropical forested parts of Brazil, Panama, Costa Rica, etc, in areas not yet reached by Brazilian bees, comparable observations indicate that European bees are far less common than in the United States. One can often collect flower-visiting insects for long periods without seeing an Apis. The Brazilian bee changed this; the only quantitative data are from savanna (cerrado) areas in the states of Goias and Mato Grosso where Kerr (46) found an average of 107.5 colonies of feral Apis per km2• Nests are common not only in the traditional places but in holes in the ground, in termite mounds, etc. Reportedly, Brazilian bees will occupy smaller cavities than those utilized by European races (B; 27, 31). On highly attrac tive flowers in Parana and Sao Paulo, J. S. Moure (personal communication) reports up to 15 workers per m2 in areas without beekeeping. A result of the large feral populations of Brazilian bees is that virgin queens from apiaries encounter large numbers of Brazilian drones with which they can mate. Of course another result of the large feral population is intense competition for food resources with the hive bees of whatever race (35). Variation A frustrating aspect of the literature on Brazilian honey bees has been the divergence of opinions and information presented. The contradictory statements are probably mostly justified for different times and areas. Great genetic variability is to be expected in a population of hybrid origin. Moreover, differential selection is to be expected-the distribution encompasses well over 30° of latitude from treeless temperate grasslands to the xeric scrub of northeastern Brazil and the equatorial rain forest of the Amazon basin. Subsequent sections contain references to differences between northern and south ern populations of Brazilian bees. No one has experimentally moved bees from one area to another to verify that these differences are genetic rather than the direct effects of environmental and colonial conditions (weather, nectar flow, colony strength, etc). Yet it seems extremely probable that most of the differences recorded do result from differi ng amounts of hybridization with European bees and differing


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subsequent selection, and so have genetic bases. In the states of Sao Paulo and even Minas Gerais and the more southern states of Parana. Santa Catarina. and Rio Grande do SuI. there were rather numerous beekeepers and some feral European bees. Hence there were many European bees with which invading Brazilian bees could mate. To the north and especially in the far north and northeast. beekeepers were much less numerous and feral European bees were rare. One would. therefore. expect the Brazilian bee of the northern states to be more like its African ancestors than is the southern population. This initial probable difference has been augmented by several factors. as follows. In view of the effect of the Brazilian bee on apiculture and because of the public outcry against it. W. E. Kerr produced and supplied to beekeepers queens of European bees (mostly Italians) with the objective of diminishing the undesirable features of Brazilian bees. In 1963-1964 200 Italian queens mated primarily with Italian drones were distributed; in 1965-1972 23.000 virgin Italian (including a few Caucasian) queens were distributed (3 I). W. E. Kerr is convinced that this program played a significant role in improving the characteristics of the bees over a wide area, in spite of reports that some beekeepers killed the queens (especially those mated to Italian drones) because of their belief that the European attributes included lower honey production (27. 31). Since the European queens went to beekeepers, they further augmented the European attributes of the population in southern Brazil. Some beekeepers destroy or requeen their most aggressive colonies and put frames of drone comb into their gentlest and most productive colonies. as recommended as early as 1964 (12, 30). Kerr (45. 47) provides practical recommendations for selection toward mildness. Cosenza (22). advocating continuation of such pro grams of improvement by beekeepers. also recommends further introduction of European genes but Weise, Kerr. and many other Brazilian apiculturalists do not. for fear of reducing the high productivity. These practices. plus perhaps natural selection. appear to be leading to the devel opment of a reasonably tractable southern Brazilian population, well adapted to its subtropical and warm temperate environment. Some beekeepers work without gloves, a few even without shoes, veils, or shirts, to demonstrate the gentleness of their bees (27, 31). In short, the suggestion in the title of Kerr's (42) paper "The Solution is to Create a New Race" is being realized (80), albeit belatedly and after considerable grief. Those who have seen only this form often feel that the situation · does not warrant costly measures to prevent further spread. Comparison of the present situation in southern Brazil with the strong reaction against the Brazilian bees in the early years of their invasion of these same areas (10-12,62) and currently in Argentina, Bolivia. Paraguay, and Uruguay (4, 5, 15, 26, 34-39. 65) seems to verify improvement of the bee population, although familiarization of beekeepers with attributes of a race of bees new to them is doubtless part of the story (27, 31. 75). Meanwhile, to the north and especially northeast, where there are few beekeepers. selection may have favored those that flew farthest into areas with almost no competing Apis, and thus largely escaped the European influence. In any case, the population in arid states like Pernambuco. Rio Grande do Norte. and Ceara is



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highly aggressive, quite different from that in the south (27, 31). The appearance of people who sell honey from wild colonies (31), in an area where Apis honey was previously little known, shows that the species has become common in the bush. Destruction of wild colonies in the process of taking honey is probable and selection favoring aggressiveness is therefore likely at present. The same thing may be occur ring in other areas; for example certain Paraguayan Indians formerly little interested in honey are now producing much more, mostly from wild colonies (79). Exporta tion of large amounts of honey now (first major year, 1972; 31) from northeast Brazil (Recife) suggests that apiaries there too are productive and evolution like that in the south may result. The most noteworthy attribute of the northeastern populations (at least in 1971; 27) is frightening and is described below in the section on Stinging. Northward Dispersal

By 1971 Brazilian honey bees had reached Belem, the Ilha de Maraj6, and across the Amazon, Macapa, humid areas all near the mouth of the Amazon (27, 31). African bees occur in wet tropical forests (73; Michener, personal observations in Cameroon), although probably less commonly than in savanna. Whether or not the Brazilian bee reached the Amazon under its own power or was carried there, it seemed likely that it would continue without delay across the rest of the Amazon forest. This may now be happening, although recent reports indicate that it is not common on flowering plants near Belem (31). It may be that all but the best located colonies are destroyed during wet seasons and that progress through the humid tropics will be slower than anticipated in 1971. Nesting sites in the Amazon forest are reported to be restricted to large dead dry trees (33). Unverified press reports of the Brazilian bee as far north as the Orinoco River in Venezuela in 1973 suggest, on the other hand, that the Amazon forest did not delay it greatly. The attributes of the bees which will presumably finally pass through (or around) the forest and continue on their way toward North America cannot be predicted. A single report from Porto Velho, Rondonia (B), farther west in the Amazon area, compares the bees favorably with those of southern Brazil (31). At least there are not many people in the forest whose activities might cause selection for aggressive ness. For the future, one must presume that the Brazilian bee will migrate through Central to North America, to latitudes where the climate is similar to that of the southernmost areas now occupied in Uruguay and Argentina. But what its at tributes will then be cannot be predicted. Current Brazilian conditions show that it can be modified; changes in it will doubtless occur as it moves northward. It could be as intractable as the present population of northeastern Brazil, or it could have attributes like the southern Brazilian population. Much will depend on the stocks of Apis which it encounters and on their abundance. A barrier of abundant gentle bees (27) could presumably modify it as it moves northward. An important factor in the future spread of Brazilian bees is their overwintering ability. There are no records of winter cluster formation. Thermoregulation is reported to be less efficient for African bees than for European ones (25), although no direct comparisons were made; the frequency of subterranian nests in Africa may


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be a result of the uniform temperature of such sites. In cold weather Brazilian bees are reported to abscond or to continue activity in the nest (B; 27); in the latter case, stores are quickly used up. Long cold spells are therefore commonly fatal, leading to high autumn mortality on the southern Brazilian plateau and presumably explain ing the failure of African and Brazilian bees to become established when introduced into central or eastern Europe (81) or the United States. [Stort reports that a beekeeper in South Africa has sent (iIl�ally) various African queens to the US in recent years (31). Presumably their colonies would thrive only in the southernmost states.] Winter mortality would be a serious problem for southern queen or package bee producers marketing in regions of colder climates, no matter what other features the population might have. CHARACTERISTICS OF THE BRAZILIAN HONEY BEE Some attributes of the Brazilian bee that conspicuously relate to its history and spread are discussed above. Other features are summarized below. No one feature will always distinguish Brazilian or even African bees from European bees. Means differ, and the combination of characteristics is distinctive. Differences all are quan titative, i.e. of degree and not of kind. Every seemingly peculiar feature of Brazilian bee behavior has its counterpart, perhaps seen only rarely, in European bees. Color, Size, and Morphology

Color is highly variable but most workers have yellow abdominal bands. J. S. Moure (personal communication) reports about 15% of workers to be black in areas in Parana and Santa Catarina. As in Africa, a single colony commonly has both black and partly yellow workers (27). Kerr (30) considers chestnut bronze abdominal terga to be characteristic of drones (SP) but other color patterns (with yellow) are also found in northern Brazilian drones (27) and in Africa (66, 67). In size Brazilian bees average slightly smaller than European races. Virgin queens of Italian and Caucasian bees weigh 208.8 ± 25.39 mg SD (N Il l ) and 207.7 ± 21.07 mg SD (N 132), respectively, whereas equivalent figures for Brazilian queens (SP) are 199.3 ± 25.59 mg SD (N 110) (30). Numerous measurements of various structures of workers verify the smaller size of Brazilian bees (23, 69). Of possible importance in relation to feeding and pollination is the observation that glossal length of Brazilian bees averages 3.87 mm, compared to 4.15 mm for Cauca sian bees and 4.02 mm for hybrids (23). Size of worker cells is correlated with bee size. For Brazilian bees, measurements across 25 adjacent cells (not made on foundation) averaged 12.6 cm (range 12.113.6, N = 55 colonies) (27). There was no significant difference between northern and southern regions. For European bees at Guelph, Ontario, comparable figures were 13.5 cm (range 12.9-14.3, N 41 colonies). Measurements of comb from small numbers of colonies by others (e.g. 23) give similar results. Kerr and his associates emphasize that while none of the newly introduced African bees would use standard comb foundation, Brazilian apiary bees, especially =

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in southern Brazil, now do so. Even there wild swarms may not use standard foundation (B; 27, 31). Selection for European genes including larger-sized bees is presumably responsible for the change. Maa (57) gave some morphological characters for the recognition of Apis mel/if era adansonii. No one of them seems reliable, probably especially for the Brazilian bee. However, H. V. Daly (not published), using numerous measurements of each bee and multivariate analysis, has demonstrated the possibility of distinguishing Brazilian from European forms by simultaneous consideration of the various fea tures. Size was the most important factor in his study but after its removal apprecia ble variation remained and aided in making distinctions. The greatest need in tracing the spread of the Brazilian honey bee is ability to identify it on the basis of few specimens. Daly's methods offer the best hope for doing so. The situation is not simple, however, as illustrated by the following comment from W. E. Kerr (personal communication): "In Colombia and Venezuela there is a hybrid between A. m. melli/era and A. m. ligustica that has many genetic segregants that resemble the African bee, both in external morphology and in temper." He first saw this form in 1952, four years before introduction of African bees to Brazil. This form evidently lacks the ability found in Brazilian bees to form large feral populations, to spread, and to replace other European bees. Gonr;alves (29) and Stort (78) have analyzed the inheritance of various morpho logical features in relation to aggressiveness in crosses and backcrosses between Italian and Brazilian (SP) bees. Characters which within one group of crosses or another showed significant correlations with one or more components of aggressive ness included diameter of median ocellus, tergal and sternal measurements, and mesoscutal measurements. Isozymes

Mestriner (59) found a difference in allelic frequencies between Brazilian bees (SP) and Italian bees, on the basis of 68 colonies of the former and 7 of the latter, a total of 300 workers analyzed. At what he called the P3 locus, both races were variable, the Brazilian bee with the allele P3S at a frequency of .�9S, P3F at .006. Comparable figures for Italian bees were P3S .531, P3F .469. Thus the Brazilian bees were almost monomorphic at this locus. Other loci examined showed no racial differences. Individual and Colonial Development

The developmental period of workers of Brazilian bees is reported to be about a day shorter than for European bees (51,80). Although similarly short development may occur in European races (27), a mean difference in developmental period seems to exist for workers (but not for reproductives) reared in the same region. Colony growth of Brazilian bees is reported to be rapid (B; 27, 31). That these reports are justified is suggested by the large numbers of eggs laid in 3 colonies of Brazilian bees (SP), as compared to 3 colonies ofItalian bees and 3 of hybrids. Over a 12-month period, the totals for the 3 colonies of each type were 104,520; 58,164; and 55,390 eggs, respectively (51).

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General Activity

Brazilian and African bees seem more excitable and active than European bees, although not as much as Apis cerana (as I have seen it in Java and MalaysIa). Flight around flowers is quicker and more nervous than that of European bees (27, 31). Brazilian bees often fly right into the hive entrance rather than alighting and walking in. Nunez reports that Brazilian bees make decisions more rapidly than European bees (SP; in 31). Waggle dances often indicate the directions to food sources as little as 20 m away (SP; 27, 31) (or 33 m in African bees, in Tanzania; 71). These distances are much shorter than for European bees. The general high activity of Brazilian bees is evident the moment a hive is opened. When a comb is lifted the bees run on it, often form hanging festoons, and many of them may take flight. These features are most evident and very troublesome in northern Brazil, less obvious in southern Brazil, and scarcely apparent in the gen tlest (most Europeanized?) colonies (27, 31). Movement of hives in migratory bee culture is sometimes said to lead to balling and killing of queens (27; Santa Catarina), but in Sao Paulo (31, 50) and with African bees in South Africa (32, 60) no such problem is reported. Foraging

Brazilian bees are reported to start work earlier and finish later than European bees, often working on cool days and almost until full darkness in the evening (B; 27, 31, 44). However, analysis of data on temperatures and times of day of flights of some 885,000 bees (SP; 51) does not strongly verify this statement. There were no appre ciable differences in hour of starting and Brazilian bees were recorded flying only 12 min later in the evening than Italian bees. Temperatures required for activity also scarcely differed for Brazilian and Italian colonies. However, there was a marked difference in the time of maximum flight activity. Maximal activity for Italian bees was from 8:30 to 10:30 A.M., with decreasing flight activity during the afternoon. Brazilian bees as well as hybrids, however, showed maximal activity in the after noon. If one wishes to work hives when the maximum number of bees are afield, one works Italian colonies in the morning, Brazilian colonies in the afternoon (B, SP; 51). These results were obtained over a period of 13 months and hence are unlikely to result from a flower favored by the Brazilian colonies that produces nectar or pollen largely in the afternoon. Since most flowers are richest in nectar in the morning, the behavior of the Brazilian bees is unexpected. At calibrated syrup sources (50% sucrose), compared to Italian bees a Brazilian bee (SP) makes briefer visits and carries less to the hive per trip (64). For high flow rates this difference could result merely from the smaller crop capacity, 54.6 ± 7.34 mg (N = 42) for Brazilians, 65.1 ± 9 26 (N = 50) for Italians (2), but at low flow rates the difference is augmented. At a rate of 0.70 J.Ll/min, Brazilians carry 67% less per trip than Italians. Below that rate motivation for collecting by Brazilian bees disappears while Italians continue working at least to 0.35 J.LlImin. Because Brazil ian bees take less time to take food, they return more often to their colonies. This should lead to more communication and to larger recruitable populations at any .



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time. Thus Brazilian bees may be adapted to large nectar sources and to quickly recruiting many bees to exploit them (64). Production figures for typical Brazilian municipios show sharp reductions in number of hives and total honey crop during 3 or 4 years after arrival of Brazilian bees (27). Comparisons of hives of different races in the same apiary consistently show the excellent production of Brazilian bees compared to European races at the same times and places (40). Cosenza (19, 21) compared production of 6 colonies of Caucasian bees, 22 colonies of Brazilian bees, and 22 colonies of Brazilian X Cauca· sian hybrids during one month in Minas Gerais. All colonies were about the same size. The Caucasian bees produced nil; the Brazilians and hybrids produced equally, averaging about 9 and 5.5 kg of honey each in two different apiaries. As another example, Portugal-Araujo (67) reports average honey production of 8.8 kg, 19.2 kg, and 35.5 kg per hive for 10 hives each of black European, Italian, and Brazilian bees, respectively, during a nectar flow of about 65 days (SP). Presumably the 30 hives were in the same apiary and similar in strength. There are many reports of excellent annual productivity, e.g. 80 colonies (SP) that produced an average of 68 kg of honey each in 1969; in the first four months of 1970 some of the same colonies had gathered over 100 kg of honey and one, over 200 kg (31,51). Or again, in Parana, 180 kg of honey per hive are recorded annually (75). Annual production figures should be higher than in cool temperate climates where cold often prevents foraging. Because of excellent productivity, most Brazilian beekeepers, particularly in the south, favor the Brazilian bee, although some (but not others) say that temperate area colonies use so much honey to keep alive in winter that the advantage of this race disappears (B; 27, 31). Most of the high production noted by beekeepers is with fewer colonies in the apiaries than formerly, when European bees were used. Thus there may be more forage per colony than was customary for the European bees. However, the large competing feral populations should have the opposite effect; some beekeepers de stroy feral colonies before moving hives into an area. Simultaneous controlled tests of productivity should be repeated. Such tests must be done in such a way as to guard against robbing, for Brazilian bees are excellent robbers (27, 31) and for this test must be prevented from foraging in the hives of their competitors. A laboratory assessment of hoarding might prove informative (53). Brazilian bees are highly variable in propolization but some collect even more propolis than Caucasian bees, making working of hives difficult and slow (27). Absconding and Swarming

Brazilian bees do not die in the hive for lack of food and water; they abscond instead and migrate until they either find a suitable site or die. Small colonies, such as baby nuclei, often abscond when the queen makes her nuptial flight (80); thus it is difficult to use small nuclei for mating queens. Larger colonies do not give trouble by absconding if food, water, and space are available (B; 27, 31), The large number of feral colonies, probably often absconding or swarming because of inadequate space resulting from the rapid colony growth so that a colony quickly outgrows a small cavity, leads to frequent observation of swarms. (Abscond-


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ing colonies look just like reproductive swarms.) Cosenza (18,19) found that 79% of 31 swarms in Minas Gerais occurred during a time of food scarcity, suggesting that they were migratory colonies; 52% of these 31 swarms contained more than one queen, probably as a result of fusion of smaller swarms as is reported in Africa (72, 73) for migrating colonies (but not reproductive swarms). Only 5.7% of 175 swarms observed in northeastern Brazil (state of Ceara) in all months of the year contained more than one queen (51). Migrating colonies with up to 14 queens have been reported (B; 27, 31) and they are sometimes seen to divide into small monogy nous colonies. If fission does not occur, all but one of the queens are killed after the bees enter a nest (31; based on 8 polygynous swarms, SP). The same thing evidently occurs in Africa (1, 72), although multiple laying queens are also reported (68). Queens in swarms are usually mated; all those in Cosenza's 31 swarms had sperm cells in their spermathecae. Swarms are often seen flying, sometimes high (30 m), sometimes across rivers or cities (B; 27, 31). One was reported as landing on a boat 10 km from land in the Amazon estuary. Swarms are often seemingly attracted from the bush to apiaries, where they may invade apiary colonies as indicated above. Swarms are less com monly seen now in southern Brazil than in the years shortly after the Brazilian bee arrived there (B). Stinging

The best known characteristic of Brazilian bees is their aggressiveness (sense of 56). Individual stings of Brazilian bees produce effects comparable to stings from other honey bees; no chemical differences between venoms of Brazilian and Italian bees are known (58). But Brazilian bees, especially in the northern states, differ dramati cally from other races in their sensitivity to disturbance, their ability to communi cate alarm within and between colonies, and their capacity to respond quickly by massive and persistent attack on intruders (27, 31). The mechanisms are not clear but could involve release of greater quantities of alarm pheromones; different behav ior in pheromone release, e.g. release at the hive entrances instead of in the air; enhanced responsiveness to alarm pheromones; increased use of visual or other signals around the victim; or some combination of the above factors. Enhanced responsiveness to the alarm pheromone is suggested by Stort's (31) finding of a positive correlation in Brazilian bees between the number of olfactory sensilla on the worker antennae and both numbers of stings and distance that bees follow a stung object (SP). Among Italian bees no such relationship was found. A study of European bees showed both higher responsiveness to the alarm pheromone and higher production of it in an aggressive line than in a gentle line (3). The slightest disturbance at or near the hive entrance in northern populations of Brazilian bees can set off a chain reaction that explodes within seconds; whole apiaries may go out of control. Hundreds of bees become airborne and pursue and sting any animals or people within perhaps 100 m of the apiary (27, 31). The length of time required for recovery from such a disturbance by Brazilian bees (SP) differs greatly (rom that of Italian bees. According to Stort (77), the former require, on the average, 28.2 min to return to the normal quiet state when there is an enemy

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standing 3 m away (N 45 tests, 9 colonies); Italian bees require 2.9 min (N 25, 5 colonies). FJ hybrids were intermediate but more like theItalians, although highly variable, with a mean of 9.0 min (N 15, 3 colonies). In southern Brazil, colonies rarely go out of control; only rarely in that area do bees from an undisturbed colony fly (2-3 m) and strike the veil of an observer. This is in contrast to experience in the northern states, where bees often attack persons even before they enter apiaries. Some observers report that behavior like that which occurs in the north was prevalent in the south early in the spread of Brazilian bees. Stort (76, 77) provides some documentation for the racial differences in aggres siveness at hive entrances. Using two colonies of Brazilian bees (SP) and four colonies of Italian bees, he jiggled small leather balls in the air for 60 sec at varying distances from the hive entrances. At 30 cm from the entrance, Brazilian bees stung the ball a mean of 14.0 times (5 trials). The comparable figure for Italian bees was 2.2. With greater distances from the hive entrance of course the number of stings diminishes regularly; it will suffice to note that at 1 SO cm from the entrance Brazilian bees stung a mean of 1.2 times, Italian bees 0.2. Cosenza (17, 20) reports on similar tests made on five colonies each of Caucasian, Brazilian, and hybrid bees in Minas Gerais. The balls were jiggled 30 cm from the hive entrances and the time to the first sting and the number of stings in the 60 seconds after the first sting were recorded. Mean times in seconds until the first sting were 229, 14, and 89, respec tively, for the three racial groups; mean numbers of stings were 1.4, 34.9, and 10.5. The differences were highly significant; the hybrids were intermediate between the Caucasian and Brazilian bees in each case. Disturbed Brazilian bees pursue a person or animal that has been stung for distances far greater than is usual for European bees. For the distance followed stung leather balls carried away from the hive by an observer, Stort (77) obtained a mean of 160.2 m ± 40.36 (N 40 tests, 8 colonies) for Brazilian bees (SP), 2 1.5 ± 1 1.67 for Italians (N 20, 4 colonies), and 38.8 ± 25. 12 (N = 15, 3 colonies) for the hybrids. A particularly dangerous attribute of Brazilian bees is their aggressiveness after slight jarring or vibration of the hive. For example, a colony in Rio Grande do Sui judged to be only moderately aggressive when tested using a modification of Stort's method, was extremely aggressive when similarly tested after the hive had been inadvertently slightly jarred (27, 31). The test-leather (2.5 X 2.5 cm) received 92 stings (it was jiggled for only 5 sec) and the bees followed the leather (and the person carrying it) for over a kilometer! Within probably every race of bees there is much variation in aggressiveness between colonies. Brazilian bees are said to vary particularly from day to day, depending upon previous and present conditions (B). Some persons report colonies particularly aggressive during a nectar flow. Others report them particularly aggres sive when there is little food. Some report the bees more aggressive in hot weather, others in cool weather. Some in the tropics reported greater aggressiveness in humid weather. All agreed on one point: aggressiveness is v�riable, and a colony that is hard to handle one day may be relatively gentle another day. Some data on aggres siveness at different seasons are available ( 17). =

=


=

=

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412

MICHENER

Readiness to sting must be determined by a number of different and independently inherited responses, e.g. amounts of alarm pheromones produced and responses to alarm plieromones, vibrations, movements, breath of an intruder, etc. Inheritance of aggressiveness is therefore complex and polygenic. Stort (76) indicated the exist ence of eleven genes controlling aggressive behavior responsible for the difference between Brazilian (SP) and Italian bees. Kerr (31, footnote 32), because of correla tions between some of Stort's characteristics, attributed the effects to eight genes. In addition to the problems around hives or nests of feral Brazilian bees, swarms and absconding colonies constitute a perhaps more severe stinging hazard. Possibly only because of their abundance, swarms land on people and probably on animals from time to time (27, 31). Even a gentle swarm, landing on a person unfamiliar with bees, would probably lead him to attempt to brush them off, inciting stings, in turn probably followed by massive stinging in response to the release of alarm pheromones. There are persistent reports that swarms sometimes attack and sting without provocation, and Smith (73) indicates that in Africa absconding colonies, particularly those which have undergone fusion so that they have several queens, may attack if disturbed, unlike true swarms. There are many reports of animals and even people being killed by stings of Brazilian bees. Some deaths, especially those involving allergic persons, could have occurred had the African bees never been introduced into Brazil. Others resulted from rash efforts to destroy hives in the hysteria arising from overpublicity about the dangers. But there appear to be a substantial number of cases in which animals and men have been severely or fatally stung because of the abundance and special behavioral characteristics of Brazilian bees. Changes in Brazilian Beekeeping Caused by the Brazilian Bee

Before 1957 bees were often kept in or near settlements, especially in southern Brazil and countries to the south. There was no difficulty in obtaining apiary sites. In the tropics, there was little interest in honey bees. After the spread of the Brazilian bee, the situation changed. Most beekeepers had to move their apiaries away from settlements (7, 39, 80). Beekeeping as a hobby almost disappeared and many beekeepers went out of business because they did not want to work with such vicious bees or because they could not operate apiaries on farms along with livestock. Others moved their bees to iso.Iated spots where they could not disturb animals. Although in many areas beekeepers became unpopular, commercial beekeepers especially in southern Brazil mostly feel that the Brazilian bee is superior to any race they have had before. Even in the north this attitude may be developing (for Bahia, see 55). Beekeepers value the large crops of honey that the Brazilian bee produces. In the Recife area in the north, beekeeping has shifted from native stingless bees to honey bees. Changes in bee management resulting from use of the Brazilian bee in Brazil include (a) dispersal of hives into scattered small apiaries (75), (b) wide dispersal of hives within apiaries and facing them in different directions to reduce interactions among bees of nearby colonies (6), (c) use of large smokers (8, 54) and other special equipment (9, 80). In Bolivia the gas N20 at night has been recommended to



413

anesthetize the bees while hives are being worked (37, 38, 39). In southern Brazil some beekeepers make large fires on one side of the apiary to blanket it with smoke before working hives. In southernmost Brazil, in a climate to which the Italian bee is probably well adapted, serious efforts are being made to maintain populations of Italian bees in spite of the feral Brazilian bees (16). This is only possible with queen excluders at the hive entrances to prevent queens in swarms of Brazilian bees from entering. In Argentina and Bolivia also, acceptance of Brazilian bees is far less complete than in the honey-producing states of Brazil. The mutual adaptation of bees and beekeep ers is most complete in the more central part of the range where the Brazilian bee has existed for five or more years. Diseases do not seem particularly prevalent in Brazilian bees and seem to present no special management problems; diseases vary from place to place and reports as to susceptibility relative to European bees vary. Brazilian bees in Minas Gerais remove dead brood from comb more effectively than Caucasian bees and hence may be more resistant to larval diseases; hybrids are intermediate (24). Acarapis woodi. an acarine parasite not found in North America. occurs in Apis in Brazil (61) and is likely to spread with the Brazilian bee. ACKNOWLEDGMENTS

For reading the manuscript and offering useful suggestions, I thank Drs. H. V. Daly, W. E. Kerr, M. D. Levin, W. C. Rothenbuhler, and O. R. Taylor. Literature Cited

1. B avaresco F. A. Apicultu ra afric an a. ,

2.

3.

4. 5. 6. . 7. 8.

9.

See Ref. 13, pp. 3 1 4-21 Beig, D., Pizani. J., Kerr, W. E. 1972. Capacidade estomacal de duas subespe cies de Apis melli/era. Cienc. Cult. Sao Paulo 24:464-68 Boch, R., Rothenbuhler, W. C. 1 974. Defensive behavior and alarm phero mone production in honeybees. J. Apic. Res. In press Boggino, P. A. 1969. Consideraciones a la abeja africana en Paraguay. Gac. Co/menar 3 1 : 1 37-38 Boggino, P. A. 1 97 1 . My experiences with African bees in Paraguay. Am. Bee J. 1 1 1 :232 Both, A. Nova distribuir;ao de colmeias em apiarios com abelhas africanizadas. See Ref. 13. pp. 88-90 Both. A. Nova situa

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