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Important bee plants for stingless bees (Melipona andTrigonini) and Africanized honeybees (Apis mellifera) in

neotropical habitats: a reviewM Ramalho, A Kleinert-Giovannini, Vl Imperatriz-Fonseca

To cite this version: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�

Review article

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 pollen and nectar sources for stingless bees in neotropical habi-tats. Some 288 species were considered important bee plants. Eighty of these were important forthe Africanized honeybee. Plant families with the largest number of important species for both beegroups are also among those with the greatest diversity in neotropical regions. Some differencesamong the bee groups are highlighted

Africanized honeybee / Melipona / Trigonini / bee plant / neotropics

INTRODUCTION

Studies of flower visiting by species of

stingless bees and Africanized honeybeesin neotropical regions of the Americas arestill few and far between, and limited in

scope, with variable objectives and metho-dologies (Absy and Kerr, 1977; Roubik,1978, 1979; Iwama and Melhem, 1979;Absy et al, 1980, 1984; Engel and Dinge-mans-Bakels, 1980; Sommeijer et al,1983; Imperatriz-Fonseca et al, 1984,1987, 1989; Silveira et al, 1984; Ramalhoet al, 1985, 1989; Roubik et al, 1986; Klei-nert-Giovannini and Imperatriz-Fonseca,1987; Kleinert-Giovannini et al, 1987; Cor-topassi-Laurino and Ramalho, 1988; Ra-malho, 1990). Thus any review such asthis must be selective and preliminary innature. Bee plants have been character-ized most frequently in relation to observa-tions of Africanized and European honey-bees when visiting flowers, and this hasyielded significant information on bee

plants (Crane et al, 1984), but at the sametime this makes comparison with otherbee species difficult. As to studies of thefloral origin of honey using pollen grainsanalysis (eg Barth, 1970 a,b), they presentestimates of nectar collecting from eachplant species, but these are subject to er-rors of interpretation due to variations be-tween different plant species in terms of

pollen grains production. With a few ex-ceptions, studies of bee communities

(Sakagami et al, 1967; Sakagami and La-roca, 1971; Heithaus, 1979; Roubik, 1978,1979; Cortopassi-Laurino, 1982; Laroca etal, 1982; Hakim, 1983; Opler, 1983; Orth,1983; Camargo and Masukato, 1984;Knoll, 1985; Bortoli, 1987; Knoll et al,1987; Almeida and Laroca, 1988; Knoll,1990) fail to present data on the use ofspecific floral sources, since they deal withecological questions at a different level ofanalysis, such as: diversity and phenologyof bee species, characterization of syn-dromes and guilds of flower visitors, etc.

Hence in this review of bee plant spe-cies in neotropical zones, we have onlyconsidered quantitative information on

flower visiting which permits a comparisonof the value of specific floral sources forstingless bees and for Africanized honey-bees. Most of the data used were basedon melissopalynological studies, whose

positive and negative aspects are notori-ous (Louveaux et al, 1978).

METHODS

The important floral sources of pollen and nec-tar for stingless bees (Melipona and Trigonini)and Africanized honeybees in neotropical habi-tats were reviewed and a synthesis prepared.The species important for Africanized honeybeewere included in the results taken from studies

comparing Africanized honeybee and stinglessbees. With regard to the plant species alreadyincluded in the list according to the above criteri-on, supplementary information taken from stud-ies of Africanized honeybees was added.

Most the data were obtained via a pollenanalysis of the food collected by bees. In thesecases, we selected only plant species with apollen representativity exceeding 10%, or fromthe pollen categories "frequent" (5-30%), "abun-dant" (> 30%), "secondary" (15-45%), and "pre-dominant" (> 45%), in accordance with classifi-cation schemes used by various authors

(Iwama and Melhem, 1979; Engel and Dinge-mans-Bakels, 1980; Sommeijer et al, 1983; Im-peratriz-Fonseca et al, 1984, 1987, 1989; Ra-malho et al, 1985, 1989; Kleinert-Giovanniniand Imperatriz-Fonseca, 1987; Ramalho, 1987;Cortopassi-Laurino and Ramalho, 1988). Absy’sstudies (Absy and Kerr, 1977; Absy et al, 1980,1984) provided us with the plant species mostfrequently found in pollen and nectar samples,those most persistent throughout the year (innumber of months), or those visited by the larg-est number of stingless bees. Roubik et al’sstudy (1986) provided us with references to theplant species "heavily" utilized by bees for pol-len. A few field studies were used to list plantspecies visited by > 5% of the total number ofindividuals of some species of stingless bee andAfricanized honeybee on flowers (Sakagami

and Laroca, 1971; Orth, 1983; Knoll, 1985; Knolland Imperatriz-Fonseca, 1987; Almeida and La-roca, 1988; Knoll, 1990).

RESULTS AND DISCUSSION

The data on flower visiting by species ofstingless bees and Africanized honeybee(Apis mellifera L) in neotropical habitatsare summarized in table I. Of the 23 stud-ies mentioned, 5 compare Africanized hon-eybee and stingless bees, and a further 6compare Melipona and Trigonini. In 6 ofthe studies, there is information on Melipo-na alone, and in 9 others, the informationconcerns only Trigonini. The data shown intable II are therefore biased as regards thenumber of plant species visited by the dif-ferent groups of bees, or by 2 or moregroups. The studies were conducted in ar-eas with different types of vegetation, influ-enced in some cases by the presence ofagriculture, pasture and or urbanization.Some studies were carried out in natural

forests, a very few in grasslands or savan-nah. Herbaceous species and shrubbery,both ruderal and opportunistic, albeit origi-nally under forest cover, are evidentlyabundant in areas with open vegetation.

Table II shows all the plant species withthe highest levels of representativity in thediet of these bees in accordance with the

quantitative studies listed in table I. Partic-

ularly in the case of the plant families ofgreatest significance for bees in neotropi-cal zones, some common trends in latitudi-nal distribution may be detected. Generallyspeaking, the families with a larger numberof species, ie Anacardiaceae, Compositae,Euphorbiaceae, Labiatae, Leguminosae,Melastomataceae, Moraceae, Myrtaceae,Palmae, Rubiaceae and Solanaceae, arealso the most consistent pollen and nectar

sources from the South of Brazil (SouthAmerica) up to the South of Mexico (NorthAmerica). In addition to the studies re-

ferred to in table I, some field studies (Sak-agami et al, 1967; Sakagami and Laroca,1971; Roubik, 1978; Laroca et al, 1982;Knoll, 1990), and an extensive survey ofthe principal pollen sources for Europeanand Africanized honeybees in the Centraland Western parts of Panama (Roubik etal, 1984) confirm this trend.

The families mentioned above comprise≈ 60 000 species. Except for Compositae,Labiatae and Leguminosae, with 25 000,3 000 and 17 000 species respectively, therest are mainly distributed in tropical andsubtropical regions all over the world (Joly,1977; Heywood, 1978). Species of Com-positae and Labiatae are very abundant inwoodlands, wooded grasslands, grasslandand bushland formations of South Ameri-

ca, but are poorly represented in the tropi-cal rain forests. Species of Caesalpinoi-deae and Mimosoideae (Leguminosae)are also more common in the tropics andsubtropics. The neotropics are distin-

guished as a zone in which Solanaceae isconcentrated, as the second largest con-centration of Euphorbiaceae and Palmae,and the main center for dispersion of Myr-taceae, together with Australia, as well as

being noted for the presence of Melasto-mataceae, one of the largest families in

South America.

Thus when a general view is taken, it isevident that the main pollen and nectarsources for stingless bees are to be foundamong the plant families which are bestrepresented in neotropical habitats. Re-

gional differences can be seen, nonethe-less. For example, the families Ericaceae,Labiatae and Polygonaceae are importantfor bees in the subtropics or in the zoneswhere the tropics meet the subtropics, asshown by studies conducted in the Southof Brazil (Sakagami and Laroca, 1971, La-

roca et al, 1982, Orth, 1983; Knoll, 1990).Compositae and Labiatae predominate asbee plants in areas with open vegetation,often under anthropic influence. Palmae ismore important in forested intertropicalzones.

The following genera were important forboth stingless bees and Africanized honey-bees virtually over the entire neotropicalzone: Alchornea, Baccharis, Cassia, Ce-cropia, Croton, Euphorbia, Miconia, Mimo-sa, Piptadenia, Solanum, Tibouchina, Tre-ma and Vernonia. The importance of

Cecropia (Moraceae) is surprising in viewof the supposedly anemophilous nature ofthis group, which is commonly found at theforest edge, on river banks, and in secon-dary forests throughout the neotropicalzone. Piptadenia seems to be especiallyimportant for bees on the Atlantic coast ofSouth America, from the South to theNortheast of Brazil. Other native generafrequently cited in the literature and whichare regionally important are: Spondias(Anacardiaceae), Protium (Burseraceae),Euphorbia (Euphorbiaceae), Byrsonima(Malpighiaceae) and Eugenia (Myrtaceae).

Out of a total of approximately 288 plantspecies, 126, 52 and 25 plant specieswere important solely for Trigonini, Melipo-na and Africanized honeybee respectively.Fifty-three plant species were importantboth for Trigonini and Melipona. It shouldbe noted that the information available for

Melipona covers 13 species as opposed tothat for Trigonini, which covers 36 species,so that the data are biased in favor of thelatter group of bees. Finally, 58 specieswere simultaneously important for African-ized honeybees and stingless bees. In thiscase, there is an evident underestimationof the number of plant species that are im-portant for both bee groups, in view of thesmall number of comparative studies (tableI). Be that as it may, when only compara-tive studies are considered, Trigonini may

appear to be a more generalistic flower vis-itor than Melipona (Roubik, 1978; Orth,1983; Knoll, 1990; and table II). Roubik

(1978) also notes that Trigonini seem to bea more generalistic flower visitor than Afri-canized honeybees in forest and savannahabitats of Amazonia.

Preferential relationships of stinglessbees with some plant families also seempossible (table II). If the frequency withwhich plant families are important in thevarious habitats or areas under study (ta-ble I) is considered, the following overallpicture emerges: the families Legumino-sae, Myrtaceae, Palmae and Rubiaceaeare important for Africanized honeybees,Trigonini and Melipona; Anacardiaceae,Balsaminaceae, Compositae, Euphorbia-ceae, Labiatae, Moraceae, Proteaceaeand Sterculiaceae are more important forAfricanized honeybees and Trigonini thanfor Melipona; Ericaceae, Liliaceae and Um-belliferae are more important for Trigoninithan for Africanized honeybees and Meli-pona; Mimosoideae (Leguminosae), Me-

lastomataceae, and Solanaceae are moreimportant for Melipona than for Africanizedhoneybees and Trigonini. This kind of defi-nition is obviously circumstantial and hasto be experimentally verified.

Stingless bees have perennial colonieswith specific populations of varying size

but, with some exceptions (eg some spe-cies of Trigona), far smaller than those ofAfricanized honeybee colonies. Seen froma cost-benefit angle, for stingless bee colo-nies of a small size, it is an advantage toexploit flowers less frequently visited bythose with a larger population, while for thelatter it may well be that the adoption ofstrategies which give them more of a com-petitive edge in productive resources

(Johnson and Hubbell, 1974, 1975; Hub-bell and Johnson, 1978) is their mainmethod for meeting their energy needs.Thus it is no surprise to find that in a given

local context most of the food is obtainedfrom only a few plant groups (table I), de-spite the huge number of important floralsources available on a regional scale andthe vast plant diversity in tropical foresthabitats (even when subject to anthropicinfluence).

As regards the impact of Africanized

honeybees on neotropical bee plants, andparticularly on stingless bees, there are

forecasts of local extinction (Roubik, 1978;Roubik et al, 1986). Roubik (1989) admitsthat "Africanized honeybees seem prea-dapted to invade and persist in mosaic

tropical habitats which gives them advan-tages over native bees", mostly owing totheir generalized nesting habits. Thesebees are also better adapted than Europe-an honeybees to foraging in conditions oflow nectar availability (Rinderer et al,1984, 1985), a situation which can be com-mon at the forest edge and in open areaswith unmanaged flora in the neotropics.Stingless bees are particularly abundant inregions of rain forest and subhumid forestzones of the neotropics, and are evidentlyadapted to the seasonal or apparently un-foreseeable rhythms of flowering and vari-ations in floral composition (as part of thehigh degree of diversity) in relatively closeareas within neotropical forest habitats. Itis not yet clear whether in such habitatsthe basis and pattern of food supply favorsthe Africanized honeybee’s foraging strate-gies, although countless native plant spe-cies are important food sources for this

bee.

ACKNOWLEDGMENTS

We wish to thank Mrs TC Giannini for helpin elaborating the table.

Résumé - Les plantes mellifères impor-tantes pour les abeilles sans aiguillon(mélipones et trigones) et les abeillesafricanisées dans les régions néotropi-cales : une synthèse. Cet article pré-sente une synthèse des sources de nectaret de pollen pour les abeilles sans aiguil-lon dans les régions néotropicales (Amé-rique du Sud, sauf Patagonie et Amériquecentrale). Seules ont été prises en compteles informations quantitatives concernantles visites de fleurs, ce qui permet de com-parer la valeur des sources florales spéci-fiques pour les abeilles sans aiguillon et

les abeilles africanisées (tableau I). La plu-part des données ont été obtenues parl’analyse pollinique de la nourriture récol-tée par les abeilles. Quelques études deterrain ont été utilisées pour les listes de

plantes visitées par les 2 groupesd’abeilles. Les études ont été faites dansdes régions avec des types de végétationvariés, influencés parfois par la présenced’agriculture, de prairies ou parl’urbanisation. Certaines ont été menéesdans des forêts naturelles, très peu dansdes régions d’herbages ou de savane.

Les familles botaniques suivantes :

Anacardiacées, Composées, Euphorbia-cées, Labiacées, Légumineuses, Mélasto-matacées, Moracées, Myrtacées, Pal-

mées, Rubiacées et Solanacées, quirenferment le plus grand nombre

d’espèces importantes, à la fois pour lesabeilles sans aiguillon et les abeilles afri-canisées (tableau II), sont aussi parmicelles qui présentent la plus grande diver-sité dans les habitats néotropicaux. Lesgenres Alchornea, Baccharis, Cassia, Ce-cropia, Croton, Euphorbia, Miconia, Mimo-sa, Piptadenia, Solanum, Tibouchina, Tre-ma et Vernonia sont importants pour les 2groupes d’abeilles dans pratiquementtoute la zone néotropicale.

Sur un total de 288 espèces de plantes,126, 52 et 25 sont importantes pour uni-

quement les trigones, les mélipones et lesabeilles africanisées, respectivement. Cin-quante trois espèces sont importantespour les trigones et les mélipones à la fois.Les informations disponibles pour les méli-pones couvrent 13 espèces, alors qu’ellesen couvrent 36 pour les trigones; les don-nées sont donc biaisées en faveur de cesdernières. Comme cela peut toujours seproduire quand on ne fait que des étudescomparatives, les trigones semblent êtreplus généralistes que les mélipones dansleurs visites de fleurs. Cinquante huit

espèces sont importantes pour les 2

groupes d’abeilles, abeilles sans aiguillonet abeilles africanisés. Il y a une sous-estimation évidente du nombre d’espècesimportantes pour les 2 groupes, étant don-né le faible nombre d’études comparatives(tableau I).

En ce qui concerne l’impact des abeillesafricanisées sur les plantes mellifères néo-tropicales et en particulier sur les abeillessans aiguillon, on peut prévoir l’extinctionlocale de plantes données. Mais l’on nesait pas encore si la base et les modalitésde l’offre de nourriture dans les habitats fo-restiers néotropicaux favorisent les straté-gies de butinage des abeilles africanisées,bien que de nombreuses espèces de

plantes indigènes soient d’importantessources de nourriture pour ces abeilles.

abeille africanisée / Melipona / Trigoni-ni/ plante mellifère / région néotropi-cale

Zusammenfassung - Wichtige Tracht-pflanzen für Stachellose Bienen (Meli-ponen und Trigonen) und für Afrikani-sierte Bienen an neotropischen Stan-dorten : Eine Übersicht. Diese Arbeitbietet eine Übersicht über die Pollen- undNektarquellen von Stachellosen Bienen anneotropischen (= südamerikanischen)

Standorten. Es wurden nur zahlenmäßigeInformationen über den Blütenbesuch

berücksichtigt, wodurch ein Vergleich desWertes spezifischer Trachtblüten für Sta-chellose Bienen und für Afrikanisierte Hon-

igbienen möglich wird (Tabelle I). Die meis-ten Daten wurden durch die Pollenanalyseder von den Bienen gesammelten Nahrunggewonnen. Außerdem wurden einige Feld-beobachtungen zur Aufstellung von Listender von beiden Bienengruppen besuchtenPflanzenarten herangezogen. Die Untersu-chungen wurden in Gebieten mit unter-

schiedlicher Vegetation durchgeführt, in ei-nigen Fällen beeinflußt durch landwirts-

chaftliche Nutzung, Viehweide oder

städtische Siedlungen. Andere wurden in

ursprünglichen Wäldern durchgeführt undsehr wenige in Gebieten mit Grasland oderSavanne.

Die Pflanzenfamilien Anacardiaceen,Compositen, Euphorbiaceen, Labiaten, Le-guminosen, Melastomataceen, Moraceen,Myrtaceen, Palmae, Rubiaceen und Sola-naceen enthalten einerseits die größteZahl wichtiger Arten sowohl für die Sta-chellosen wie für die Afrikanisierten Bienen

(Tabelle II), anderseits zeigen sie aber diegrößte Vielfalt an neotropischen Standor-ten. Die Gattungen Alchorea, Baccharis,Cassia, Cecropia, Croton, Euphorbia, Mi-conia, Mimosa, Piptadenia, Solanum, Ti-

bouchina, Trema und Vernonia sind fürbeide Bienengruppen in praktisch der ge-samten neotropischen Zone wichtig.

Aus einer Gesamtheit von 288 Pflan-zenarten sind 126 ausschließlich für die

Trigonen von Bedeutung, 52 nur für Meli-ponen und 25 nur für Honigbienen. 53 Art-en sind sowohl für Trigonen wie für Melipo-nen wichtig. Die zur Verfügung stehendenInformationen über Meliponen beziehensich auf 13 Arten, diejenigen über Trigo-nen jedoch auf 36 Arten, so daß diese

Gruppe in unseren Daten stärker vertretenist. Wie immer es sich verhalten mag,

wenn man nur die Vergleichsstudien he-ranzieht, so ergibt sich, daß die Trigonenbeim Blütenbesuch stärkere Generalistensind als die Meliponen. Für beide Bienen-gruppen, Stachellose Bienen und Afrikani-sierte Honigbienen, waren 58 Pflanzenart-en gleichermaßen wichtige Trachtquellen.Es besteht eine deutliche Unterschätzungder Zahl von Trachtpflanzen, die für beideGruppen von Bedeutung sind, besonderswenn man die geringe Zahl vergleichenderStudien berücksichtigt (Tabelle I).Was die Auswirkungen der Afrikanisier-

ten Honigbienen auf neotropische Bie-

nenpflanzen und besonders auf die heimis-chen Stachellosen Bienen betrifft, so gibtes Voraussagen für ein lokales Aussterbenbestimmter Arten. Aber es ist noch keines-

wegs klar, ob die Basis und das Musterdes Nahrungsangebots in neotropischenWaldstandorten die Sammelstrategie Afri-kanisierter Bienen begünstigt. Es ist zu be-denken, daß dieser Biene zahllose heimi-sche Pflanzenarten als wichtige Nahrung-squellen zur Verfügung stehen.

Afrikanisierte Biene / Melipona / Trigoni-ni / Bienenpflanzen / neotropische Zone

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