Important plants for stingless ( and Trigonini) and Africanized honeybees (Apis mellifera) in neotropical habitats: a review M Ramalho, A Kleinert-Giovannini, Vl Imperatriz-Fonseca

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M Ramalho, A Kleinert-Giovannini, Vl Imperatriz-Fonseca. Important bee plants for stingless bees (Melipona and Trigonini) and Africanized honeybees (Apis mellifera) in neotropical habitats: a review. Apidologie, Springer Verlag, 1990, 21 (5), pp.469-488. ￿hal-00890877￿

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Important bee plants for stingless bees (Melipona and Trigonini) and Africanized honeybees (Apis mellifera) in neotropical habitats: a review

M Ramalho, A Kleinert-Giovannini, VL Imperatriz-Fonseca

Departamento de Ecologia Geral do Instituto de Biocièncias, Universidade de São Paulo, 05508, São Paulo, Brazil

(Received 13 July; accepted 3 August 1990)

Summary — This paper reports on and sources for stingless bees in neotropical habi- tats. Some 288 were considered important bee plants. Eighty of these were important for the Africanized honeybee. Plant families with the largest number of important species for both bee groups are also among those with the greatest diversity in neotropical regions. Some differences among the bee groups are highlighted Africanized honeybee / Melipona / Trigonini / bee plant / neotropics

INTRODUCTION plants (Crane et al, 1984), but at the same time this makes comparison with other Studies of flower visiting by species of bee species difficult. As to studies of the stingless bees and Africanized honeybees floral origin of using pollen grains in neotropical regions of the Americas are analysis (eg Barth, 1970 a,b), they present still few and far between, and limited in estimates of nectar collecting from each scope, with variable objectives and metho- plant species, but these are subject to er- dologies (Absy and Kerr, 1977; Roubik, rors of interpretation due to variations be- 1978, 1979; Iwama and Melhem, 1979; tween different plant species in terms of Absy et al, 1980, 1984; Engel and Dinge- pollen grains production. With a few ex- mans-Bakels, 1980; Sommeijer et al, ceptions, studies of bee communities 1983; Imperatriz-Fonseca et al, 1984, (Sakagami et al, 1967; Sakagami and La- 1987, 1989; Silveira et al, 1984; Ramalho roca, 1971; Heithaus, 1979; Roubik, 1978, et al, 1985, 1989; Roubik et al, 1986; Klei- 1979; Cortopassi-Laurino, 1982; Laroca et nert-Giovannini and Imperatriz-Fonseca, al, 1982; Hakim, 1983; Opler, 1983; Orth, 1987; Kleinert-Giovannini et al, 1987; Cor- 1983; Camargo and Masukato, 1984; topassi-Laurino and Ramalho, 1988; Ra- Knoll, 1985; Bortoli, 1987; Knoll et al, malho, 1990). Thus any review such as 1987; Almeida and Laroca, 1988; Knoll, this must be selective and preliminary in 1990) fail to present data on the use of nature. Bee plants have been character- specific floral sources, since they deal with ized most frequently in relation to observa- ecological questions at a different level of tions of Africanized and European honey- analysis, such as: diversity and phenology bees when visiting flowers, and this has of bee species, characterization of syn- yielded significant information on bee dromes and guilds of flower visitors, etc. Hence in this review of bee plant spe- and Laroca, 1971; Orth, 1983; Knoll, 1985; Knoll cies in neotropical zones, we have only and Imperatriz-Fonseca, 1987; Almeida and La- roca, 1988; Knoll, considered quantitative information on 1990). flower visiting which permits a comparison of the value of specific floral sources for stingless bees and for Africanized honey- RESULTS AND DISCUSSION bees. Most of the data used were based on melissopalynological studies, whose positive and negative aspects are notori- ous (Louveaux et al, 1978). The data on flower visiting by species of stingless bees and Africanized honeybee mellifera in habitats METHODS (Apis L) neotropical are summarized in table I. Of the 23 stud- ies mentioned, 5 compare Africanized hon- The important floral sources of pollen and nec- eybee and stingless bees, and a further 6 bees and tar for stingless (Melipona Trigonini) compare Melipona and Trigonini. In 6 of and Africanized honeybees in neotropical habi- the studies, there is information on Melipo- tats were reviewed and a synthesis prepared. The species important for Africanized honeybee na alone, and in 9 others, the information were included in the results taken from studies concerns only Trigonini. The data shown in comparing Africanized honeybee and stingless table II are therefore biased as regards the bees. With regard to the plant species already number of plant species visited by the dif- included in the list according to the above criteri- ferent groups of bees, or by 2 or more on, information taken from stud- supplementary groups. The studies were conducted in ar- ies of Africanized honeybees was added. eas with different types of vegetation, influ- Most the data were obtained via a pollen enced in some cases by the presence of analysis of the food collected by bees. In these and or urbanization. cases, we selected only plant species with a agriculture, pasture Some studies were carried out in natural pollen representativity exceeding 10%, or from the pollen categories "frequent" (5-30%), "abun- forests, a very few in grasslands or savan- dant" (> 30%), "secondary" (15-45%), and "pre- nah. Herbaceous species and shrubbery, dominant" (> 45%), in accordance with classifi- both ruderal and opportunistic, albeit origi- cation schemes used various authors by nally under forest cover, are evidently and Melhem, 1979; and (Iwama Engel Dinge- abundant in areas with mans-Bakels, 1980; Sommeijer et al, 1983; Im- open vegetation. peratriz-Fonseca et al, 1984, 1987, 1989; Ra- Table II shows all the plant species with malho et al, 1985, 1989; Kleinert-Giovannini the highest levels of representativity in the and Imperatriz-Fonseca, 1987; Ramalho, 1987; diet of these bees in accordance with the Cortopassi-Laurino and Ramalho, 1988). Absy’s quantitative studies listed in table I. Partic- studies (Absy and Kerr, 1977; Absy et al, 1980, in the case of the families of 1984) provided us with the plant species most ularly plant frequently found in pollen and nectar samples, greatest significance for bees in neotropi- those most persistent throughout the year (in cal zones, some common trends in latitudi- number of months), or those visited by the larg- nal distribution may be detected. Generally est number of stingless bees. Roubik et al’s speaking, the families with a larger number study (1986) provided us with references to the of ie , utilized by bees for species, Compositae, plant species "heavily" pol- Labiatae, len. A few field studies were used to list plant , Leguminosae, species visited by > 5% of the total number of Melastomataceae, Moraceae, Myrtaceae, individuals of some species of and Palmae, and , are Africanized honeybee on flowers (Sakagami also the most consistent pollen and nectar

sources from the South of Brazil (South roca et al, 1982, Orth, 1983; Knoll, 1990). America) up to the South of Mexico (North Compositae and Labiatae predominate as America). In addition to the studies re- bee plants in areas with open vegetation, ferred to in table I, some field studies (Sak- often under anthropic influence. Palmae is agami et al, 1967; Sakagami and Laroca, more important in forested intertropical 1971; Roubik, 1978; Laroca et al, 1982; zones. and an extensive of Knoll, 1990), survey The following genera were important for the principal pollen sources for European both stingless bees and Africanized honey- and Africanized in the Central honeybees bees virtually over the entire neotropical and Western of Panama et parts (Roubik zone: Alchornea, , Cassia, Ce- al, 1984) confirm this trend. cropia, Croton, Euphorbia, Miconia, Mimo- The families mentioned above comprise sa, Piptadenia, Solanum, Tibouchina, Tre- ≈ 60 000 species. Except for Compositae, ma and Vernonia. The importance of Labiatae and Leguminosae, with 25 000, Cecropia (Moraceae) is surprising in view 3 000 and 17 000 species respectively, the of the supposedly anemophilous nature of rest are mainly distributed in tropical and this group, which is commonly found at the subtropical regions all over the world (Joly, forest edge, on river banks, and in secon- 1977; Heywood, 1978). Species of Com- dary forests throughout the neotropical positae and Labiatae are very abundant in zone. Piptadenia seems to be especially woodlands, wooded grasslands, grassland important for bees on the Atlantic coast of and bushland formations of South Ameri- , from the South to the ca, but are poorly represented in the tropi- Northeast of Brazil. Other native genera cal rain forests. Species of Caesalpinoi- frequently cited in the literature and which deae and (Leguminosae) are regionally important are: Spondias are also more common in the tropics and (Anacardiaceae), Protium (Burseraceae), subtropics. The neotropics are distin- Euphorbia (Euphorbiaceae), Byrsonima guished as a zone in which Solanaceae is () and Eugenia (Myrtaceae). as the second con- concentrated, largest Out of a total of approximately 288 plant centration of Euphorbiaceae and Palmae, species, 126, 52 and 25 plant species and the main center for of dispersion Myr- were important solely for Trigonini, Melipo- with as well as taceae, together Australia, na and Africanized honeybee respectively. noted for the of Melasto- being presence Fifty-three plant species were important mataceae, one of the largest families in both for Trigonini and Melipona. It should South America. be noted that the information available for Thus when a general view is taken, it is Melipona covers 13 species as opposed to evident that the main pollen and nectar that for Trigonini, which covers 36 species, sources for stingless bees are to be found so that the data are biased in favor of the among the plant families which are best latter group of bees. Finally, 58 species represented in neotropical habitats. Re- were simultaneously important for African- gional differences can be seen, nonethe- ized honeybees and stingless bees. In this less. For example, the families , case, there is an evident underestimation Labiatae and are important of the number of plant species that are im- for bees in the subtropics or in the zones portant for both bee groups, in view of the where the tropics meet the subtropics, as small number of comparative studies (table shown by studies conducted in the South I). Be that as it may, when only compara- of Brazil (Sakagami and Laroca, 1971, La- tive studies are considered, Trigonini may appear to be a more generalistic flower vis- local context most of the food is obtained itor than Melipona (Roubik, 1978; Orth, from only a few plant groups (table I), de- 1983; Knoll, 1990; and table II). Roubik spite the huge number of important floral (1978) also notes that Trigonini seem to be sources available on a regional scale and a more generalistic flower visitor than Afri- the vast plant diversity in tropical forest canized honeybees in forest and savanna habitats (even when subject to anthropic habitats of Amazonia. influence). Preferential relationships of stingless As regards the impact of Africanized bees with some plant families also seem honeybees on neotropical bee plants, and possible (table II). If the frequency with particularly on stingless bees, there are which plant families are important in the forecasts of local extinction (Roubik, 1978; various habitats or areas under study (ta- Roubik et al, 1986). Roubik (1989) admits ble I) is considered, the following overall that "Africanized honeybees seem prea- picture emerges: the families Legumino- dapted to invade and persist in mosaic sae, Myrtaceae, Palmae and Rubiaceae tropical habitats which gives them advan- are important for Africanized honeybees, tages over native bees", mostly owing to Trigonini and Melipona; Anacardiaceae, their generalized nesting habits. These Balsaminaceae, Compositae, Euphorbia- bees are also better adapted than Europe- ceae, Labiatae, Moraceae, an honeybees to foraging in conditions of and Sterculiaceae are more important for low nectar availability (Rinderer et al, Africanized honeybees and Trigonini than 1984, 1985), a situation which can be com- for Melipona; Ericaceae, and Um- mon at the forest edge and in open areas belliferae are more important for Trigonini with unmanaged flora in the neotropics. than for Africanized honeybees and Meli- Stingless bees are particularly abundant in pona; Mimosoideae (Leguminosae), Me- regions of rain forest and subhumid forest lastomataceae, and Solanaceae are more zones of the neotropics, and are evidently important for Melipona than for Africanized adapted to the seasonal or apparently un- honeybees and Trigonini. This kind of defi- foreseeable rhythms of flowering and vari- nition is obviously circumstantial and has ations in floral composition (as part of the to be experimentally verified. high degree of diversity) in relatively close Stingless bees have perennial colonies areas within neotropical forest habitats. It with specific populations of varying size is not yet clear whether in such habitats the basis and of food favors but, with some exceptions (eg some spe- pattern supply cies of ), far smaller than those of the Africanized honeybee’s foraging strate- Africanized honeybee colonies. Seen from gies, although countless native plant spe- cies are food sources for this a cost-benefit angle, for stingless bee colo- important bee. nies of a small size, it is an advantage to exploit flowers less frequently visited by those with a larger population, while for the latter it may well be that the adoption of which them more of a com- strategies give ACKNOWLEDGMENTS petitive edge in productive resources (Johnson and Hubbell, 1974, 1975; Hub- bell and Johnson, 1978) is their main method for meeting their energy needs. We wish to thank Mrs TC Giannini for help Thus it is no surprise to find that in a given in elaborating the table. Résumé - Les plantes mellifères impor- quement les trigones, les mélipones et les tantes pour les abeilles sans aiguillon abeilles africanisées, respectivement. Cin- (mélipones et trigones) et les abeilles quante trois espèces sont importantes africanisées dans les régions néotropi- pour les trigones et les mélipones à la fois. cales : une synthèse. Cet article pré- Les informations disponibles pour les méli- sente une synthèse des sources de nectar pones couvrent 13 espèces, alors qu’elles et de pollen pour les abeilles sans aiguil- en couvrent 36 pour les trigones; les don- lon dans les régions néotropicales (Amé- nées sont donc biaisées en faveur de ces rique du Sud, sauf Patagonie et Amérique dernières. Comme cela peut toujours se centrale). Seules ont été prises en compte produire quand on ne fait que des études les informations quantitatives concernant comparatives, les trigones semblent être les visites de fleurs, ce qui permet de com- plus généralistes que les mélipones dans parer la valeur des sources florales spéci- leurs visites de fleurs. Cinquante huit fiques pour les abeilles sans aiguillon et espèces sont importantes pour les 2 les abeilles africanisées (tableau I). La plu- groupes d’abeilles, abeilles sans aiguillon part des données ont été obtenues par et abeilles africanisés. Il y a une sous- l’analyse pollinique de la nourriture récol- estimation évidente du nombre d’espèces tée par les abeilles. Quelques études de importantes pour les 2 groupes, étant don- terrain ont été utilisées pour les listes de né le faible nombre d’études comparatives plantes visitées par les 2 groupes (tableau I). d’abeilles. Les études ont été faites dans En ce qui concerne l’impact des abeilles des avec des de régions types végétation africanisées sur les plantes mellifères néo- influencés la variés, parfois par présence tropicales et en particulier sur les abeilles de ou d’agriculture, prairies par sans aiguillon, on peut prévoir l’extinction l’urbanisation. Certaines ont été menées locale de plantes données. Mais l’on ne dans des forêts très dans naturelles, peu sait pas encore si la base et les modalités des régions d’herbages ou de savane. de l’offre de nourriture dans les habitats fo- Les familles botaniques suivantes : restiers néotropicaux favorisent les straté- Anacardiacées, Composées, Euphorbia- gies de butinage des abeilles africanisées, cées, Labiacées, Légumineuses, Mélasto- bien que de nombreuses espèces de matacées, Moracées, Myrtacées, Pal- plantes indigènes soient d’importantes mées, Rubiacées et Solanacées, qui sources de nourriture pour ces abeilles. renferment le plus grand nombre d’espèces importantes, à la fois pour les abeille africanisée / Melipona / Trigoni- abeilles sans aiguillon et les abeilles afri- ni/ plante mellifère / région néotropi- canisées (tableau II), sont aussi parmi cale celles qui présentent la plus grande diver- sité dans les habitats néotropicaux. Les genres Alchornea, Baccharis, Cassia, Ce- Zusammenfassung - Wichtige Tracht- cropia, Croton, Euphorbia, Miconia, Mimo- pflanzen für Stachellose Bienen (Meli- Tre- sa, Piptadenia, Solanum, Tibouchina, ponen und Trigonen) und für Afrikani- ma et Vernonia sont les 2 importants pour sierte Bienen an neotropischen Stan- groupes d’abeilles dans pratiquement dorten : Eine Übersicht. Diese Arbeit toute la zone néotropicale. bietet eine Übersicht über die Pollen- und Sur un total de 288 espèces de plantes, Nektarquellen von Stachellosen Bienen an 126, 52 et 25 sont importantes pour uni- neotropischen (= südamerikanischen) Standorten. Es wurden nur zahlenmäßige wenn man nur die Vergleichsstudien he- Informationen über den Blütenbesuch ranzieht, so ergibt sich, daß die Trigonen berücksichtigt, wodurch ein Vergleich des beim Blütenbesuch stärkere Generalisten Wertes spezifischer Trachtblüten für Sta- sind als die Meliponen. Für beide Bienen- chellose Bienen und für Afrikanisierte Hon- gruppen, Stachellose Bienen und Afrikani- igbienen möglich wird (Tabelle I). Die meis- sierte Honigbienen, waren 58 Pflanzenart- ten Daten wurden durch die Pollenanalyse en gleichermaßen wichtige Trachtquellen. der von den Bienen gesammelten Nahrung Es besteht eine deutliche Unterschätzung gewonnen. Außerdem wurden einige Feld- der Zahl von Trachtpflanzen, die für beide beobachtungen zur Aufstellung von Listen Gruppen von Bedeutung sind, besonders der von beiden Bienengruppen besuchten wenn man die geringe Zahl vergleichender Pflanzenarten herangezogen. Die Untersu- Studien berücksichtigt (Tabelle I). chungen wurden in Gebieten mit unter- Was die Auswirkungen der Afrikanisier- schiedlicher Vegetation durchgeführt, in ei- ten Honigbienen auf neotropische Bie- nigen Fällen beeinflußt durch landwirts- nenpflanzen und besonders auf die heimis- chaftliche Viehweide oder Nutzung, chen Stachellosen Bienen betrifft, so gibt städtische Andere wurden in Siedlungen. es Voraussagen für ein lokales Aussterben ursprünglichen Wäldern durchgeführt und bestimmter Arten. Aber es ist noch keines- sehr in Gebieten mit Grasland oder wenige wegs klar, ob die Basis und das Muster Savanne. des Nahrungsangebots in neotropischen Die Pflanzenfamilien Anacardiaceen, Waldstandorten die Sammelstrategie Afri- Compositen, Euphorbiaceen, Labiaten, Le- kanisierter Bienen begünstigt. Es ist zu be- guminosen, Melastomataceen, Moraceen, denken, daß dieser Biene zahllose heimi- Myrtaceen, Palmae, Rubiaceen und Sola- sche Pflanzenarten als wichtige Nahrung- naceen enthalten einerseits die größte squellen zur Verfügung stehen. Zahl wichtiger Arten sowohl für die Sta- chellosen wie für die Afrikanisierten Bienen Afrikanisierte Biene / Melipona / Trigoni- (Tabelle II), anderseits zeigen sie aber die ni / Bienenpflanzen / neotropische Zone größte Vielfalt an neotropischen Standor- ten. Die Gattungen Alchorea, Baccharis, Cassia, Cecropia, Croton, Euphorbia, Mi- REFERENCES conia, Mimosa, Piptadenia, Solanum, Ti- bouchina, Trema und Vernonia sind für Absy ML, Kerr WE (1977) Algumas plantas visi- beide Bienengruppen in praktisch der ge- tadas para obtencão de pòlen por operàrias samten neotropischen Zone wichtig. de merrillae em Manaus. 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